Parallel visual pathways: A review

PARALLEL VISUAL PATHWAYS: A REVIEW PETER LMNIE Centre for Research in Perception and Cognition, Laboratory of Experimental Psychology. University of Sussex, Brighton BNI 9QG. England

INTRODUCTION the last fifteen years it has become clear that the principal visual pathway in higher mammals, which connects the retina to the cortex via the dorsal lateral geniculate nucleus (LGNd), may fruitfully be regarded as a group of parallel pathways, each containing neurons that have distinctive physiological properties and which presumably contribute distinctively to vision. The aims of this paper are first, to examine the properties that characterize the neurons of the different classes and to understand what mechanisms might underly the differences; second, to trace the major Within

central projection of the different cell types; third, to try to understand their significance for seeing The work to be discussed concerns primarily the cat and the macaque monkey, for the visual organization of the former is best understood, and the visual organization of the latter is of greatest relevance to human vision. Related observations made on other species will be mentioned in passing This is not an historical review; for clarity of exposition the chronology of discovery has in several places been corrupted.

GANGLION Background

Kuffler (1953) gave the first systematic description of the receptive fields of ganglion cells in the cat’s retina He recorded from cell bodies, and all those he studied had receptive fields organized in one of two ways: the receptive fields of “on-centre” cells contained a central region, within which increases in illumination caused an increased discharge of impulses, enclosed by an annular surrounding region of lower sensitivity that whenilluminated brought about a decrease in discharge, or reduced the increase that would have arisen from illumination of the central part of the receptive field. In “off-centre” cells the polarity of sensitivities was reversed but otherwise the two types of ceil seemed to have similar properties. Hubel and Wiesel (1960) later found that most optic tract fibres in the spider monkey had substantially the same receptive field organization as ganglion cells of the cat, although a few units had unusual receptive fields. The uniformity of receptive field properties is, with hindsight, surprising since the great morphological diversity of ganglion cells had been shown clearly by Cajal(l893). All this diversity is unlikely to be needed for the provision of complementary cell types (onand off-centre), although some of it might be (Nelson et al., 1978). It is perhaps worth pointing out that, whatever varieties of ganglion cells are ultimately recognized, complementary sub-types will probably be recognized in each class, or cells of a particular type will respond identically to incremental and decV.I.

rn'l--*

CELLS

remental stimuli for only by having complementary types can a class of cells be sensitive to increments and decrements in illumination over a wide range. Some morphologically distinct cell types might have no counterparts in physiology, but it seems more likely that microelectrodes record the activity of only certain types of cell and/or that the physiological differences between cell types are not easily revealed. Selection by electrode Kuffler supposed that his platinum electrodes preferentially recorded the activity of large ganglion cells. This- selectivity was proved by Wiesel (1960), who recorded the activity ‘of ganglion cells in one region of the cat’s retina with both micropipettes and platinum electrodes, and found with pipettes units that had smaller centres in their receptive fields. Stone (1973) made further comparisons of electrode types, and showed that cells with slower-conducting.axons (presumably smaller) were discriminated against by electrodes of low impedance. One important observation made by Stone was that a bias in favour of cells with fast-conducting axons is heightened when recordings are made from (unmyelinated) axons in the retina to the extent that the activity of the slowestconducting axons was almost never recorded. Some of Stone’s conclusions were sharply challenged by Levick and Cleland (1974) who point out that biases can be reduced with carefully-made electrodes, but the disagreement still underlines the point that different electrodes prefer different cells. There seems little doubt that the thinnest fibres in 561

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the optic nerve and tract are seldom encountered by the microelectrode, and that. until recent refinements in technique, the smallest cells in the cat’s retina also escaped attention. These problems are probably aggravated in the monkey, where cell bodies and axons are smaller.

the receptive field, and that the signals from receptors are proportional to the illumination falling on them: when a pattern is in the “null” position, and can be exchanged silently for a uniform field, the signals arising from all points in the receptive field sum to zero. In a symmetrical receptive field, like that of a ganglion cell, the silent exchange will occur when the gratPliysiological subtlety ing is placed in odd symmetry about a diameter of the As will become clear later, the small cells with thin receptive field. The silent exchange does not require axons commonly have unfamiliar receptive fields, but the cancellation of signals in the centre of the recep they probably account for only part of the morphotive field by those in the surround, for an X-cell comlogical diversity, much of which is probably reflected monly will respond to modulation of a uniform field in more subtle. but nonetheless real, distinctions that covering both centre and surround (since these mechcan be drawn between types of cells that have concenanisms may have different latencies and one may be trically organized receptive fields. Before dealing with stronger than the other). Rather, the exchange is silent these, however, we have to solve some terminological for both centre and surround; neither mechanism difficulties. generates a response. Linearity of spatial summation implies nothing about the way in which the responses Terminology of the cell are related to the sum of the incoming Recent work from different laboratories is in gensignals; indeed, Enroth-Cugell and Robson showed eral agreement about the characteristics that disthat for both X-cells and Y-cells the amplitude of retinguish one type of cell from another, although this sponse was not linearly related to stimulus contrast agreement is disguised by different nomenclatures over any substantial range. (The relationship is char(see, for example, Rowe and Stone, 1977; Hughes, acterized more fully in Robson, 1975.3 1979; Rowe and Stone, 1979). In the following disX- and Y-cells were also distinguished by their cussion I have used a uniform terminology which on different responses to sinusoidal grating patterns that the whole reflects the most common current usage moved steadily across their receptive fields in a direcand have indicated, where appropriate, what are the tion perpendicular to the orientation of the bars. To terms (if different) used by the investigator whose patterns of all spatial frequencies X-cells responded with a discharge modulated about a steady mean; work is being discussed. The most difficult problem of terminology hinges Y-cells responded to most spatial frequencies with a not upon the vocabularies used by investigators large increase in average discharge rate, upon which working on the same species, for it is usually possible modulated responses were superimposed. At high spato establish whether differently named cells have the tial frequencies the responses of Y-cells were often same properties, but upon the application of the same unmodulated. The clearest evidence for the existence in the taxonomic groupings to cells in different species. I have tried throughout this review to apply the same macaque of units with the properties of X- and Y-cells names to cells in different species only if like-named comes from the work of de Monasterio et al. (1976) cells in different species would be physiologically inand de Monasterio (1978a), who showed by the applidistinguishable or nearly so. cation of a “null” test analogous to that used by Enroth-Cugell and Robson (1966) that the population of ganglion ceils that have concentrically organized X- and Y-cells receptive fields can be dichotomized as having linear spatial summation (X-like) or non-linear summation The first and clearest distinction between types of cells that have classical (concentrically organized) (Y-like). Fortunately, a division into X-like and Y-like receptive fields was drawn by Enroth-Cugell and cells can be related to older systems of classification. Robson (1966) from experiments in which they studOne well-established scheme, introduced by Wiesel ied the responses of on- and off-centre optic tract and Hubel (1966) to classify units in the macaque’s fibres to the exchange of a pattern. whose luminance LGNd, and since adopted by de Monasterio (1978a) in one dimension was modulated sinusoidally, for a for classification of ganglion cells, is based upon the uniform field of the same average luminance. For arrangement of spatially and spectrally antagonistic some’cells (“X-cells”) the grating pattern could be regions in the receptive field. I shall use it here positioned’s0 that the exchange evoked no response because, although it can be subsumed by the X-Y from the cell-it was “silent”; for the remaining cells classification, it draws attention to some important (“Y-cells”) no position of the grating pattern permitdifferences between properties of cells in the cat and ted a silent exchange, and the cells usually responded monkey. to both the introduction and the withdrawal of the Type I cells have receptive fields with centres that grating. receive inputs from one cone type and surrounds that These experiments prove that an X-cell responds to receive inputs from a different type (or types). Their the sum of signals about illumination from all parts of receptive fields can be mapped using spots of white

Parallel visual p&hVays

light but not usually with spots of a single colour. These units show linear spatial summation and respond to moving gratings of different spatial frequencies with a discharge modulated about a constant mean (de Monasterio. 1978a). Their spatial properties are therefore very like those of X-cells in the cat, although the fact of di&rent spectral sensitivities in centre and surround of the type Xcell raises the question of whether the two cell types are functionally homologous. I make the provisional assumption that they are because, by tests made with achromatic stimuli- type I cells in the monkey would probably be distinguishable from X-cells in the cat only by their smaller receptive fields. Moreover, for some of the type I units near the fovea the colour-opponency might be a trivial consequence of input to the centre of the receptive field arising from a single cone. de Monasterio found that units showing non-linear spatial summation comprise two classes, types IfI and TV.The receptive fields of type 211units are concentrically organized but oentre and surround receive inputs from the same cone type or types, which makes then very like Y-cells in the cat. The centres of type IV receptive fields recive inputs from two or three types of cone but the surround receives inputs from only one of these (usually red). The surround in some units is purely suppressive, but in others it can generate ““off” discharges. The latter units (apparently the more common kind in the retina) therefore have coIour-opponent receptive fields. Like Y-cells in the cat, cell types III and IV respond with a modulated discharge to gratings of low spatial frequency, and with an ~rn~~lated steady discharge to gratings of higher spatial frequency (de Monasterio, 1978a). By preferentially light-adapting the surround of a type IV receptive field with red light, de Monasterio (1978a) was able to show that the mechanisms responsible for the distinctive Y-like behaviour reside mainly in the surround of the receptive field By the criterion of linearity of spatial summation, both X-cells (an appreciable number of which have colour-opponent receptive fields) and Y-cells are found in the retina of the rabbit (Caldwell and Daw, 1978). Since they have been found in the LGNd of the rat (Lennie and Perry, 198g), they presumably exist in its retina too. Shapley and Gordon (19%) found X-cells in the eel3 retina, and also units that had non-linear spatial summation within their receptive fields, but of a kind uncharacteristic of Y-cells. Since we have so far defmed Y-cells by exclusion (as units with non-linear spatial summation) we need to refine our scheme of classification if we are to admit units that are neither X- nor Y-cells.

The Rariiaeuity

of tBe Y-e&l

&&stein and Shapley (f976a,b) have given the cltarest analysis of the non-linear spatial summation in the receptive fields of Y-&s iri cat. Frey shod

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first (1976a) that optic-tract fibres can be dichotomixed without ambiguity as X or Y on the basis of their responses to a modified “null” test. The classification relies upon the analysis of responses to stationary sinusoidal grating patterns whose contrast is modulated sinusoidally in time: the amplitude of the modulated response of a cell varies with the position of the grating on the receptive geld &eaer&y the largest responses arise when the grating lies in even symmetry about the centre of the renptive field) and for X-cells but not Y-cells a “null” position is easily found. The discharges of Y-cells are modulated to some extent whatever the position of the grating, Hochstein and Shapley (1976a) showed by Fourier analysis of responses of X- and Y-cells that sensitivity, calculated from the component of response at the modulating frequency (f,), varied sinusoidally with the position of the gating upon the receptive field. This component was the only substantial one in the responses of X-cells, as would be expected from mechanisms 6th linear spatial summation However, Y-cells showed, in addition to this, an appreciable sensitivity calculated from the response component at twice the frequency of modulation (fi), and this was quite independent of spatial position. Hochstein and Shapley used the ratio of the two sensitivities f2/f as a means of identifying X- and Y-cells: X-cells were defined as those for which the ratio (measured for gratings of optimal and higher spatial frequencies) was less than 1 and Y-cells those for which the ratio was greater than 1. This definition places undue emphasis on linearity of spatial summation as the property that most distinguishes X- from Y-cells-as we shall see shortly, they are d~stinguish~ by other properties too-but it is a useful and reliable means of difftrentiating the two classes. Hochstein and Shapley (1976b) then investigated the mechanism that generates the f2 (second harmonic) component that characterizes the responses of Y-cells. They established that the mechanism is insensitive to the spatial phase of the grating pattern used to elicit responses, that it responds to patterns of higher spatial frequency than can be resolved by the central region of the receptive field and that it is distributed throu~out the classical receptive Geld and beyond it. To explain these observations Hochstein and Shap ley (1976b) postulated a population of rectifying “subunits*’ distributed throughout and possibly beyond the classical receptive field. Each subunit sums signals from photoreceptors over an area smaller than the’centre of the classical receptive field, but only responds by tending to increase the discharge. Whether an individual subunit provides whole-wave rectification (i.e. causes an increased discharge in response to both increases and decreases in jll~minat~on) or half-wave recti&ation lie. responds but to an increase or to a decrease in i~u~at~on, not both) is not known. Because subunits are supposed dispersed throughout the reoeptive field, a

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moving grating pattern will evoke in the population activity quite different from that seen when the contrast of a stationary grating is modulated in time: in the latter case all subunits are stimulated in the same temporal phase (or in antiphase, which is equivalent) and therefore give rise to a modulated discharge. Subunits stimulated by moving gratings are not activated synchronously, so the response of the population as a whole will be unmodulated, which results in the relatively steady.$evatiofi of the average discharge. X-cells evidently differ fundamentally from Y-cells, although this difference is difficult to discern when receptive fields are explored casually with spots of light. Hochstein and Shapley undertook quite complicated experiments to reveal the properties of the rectifying subunits that characterize Y-cells, so it is worth asking if X- and Y-cells can be distinguished by other means too. Time-course of response

Cleland et al. (1971, 1973) described, for cat, several behaviours that permitted the division, into two groups, of most ganglion cells that had concentrically organized receptive fields. One was the response to moving grating patterns. Cleland et al. (1971) found, as had Enroth-Cugell and Robson (1966), that one group of cells responded with a discharge modulated about a steady mean, while the other responded to gratings of high spatial frequencies with an increase in steady discharge. These groups almost certainly correspond, respectively, to X- and Y-cells, but Cleland et al. (1971) preferred different names that emphasized other characteristic properties. A spot that just fills the centre of the receptive field stimulates X- and Y-cells very effectively. Cleland et al. found that at moderate levels of background illumination the time-course of discharge following the onset of an incremental, spot (on-centre cells) or decremental spot (off-centre units) differed in X- and Y-cells, that of X-cells decaying less rapidly. These different time-courses of response led Cleland et al. to introduce the terms “sustained” and “transient” to characterize the two cell types. This new terminology found wide acceptance and was absorbed readily by psychophysicists anxious to find perceptual correlates of the two cell types, but it has now become clear that it emphasizes aspects of response that may not always distinguish X-cells from Y-cells. An important difficulty with the sustained/transient distinction is that the time-course of discharge to a centrally located spot depends upon the level of lightadapt’ation (Yoon, 1972; Enroth-Cugell and Shapley, 1973a): the more light-adapted the cell, the more transient the response. Enroth-Cugell and Shapley (1973b) showed that the level of light-adaptation (expressed as the extent to which dark-adapted sensitivity had been reduced) is determined by the number of photons absorbed from the background falling within the centre of the receptive field. Thus, at any one level of background illumination, cells with larger central areas in

their receptive fields are more light-adapted than units with smaller central areas, and so give more transient responses. At any one retinal eccentricity Y-cr$s have larger central areas in their receptive fields (see p. 566) SO, by virtue of this property alone they generate more transient responses. When X- and Y-cells are equally light-adapted, spots of moderate suprathreshold luminance evoke responses of very similar time-courses (Jakiela et al., 1976). A second problem is that units with more peripheral receptive fields (whether X or Y) tend to generate more transient responses (Cleland and Levick, 1974a; Hochstein and Shapley, 1976a). Since Y-cells are more commonly encountered in recordings made from peripheral retina, and X-cells in recordings from central retina (see p. 570), as a group Y-cells will generally give more transient responses. The third difficulty is the most interesting. The degree to which Y-cells give more transient responses than X-cells depends upon the contrast of the stimulus used to elicit the response: the time-courses of weak responses obtained from X- and Y-cells are little different (Lennie, 1980X but as contrast is increased Y-cells become appreciably less responsive to stimuli of low temporal frequency (i.e. their responses become more transient) (Shapley and Victor, 1978). One factor that promotes this is the poor sensitivity of subunits to low temporal frequencies. Their contribution to the overall discharge of a Y-cell is very transient, and the amplitude of their response seems, over some range, to be a positively accelerated function of stimulus contrast. The same subunits also seem to act covertly via the “contrast gain control” (Shapiey and Victor, 1978) to improve the sensitivity of ganglion cells to medium and high, but not low, temporal frequencies as the contrast of stimulating patterns is raised. This mechanism is much stronger in Y-cells and brings about progressively more transient responses as stimulus contrast is increased. A distinction related to the sustained/transient one was drawn independently by Fukada (1971). who described units of type I (Y, transient) and type II (X, sustained). (This classification is quite unrelated to that drawn between cells of types I and II in the monkey.) His optic tract fibres were segregated by their responses to diffuse illumination of the receptive field. Type I units generally responded well to both onset and offset of illumination, and gave transient responses to small spots; type II units (with one exception all on-centre units) responded weakly to the onset of diffuse illumination and were especially unresponsive to its offset. Their responses to small spots were more sustained. Fukada’s test probably segregated X- and Y-cells quite effectively, and it can be used with some sensitivity when the amplitude of flicker is low (Tobin, 1976). Gouras (1968) described “tonic” and “phasic” ganglion cells in the rhesus monkey’s retina. Receptive fields of “tonic” cells pose-ssed a colour-opponent organization but those of “phasic” cells did not. What

Parallcl visual pathways seems to be essentially the same distinction has been drawn by Schiller and Malpeli (1977a), who describe “colour-opponent” cells that respond tonically to maintained contrast in the receptive field and “broadband” cells that lack colour-opponent organization and respond transiently to maintained contrast. In this respect the “tonic” cells resemble X-cells and the “phasic” ones Y-cells. However, de Monasterio’s (1978a) later work suggests that, although t* I (X-like) cells generally give more sustained responses than types III or IV (which are Y-like), the time course of response does not reliably distinguish cell types. X- and Y-cells in the rabbit are also hard to distinguish by the time-courses of their responses to stimuli of long duration (Caldwell and Daw, 1978). Flicker sensitivity The temporal properties of ganglion cells can be thoroughly characterized by measurement of their sensitivity to spots or gratings that flicker on the receptive field. Fukada and Saito (1971) stimulated cat ganglion cells with small spots flickering in the centres of the receptive fields and found that X-cells generally followed flicker to higher frquencies. Moreover, at intermediate temporal frequencies, the responses of X-cells were modulated about a fairly constant mean rate while those of Y-cells were accompanied by an appreciable increase in unmodulated discharge. Fukada and Saito also found that some Y-cells, when stimulated by flicker at a certain critical frequency (between 10 and 3OHz), began to discharge impulses repetitively at around 200 Hz. Normal responses to the flickering stimulus were superimposed upon this “induced activity”. Granit (1978) discusses possible explanations of this phenomenon. The raised average discharge rate of Y-cells that results from stimulation at intermediate temporal frequencies is almost certainly brought about by rectifying subunits. These subunits are quite insensitive to low and high rates of flicker, and are most sensitive to frequencies between 5 and 8 Hz (Shapley and Victor, 1978). Shaplcy and Victor (1978) have characterized the temporal properties of X- and Y-cells in the cat by analyzing responses to station sinusoidal gratings whose contrast was modufated by several temporal sinusoids. Their experiments show that, for weak responses, the relation between sensitivity for the fi component of response and temporal frequency is very much the same in both X- and Y-cells. However, when stronger criterion responses arc required, Y-cells show a steeper decline in sensitivity as temporal frequency is reduced from the optimum (i.e. Y-cells are more transient). Measurements of temporal contrast sensitivity made with moving gratings (Lennie, 1980) show X- and Y-cells to be indistinguishabIe except at frequencies above about 40 Hz, where Y-ceils become slightly more sensitive. Since much has been made of the supposedly differ-

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ent temporal properties of X- and Y-cells it is probably worth emphasizing that, when both are stimulated by patterns of optimal spatial frequency at contrasts that give just reliable (“threshold”) responses, the temporal modulation sensitivity curves differ trivially. There are ‘no published measurements of the temporal modulation sensitivifies of the different classes of ganglion cell in the macaque. Sensitivity to speed of movement Cleland er al. (1971) found that Y-cells in cat responded better than did X-cells to the rapid movement of a disc (dark for on-centre units, light for offcentre ones) across the receptive field. The same is true for the rabbit (Caldwell and Daw. 1978). Sub units in the surround of the Y-cell’s receptive field are probably the source of the brief response when the stimulus moves fast, for Cleland and Levick found that X-cxlls in the cat are as responsive as Y-cells when the polarity of the disc is reversed (i.e. suited to the centre rather than the surround of the receptive field). When the cat’s ganglion cells are stimulated by moving gratings of optimal spatial frequency, Y-cells are very slightly more sensitive than X-cells at high velocities (Lennie, 1980), probably because they prefer stimuli of lower spatial frequency. Selectivity for size Two methods are widely used to characterize centre size. In one, the illumination required for a threshold response to a centrally placed spot is ptotted against spot size; centre size is commonly taken as the size of the smallest spot that gives the lowest threshold. By the second method, a “profile” of the centre is mapped by finding the threshold illumination for a small spot at a number of points along a diameter of the receptive field. Both methods may overestimate the size of the central region (the area covered by the linearly summating mechanism) of the receptive field of a Y-cell because the spots stimulate the rectifying subunits that are distributed throughout the receptive field. Subunits generate responses at both light onset and offset and thus contribute to the responses characteristic of both centre and surround. This cont~bution will be especially evident at parts of the receptive field where the principal mechanisms have relatively low sensitivity, and ought to result in the appearance of a large region where centre and surround overlap (cf. Enroth-Cugell and Lennie, 1975). This region may be so large as to give the impression that surround antagonism is relatively much weaker in Y-cells than in X-cells, but the measurements of Cleland et al. (1973) show that this is not the case. The contribution of subunits to the responses of Y-cells probably also explains why Ikeda and Wright (1972) found that the profiles of sensitivity in the receptive fields of “transient” cells had much shallower slopes than those of “sustained” c&s. Characteristically different distributions of sensi-

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tivity are found in the surrounds of X- and Y-cells, the latter showing an apparently greater extension into the middle of the receptive field (Cleland et al., 1973). This too can easily be explained by the action of subunits which, even in the middle of the receptive field. generate responses characteristic of the surround. How then should we characterize the size of the receptive fields of Y-cells? If Hochstein and Shapley’s hypothesis is correct (and it explains so many of the peculiarities of Y-cells that it is difficult to doubt it) the most reliable way to characterize the sizes of the centre and surround might be to adopt the technique used by Enroth-Cugell and Robson (1966) to describe the receptive fields of X-cells. This involved finding two Gaussian spectra (representing centre and surround) whose difference yielded the spatial contrast sensitivity curve derived from responses to moving gratings. Unfortunately, no such estimates exist, but measurements made by the other methods show that in the central retina the centres of receptive fields of X-cells have diameters of around 0.5” or less and Y-cells about 1” (Cleland and Levick, 1974a; Stone and Fukuda, 1974a-whose values are lowest; Peichl and Wlssle, 1979). Peichl and Wassle’s extensive comparisons of centre size at different eccentricities show that at any one eccentricity the centre diameters of Y-cells are about 2.5 times those of X-cells and that for each cell type the range of diameters is small. Spatial properties of receptive fields of the monkey’s ganglion cells have been studied much less extensively. Gouras (1968) found that “tonic” cells in the rhesus monkey’s retina had larger receptive field centres than did “phasic” ones. However, later work (de Monasterio and Gouras, 1975) showed that the tonically responding “colour-opponent” cells (mostly, it seems, type I) had the smallest centres, whose diameters, mapped with small spots, increase very little with eccentricity within the central 20” of retina. Units receiving inputs from red or green cones have centre diameters of around 3.6min arc while diameters of those driven by blue cones are two to three times larger. This was, confirmed by de Monasterio (1978b). Type III and IV receptive fields have centres whose diameters increase with eccentricity: in the fovea the diameters are around 9 min arc; at 10 eccentricity, around 24min arc (de Monasterio and Gouras, 1975; de Monasterio, 1978b). Thus centre sizes of X-like and Y-like cells in the monkey differ by at least as much as they do in the cat. Possibly homologous “sustained” and “transient” ganglion cells in the tree shrew have correspondingly different centre sizes (van Dongen et al., 1976). Influence of remote stimulation

McIlwain (1964) found that movement of a small disc in the visual field, far from the classically defined receptive field of a cat’s ganglion cell, brought about a &all increase in steady discharge. This “periphery effect” does not result from light scattered within the

eye (Levick et al., 1965) so it must reflect some longranged neural interaction. The periphery effect is clearly seen in nearly all Y-cells, although it is never a substantial response; it is weak or absent in most X-cells (Cleland et al., 1971). A much more dramatic effect of peripheral stimulation was discovered by Kruger and Fischer (1973): a transient discharge, of peak amplitude up to IO0 impulses set- i can be elicited by abrupt movement of a grating that covers a large part of the recep tive field, but not the region containing the classical receptive field. This “shift effect” is, like McIlwain’s periphery effect, not a consequence of light scattered on to the classical receptive field, for its strength is undiminish~ by strong background lights that fall on the classical receptive field and markedly desensitize it (Barlow et al., 1977). Strong responses to shifts of gratings in the periphery are readily obtained from Y-cells but not X-cells (Barlow et al., 1977; Derring ton et al., 1979). These responses almost certainly arise from the same mechanism that generates the periphery effect (Fischer et al., 1975; Derrington et al., 1979) but are distinctive because abrupt movement of a grating activates the mechanism particularly well. The peripherally-evoked responses are generated by mechanisms that are insensitive to the spatial phase of the grating, have good spatial resolution and poor temporal resolution, and are distributed over a region that extends to at least 40” from the centre of the classical receptive field (Derrington et al., 1979). Moreover, the mechanisms have a true threshold and generate responses that saturate rapidly with increasing contrast (Barlow et af., 1977). These mechanisms have properties so like those of Hochstein and Shapley’s (1976b) subunits that Derrington er al. (1979) suggested they were the same. Thus, the distinctive non-linearities of Y-cells probably arise in mechanisms that are distributed densely over a large region centred on the classical receptive field. Peripherallyevoked responses are found in some X-cells, but they are invariably weak and more sluggish than those observed in Y-cells (Cleland et al., 1971; Barlow et al., 1977 ; Derrington et al., 1979). When stimulated by gratings remote from the classical receptive field, many optic tract fibres in the rhesus monkey respond like Y-cells in the cat, although less vigorously (Kruger et al., 1975). It is not clear to what classes these units belonged, but since recordings were made from optic tract Kruger et al. were more likely to have encountered units with larger axons. probably types III and IV (see p. 571). Caldwell and Daw (1978) found no clear “periphery effect” in the rabbit’s ganglion ceils. Since at best this effect is weak. it would be worthwhile to know whether X- and Y-cells can be distinguished by the more substantial “shift-effect”. Maintain&

discharge

The maintained discharge of an X-cell (on- or offcentre) in the cat’s retina is generally more rapid than

Parallel visual pathways that of a corresponding Y-ceil at the same (mesopic) background illumination (Cleland et al.. 1973; Stone and Fukuda, 1974a). The position in the monkey is similar. Gouras (1968) and Schiller and Malpeli (1977a) found that their coiour-opponent cells (among which X-Eke cells seem most commonly founds had more rapid maintained discharge than did nonopponent cells (probably type III and some type IV, Y-like cells). Summary The work just reviewed reveals a sharp and apparently fundamental distinction between the X- and Y-types of ganglion cell in cat. The distinction seems at least as clear in the macaque, though perhaps less so in the rabbit. One important point to emerge is that Y-cells are not just “non-linear” cells, but that they differ from X-cells in several ways (the form of the non-linearity, receptive field size and sensitivity to remote stimulation) that permit us to identify them positively. Although non-linear spatial summation is an important characteristic of Y-cells, we may quite properly talk of cells that have non-linear spatial summation but are nonetheless not Y-cells, if the non-linearity differs from that found in the receptive field of a Y-cell, or if other attributes (e.g. sensitivity to remote stimulation) are unlike those of Y-cells. By the same token, although linear spatial summation is an important characteristic of X-cells, cells that summate linearly need not be X-cells. Indeed, some ganglion cells in the monkey’s retina that show linear spatial summation are patently unlike X-cells in terms of the distribution of their spatial and spe.ctral sensitivities (see p. 569). The question then arises whether ceils with centresurround organized receptive fields can be exhaustively partitioned into X- and Y-classes.

Other Cells with Concentricaliy Organized Receptive Fields “Sluggish”

cells

Cleland and Levick (1974a) described units (about 12% in a sample of nearly 1000 studied in recordings from the cat’s retina) that had concentrically organized receptive fields, but had not been recognized in their earlier work (Cleland et al., 1971, 1973). These units, termed “sluggish”, were distinguished from the much more common “brisk” units by their low responsiveness (but not necessarily low sensitivity). Both classes of unit were further divided into “sustained“ and “transient” groups prin~pally on the basis of their responses to the onset of a steady spot (light or dark, as appropriate to cell type) centted upon the receptive field. There is little doubt that the “brisk-sustained” and “brisk-transient” units are those most commonly identified as X- and Y-cells. respect-

567

ively, but the status of “sluggish” units is less certain. They are probably not merely damaged specimens of “brisk’: units. Cleland and Levick provide impressive evidence (but make no claim) that sluggish cells cannot be Y-cells: sluggish cells have no periphery effect; they generally respond feebly to moving gratings, but with a modulated response to the highest spatial frequencies that can be resolved; a substantial number do not respond at all to gratings moving at rates (l-4 Hz) optimal for Y-cetls. Most sluggish celis have a “silent inhibitory surround” of the kind that can be demonstrated in Y-cells and less easily in X-cells (Jakiela, 1978; Shapley and Victor, 1979). Sluggish cells are not so easily distinguished from X-cells, although Cleland and Levick showed that the maintained discharge was often much lower and more regular than in X-cells and that centres of receptive fields (mapped with small spots) were on average appreciably larger. Some of the on-centre “sluggishsustained” units behaved like the “luminance unit” described by Barlow and Levick (1969). Cells with properties like those just described were also studied by Stone and Fukuda (1974a) and, less extensively, by Rowe and Stone.(1976), although differences in terminology tend to obscure the fact. Stone and his colleagues refer to these as “W-cells”, and further divide them into tonic and phasic types that correspond to Cleland and Levick’s “sluggishsustained” and “sluggish-tr~si~t” types. As with Cleland and Levick’s distinction, that drawn between the two types of W-cell is not convincingly demonstrated by their different responses to visual stimuli, although it seems to be bolstered by their different central projections (see p. 574). it seems likely that sluggish cells differ qualitatively from both X- and Y-cells. Measurements of the conduction velocities of axons (discussed shortly) suggest that many sluggish cells have small axons, which may explain why they are seldom found in recordings made from the optic tract. The issue of axon size raises the interesting possibility that the “sluggishness” of these cells merely reflects a limitation on their maximum discharge rates imposed by small axons. The minimum interval between successive impulses in myelinated fibres is almost inversely proportional to the conduction velocity of the fibre (Paintal, 1973; Jack, 1975). so sluggish cells would be expected to be less responsive than either X- or Y-cells. It is hard to know if there are units in the monkey that might be counterparts of sluggish cells in the cat. All units with centre-surround organized receptive fields seem to fall readily inro groups I, III or IV, and therefore have properties that make them more like X- or Y-cells (de Monasterio, 1978a). Caldwell and Daw (1978) found in the rabbit units like the sluggish ones in cat. These were disinguished from X- and Y-cells by their low rates of maintained discharge and by their poor responses to flickering

P.

568

LENSIE

patterns. Again the sub-types “sustained” and “transient” have been identified. Colour-opponent

cells (cat)

Cleland and Levick (1974b) found in the central area 5 units out of 73 studied that had both spatially and spectrally opponent receptive fields. (Bluesensitive cones provided the input to one mechanism and long-wavelength sensitive cones the input to the other.) These receptive fields had appreciably larger centres (c. 2” diameter) than did those of nearby X-cells, and the scotopic receptive fields seemed to be very much larger than the photopic ones, which is not the case for typical X- or Y-cells (Enroth-Cugell ec al., 1977b). Units like this may have evolved specially in species like the cat, where cone density, even in the area centralis, is very low (Steinberg et-al., 1973) and where blue-sensitive cones are probably extremely rare. Receptive Fields with Unusual Spatial Organizatiun

Some ganglion cells in cat and monkey have receptive fields that lack distinct centre and surround regions. “L.ocol edge detectors"/"on- off” unitsrexcited trast”

by con-

units

Despite different names assigned by different workers, there is good agreement on the physiological properties of these cells. The most commonly encountered type in the cat generally has a circular receptive field in which, at moderate levels of background illumination, a spot flashed on the centre gives rise to discharges, usually of equal strength, at both onset and offset. No antagonistic region can be discerned with spots or annuli but if spots larger than the central region are flashed on the receptive field responses are much weakened (Cleland and Levick, 1974b: Stone and Fukuda, 1974a). “On-off” cells have a low and regular maintained discharge and respond poorly to moving gratings of low spatial frequency; however, they can resolve fairly high spatial frequencies (3-6 c/deg). The response is much improved and becomes modulated at twice the rate of movement of the grating if the inhibitory surround is masked off to expose only the receptive field region that can be mapped with spots (Cleland and Levick, 1974b). In separate experiments Cleland and Levick investigated the resolving power of the inhibitory surround, and found it sensitive to gratings of spatial frequency 3-4 c/deg. Receptive field centres plotted with small spots are between 0.5 and 2’ in diameter and centre size does (Stone and Fukuda. 1974a). or does not (Cleland and Levick, 1974b) increase with eccentricity: sample sizes have been too small for the relationship to be characterized adequately. These units cannot be either X- or Y-ceils. but some

of their properties are strikingly reminiscent of those of the subunits that endow Y-cells with their distinctive non-linearities: transient, rectified responses and relatively high spatial resolution within a large receg tive field. Receptive fields might consist of collections of subunits without the classical centre and surround superimposed upon them. but since “on-off’ cells lack a periphery effect the arrangement of subunits is probably not the same as in the receptive field of a Y-cell. Little is known about similar receptive fields in the monkey. Schiller and Malpeli (1977a) described one unit that probably was of this type; de Monasterio (1978~) described the properties of a larger number of them (type Vb cells). These units. which have no spectrally opponent organization. give frequency-doubled (“on-off”) responses to stimuii flickering on the central parts of their receptive fields. Responses are diminished if stimuli also encroach upon a suppressive surrounding region. Type Vb units respond poorly to moving gratings of low spatial frequency but give frequency-doubled responses to moving gratings of higher spatial frequency; the latter responses occur in conjunction with a rise in the average discharge rate. Most of these properties are like those of -‘on-off” units in the cat. Some “on-off” cells that lack a suppressive surround have been described by de Monasterio and Gouras (1975) and by de Monasterio (1978~). but these have not certainly been identified as ganglion cells. “Local edge detectors” in the rabbit’s visual streak have been studied thoroughly by Levick (1967) and have also been seen by Caldwell and Daw (1978). Direction-selective

cells

In the cat these have been found by Stone and Fabian (1966) and Stone and Hoffmann (1972), and have been more extensively studied by Cleland and Levick (1974b) and Stone and Fukuda (1974a). Like the “on-off” cells they have a low maintained discharge and generally have circular receptive fields, within which spots shone on the centre elicit brief responses at both onset and offset. No surround region is exposed by flashing snots or annuli. but a powerful inhibition of responses to central stimulation is revealed when the region surrounding the receptive field is stimulated by grating patterns. This surround mechanism is not directionally selective and can resolve spatial frequencies of up to 3 c/deg. These units. as their name implies. are selective for the direction of motion of a target (darker or lighter than the background) passing through the centre of the receptive field at velocities of around 1 deg set- ‘. Movement in the opposite direction elicits no response, except at very low stimulus speeds. Cleland and Levick (1974b) found that moving gratings of spatial frequencies up to 3c/deg can be resolved by the central region of the receptive field. even though this region itself has a diameter averaging I ‘. Stone and Fukuda (1974a) found some direction selective

Parallel visual pathways cells that gave only “on” responses when spots were flashed on the centres of their receptive fields, and showed evidence of weaker inhibitory surrounds; it is unclear whether these units differ fundamentally from other direction-selective cells. No direction-selective cells have been found in the monkey’s retina, but they have been found in the grey squirrel (Cooper and Robson, 1966) the ground squirrel (Michael. 1968) and the rabbit, where they have been most thoroughly studied (Barlow ef al., 1964; Barlow and Levick, 1965; Wyatt and Daw, 1975). The commonest type of direction-selective units in the rabbit’s retina behave much like those in cat, but receptive fields are larger (c. 3’ in diameter), and units with “on-off” centres are responsive to faster-moving objects. These “on-off” direction-selective cells in the rabbit tend to prefer stimuli that move in directions approximately parallel to the line of action of one of the four rectus muscles (Oyster, 1968). Barlow and Levick (1965) were able to explain many aspects of the behaviour of the directionselective cells in the rabbit by postulating what are essentially “subunits” distributed throughout the central region of the receptive field. .These are supposed interconnected by inhibitory links only in the direction corresponding to that in which motion of an object gives a “null” response. Perhaps those “on-off” units that have directional selectivity differ in on1.y one fundamental aspect (the possession of polarized inhibitory connections between subunits) from the other “on-off” units described above. However, as Caldwell et al. (1978) point out. the two classes of cell may use different subunits, since they have different susceptibilities to the transmitter antagonists, picrotoxin and strychnine. uSu~presse~ by conmasr units”/~un~r~ity “edge-~n~ibirory offcentre units”

detectors”/

These units in the cat have in common the property that the presence of a contrast (especially in the form of a grating) within the receptive field markedly sup presses an otherwise healthy maintained discharge of up to 50imp set-’ (Rodieck. 1967; Stone and Hoffmann, 1972; Cleland and Levick, 1974b; Stone and Fukuda, 1974a). This suppression is very pronounced for patterns that move slowly through the receptive field, and it persists for some seconds if the pattern remains stationary; prolonged movement of a pattern can bring about a long-lasting suppression of discharge (Cleland and Levick. 1974b). The contrastinhibition mechanism has very fine spatial resolution (3-6 c/deg) and in this respect resembles the “contrast gain control” of X- and Y-cells (Shapley and Victor, 1978) and the “silent inhibitory surround” of “on-off” cells and direction-selective ones. The underlying mechanisms may all be the same. There is dispute about whether all units of this type can be grouped together. Cleland and Levick (1974b) subdivided them into “uniformity detectors” and “edge inhibitory otkentre units” principally because

569

the discharge of the latter, but not of the former. was suppressed only by light spots moving into the central part of the receptive field, and the receptive field mapped with spots had an “off” centre and an “on” surround. This subdivision is challenged by Rowe and Stone (1976). A few cells with properties resembling those just described were found by de Monasterio and Gouras (1975). de Monasterio (1978~) identified a class of ganglion cell (type VI) that is unresponsive to stationary stimuli flashing on the receptive fields and has a rapid maintained discharge that is inhibited by the movement (especially slow movement) of a slit of light across the receptive field. Similar units in the rabbit have been studied by Levick (1967). Colour-opponent units that iack spatial opponency wcaqu4 de Monasterio (1978~) found that 7 of 437 in his sample of ganglion cells had receptive fields in which two co-extensive antagonistic regions had different spectral sensitivities. These type II units (named after similar ones studied in the LGNd by Wiesel and Hubel, 1966) are unresponsive to achromatic stimuli of any kind, but linear spatial summation within the receptive field can be demonstrated by the use of coloured stimuli that excite either mechanism. Although linearity of spatial summation is an “X” property, type II cells are sharply distinguished from X-like cells (type I units) by the absence of spatial antagonism in their receptive fields, and by their poor responsiveness to acromatic stimuli.

Heterogeneity of Cell Types There are clear physiological grounds for distinguishing X-cells from’Y-cells, and probably for distinguishing both from the other cell types described above, but there is little agreement about whether the differences between cells of the other classes represent change along a continuum or are reflections of fundamentally different underlying mechanisms. By the use of distinctive names, Cleland and Levick (1974b) and Levick (1975) emphasize the differences between units. while Stone and his colleagues (e.g. Rowe and Stone, 1977), by their use of the “W-cell” umbrella, emphasize the similarities. Stone and Fukuda (1974a) in particular have drawn attention to a number of similarities between “on-off” units and the “phasic” cells (“sluggish-transient” units). I am impressed by the distinctive properties of the “sluggish” cells (“sluggish-sustained” and “sluggishtransient” units of Cleland and Levick and the “tonic” and “phasic” “W-cells” of Stone and Fukuda) but even some of these show behaviours in common with cells that have unfamiliar receptive fields. Several properties of the different classes give a strong suggestion of related underlying mechanisms-perhaps different arrangements of the same rectifying subunits.

We need much more systematic information about the properties of these cells-their spatial contrast sensitivity, temporal sensitivity and incrementai sensitivity-before satisfactory taxonomic groupings can be devised. The difficulty of recording from these ceils contributes substantially to the problems of classification, for only rarely can they be studied for the long periods needed for their properties to be characterized thoroughly. These problems are probably much worse in the monkey, where cell bodies and hbres are smaller.

Numbers and DlsniI~~dans of Different Phyalologleal Types The acknowledged selectivity of electrodes makes it hard to estimate from single unit records the numbers of cells of different types, but all workers are agreed that in the optic tract of cat Y-cells are most commonly encountered and units with unusual receptive fields are hardly ever found. Recordings made in the retina (Cleland and Levick, 1974a.b; Fukuda and Stone, 1974) show that X-cells are the ones most often found in the area centralis, with Y-cells more common in the periphery; units with unusual properties are relatively uniformly and sparsely distributed. There is evidence that in the peripheral part of the cat’s visual streak. so-called W-cells are the most common (Rowe and Stone, 1976). The distribution of receptive field types in the monkey’s retina is similarly uncertain. Cell bodies and axons are smaller than in the cat and sampling biases may be correspondingly more extreme. de Monasterio (1978a) found type I (X-like) units most frequently in the fovea (909,; of all units). with a progressively reduced frequency as eccentricity increased, althou~ up to lo” eccentricity they formed the largest fraction of units studied. Type III units, making up the bulk of the Y-like group, are rarely found in the fovea (70/i of units encountered by de Monasterio, 1978a). but are seen more often as eccentricity increases, and form the largest group (more than 65% of all units studied) at eccentricites between 10 and 20’. Type IV units are rare in the fovea, but constitute around 10% of the cells encountered at eccentricities beyond 2’. de Monasterio and Gouras (1975) had earlier found similar distributions of cell types, as did Schiller and MaIpeli (1977a). who classified cells into “colouropponent” (probably mostly type I) and “broadband” (probably types III and IV). Schiller and Malpeli’s sample of recordings from axons in the retina showed no differential distribution of unit types. which is not surprising. It would be unwise to suppose that the physiologically measured ditribution of cell types accurately represents the true distribution. Two methods have been used to estimate more reliably the numbers of cells of different types. By the first, conduction velocities of axons of cells of different physiolo~cal types are linked with the discrete con-

duction velocity groups discerned in the compound action potential recorded from the optic nerve; the numbers of fibres contributing to these groups can be deduced relatively straightforwardly. By the second method, a correlation is established between physiological cell type and morphological type, and cell bodies are counted in retinal whole-mounts. Conduction celocities of axons

Various measures of conduction speed show that Y-cells have the f~test-conducting axons in the optic nerve. Fukada (1971) found that the average conduction velocity of fibres classified as type I (Y) was 39.1 m set-’ whereas that of type II (X) was 26.1 m set- ‘, although the distributions overlapped substantially. The two classes of cells are more strikingly distinguished by measurements of the time taken for an antidromic pulse to travel from a point on the axon, usually in the optic tract, to the cell body. By this measure, which also reflects the speed of conduction by the unmyelinated fibres in the retina, the X- and Y-cells fall into discrete populations, Y-cells being faster (Cleland and Levick, 1974a; Stone and Fukuda, 1974a). A similarly sharp segregation is seen in conduction times from ganglion cell body to LGN (Cleland et ai.. 1971). Conduction times increase with distance of the cell body from the optic disc: for Y-cells there is a slight, for X-cells a pronounced, increase in the conduction times of units close to the area centralis (Stone and Fukuda, 1974a; Kirk et al., 1975b). “Sluggish” units of both “sustained” and “transient” types have longer conduction times that slightly overlap those of X-cells (Cleland and Levick, 1974a: Stone and Fukuda 1974a) but not those of Y-cells. “Sluggish-sustained” units have the shorter latencies (Kirk et al.. 1975a). Conduction times of units with unusual receptive fields are more variabIe, generally slow, and never overlap those of Y-cells. They are not always distinguishable from those of X-cells, especially in the area centralis. This is particularly true of the “colour-coded” units (Kirk et al.. 1975a). Antidromic conduction times of ganglion cells in the monkey’s retina were measured by Gouras (1969) (although his results are described as measurements of conduction velocities). His “phasic” (Y-like) units had shorter conduction times than did “tonic” (X-like) units. Later measurements by Schiller and Malpeli (1977a) and de Monasterio (1978a) characterized the differences more thoroughly: conduction times of type I (X-like) units to stimulation of the optic tract or chiasm are on average 1.7 times greater than those of Y-like units (types 111and IV) although the distributions overlap substantially. Schiller and Malpeli (1977a) found corresponding differences between the average conduction velocities of fibres. measured between the optic chiasm and LGNd (12.9m set-’ for “colour-opponent” units and 22.1 m see-’ for “broad-band” ones). de Monasterio (197%~) found that the conduction latencies of units that had unusual receptive fields fell

Parallel visual pathways between those of type I and types III and IV; type Vb (“on-off”) units had the longest latencies, which fell entirely within the distribution of latencies of type I units. Schiller and Malpeli measured rather longer conduction latencies in similar units Caldwell and Daw (1978) found that X- and Ycells in the rabbit were not distinguished by their latencies of response to antidromic stimulation. Both types were among the fastest-responding, as were directionally-selective units. “Sluggish” cells, and units with unusual receptive fields, had longer latencies. Compo~d action pot~~riul When the cat’s optic tract is stimulated electrically the compound action potential can be recorded at another point in the nerve or in the retina (Bishop et al., 1953). In either case the compound potential contains two modes, indicating two groups of fibres having different conduction velocities. The faster (30-40 m set- ‘) is called t, and the slower (15-23 m see-‘) t2 (Bishop and Macleod, 1954). A third- slow, conduction group (5-16m see-t, t3) contributes insu~ciently to produce a mode, but it causes a lengthening of the “tail-’ of t2 (Bishop et al., 1969). t3 is seen ciearly follo~ng electrical stimulation of the superior colticulus, for the axons that give rise to tz seem not to project there. Bishop et al. (1969) established, by electron microscopy, the distribution of fibre diameters in the optic nerve; then they used this information, together with several assumptions about the manner in which individual fibres of different diameters contribute to the compound action potential (Landau et al., 1968), to synthesize the compound potential. From this synthesis it appears that t; is contributed by fibres of diameters greater than 6 m, tz by fibres of diameter between 2.5 and 6gm, and t3 by fibres of diameter less than 2.5 pm. Rod&k (1973) calculated from the histogram of fibre diameters that about 4% of fibres contributed to tl, 44% to t2 and 52% to t3. t, almost certainly arises from Y-cells, and rz from X-cells. It seems likely that the slow-conducting axons of the other cell types give rise to t3. More than three modes have sometimes been found in the compound potential recorded following stimulation in the optic nerve or tract. Spehlmann (1967) saw between 2 and 4 in different experiments, and Freeman (1978) four. Freeman’s two fast groups fell within the range oft,, and the slower ones within the range of t2 ft3 is missed when stimuli are applied to the nerve or tract), which suggests the interesting possibility that on- and off-centre X- and Y-cells may have axons of different sizes. Possible corollaries of this are Cleland and Levick’s (1974a) finding that- at any one eccentricity, off-centre X- and Y-cells tended to have larger centres than did on-centre units. and Famiglietti and Kolb’s (1976) observation that the presumed substrates of off-centre Y-cells have the largest dendritic fields. The conduction groups ft. t2 and tJ are not re-

571

fleeted in discrete modes in the complete spectrum of optic nerve fibre diameters (Hughes and Wbsle 1976)_ but this may be because the diameter of a fibre, measured from a fixed preparation of optic nerve, varies along its length (Freeman 1978). The spectrum of myelin thicknesses has modes that seem better correlated with conduction velocity groups (Freeman, 1978). The compound action potential recorded in the monkey’s retina following electrical stimulation of the optic nerve generally shows two discrete waves that almost certainly reflect two conduction groups (Doty et al., 1964; Ogden and Miller, 1966; Gouras, 1969; Schiller and Malpeli, 1977a). Doty et al. found clear evidence for two major groups in the optic tract of the squirrel monkey, one having a conduction velocity of 6.6 m set- 1 and the other of 16.5 m set-‘. The latter group was thought to contain fewer fibres since the potential was sometimes difficult to record. Ogden and Miller’s (1966) gross measurements show the faster group in the rhesus monkey to have a conduction velocity of about 8 m see-’ and the slower about 4 m their localized me~urements, made at points XX-‘; around the edge of the disc, show that fibres ruling from the fovea1 area beIong almost exclusively to the slow-conducting group and are its slowest constituents (conduction velocities of 2.34.9 m set- ‘). At the nasal edge of the disc the slowest component of the compound potential has a conduction velocity of 5-7.5 m set- ‘, and the faster group (now clearly represented) a conduction velocity of 8-20 m set- ‘. The fovea1 fibres must therefore be the dominant contributors to the slow component recorded with gross electrodes. From Schiller and Malpeli’s (I977a) results one can calculate that the conduction velocity of the faster component cannot exceed 11.5 m set-’ and that of the slower cannot be greater than 4.5 m set- ‘. This agrees with Ogden and Miller (1966). Both conduction groups are thus appreciably slower than t2 in the cat, and the slower group is slower than t3. This is unsurprising since fibres in the monkey’s optic nerve are generally smaller (Ogden and Miller, 1966; Potts et al., 1972). Ogden and Miller calculated that the faster-conducting group of fibres had diameters of between 2.5 and 6.4 pm (77, of fibres), while the slower conducting group had diameters of between 0.7 and 2.4pm (93% of fib@, with macular fibres having diameters at the low end of this range. The fast-conducting group almost certainly represents units of types III and IV and the slow-conducting group units of types I and the rarer classes. Since the t3 wave in the cat is clearly revealed only when the superior colliculus is stimulated, the possibility of a third (slower) conduction group in the monkey should not be overlooked. Doty et al. found evidence that fibres belonging to two conduction groups in the squirrel monkey project to the superior colliculus, but there is no evidence that these groups differ from the principal groups that project to the LGNd. Clear signs of more than two conduction groups in

572

P. mediE

the optic nerve of macaque were sometimes seen by Ogden and Miiier (1966), and hints of this also appear in Couras (1969, Fig. 7). Schiller and Malpeli (1977a) and de Moaasterio (19784 occasionally found signs of a third peak, which might represent the population of units that have unusual receptive fields. Since oncentre 8bres in the spider monkey tend to have smaller centres than 0%centre ones (Hubei and Wiesel, 1960). the two ciasses may contribute to the protiferati~n of conduction groups.

1. Cat

The most widely accepted morphological classi& cation of ganglion cells in the cat is due to Boycott and Wbsle (19743, who disti~~ish~ four types (z, 8, y, Sf in Go&$-stained retinae. Two of these classes, the rx- and &types, are morphulo~~ly very similar and, ~thou~ &cells have more branched dendrites are distin~~h~ prin~p~~y by the fact that at any one ~~nt~~ty they fall into two ~puIations with respect to cell body diameter and dendritic field diameter. o-Cells are larger than /?. y-Cells have dendrites that branch much less than those of r- or &cells but their dendritic trees are as large as, or sometimes larger than. those of a-cells. Boycott and Wassle did not unequivocally identify y-cells 85 ganglion ceils, since axons were found on only a small proportion of those studied; the possibility was left open that some y-cells might be displaced amacrine cefls; some morpholo~~ly similar cehs in the rat are known to be dispfaced amacrine cells (Perry and Walker, 1980). A rarely seen type of ganglion cell (&celI) was also distin~ishe~ although tentatively. &Cells had bodies of about the same size as J?-cells at the same eccentricity, but had larger dendritic fields. Their patterns of branching resembled those of a- and @cells. The picture is complicated by the work of Famiglietti and Kolb (1976) whose distinctions, while clearly overlapping to some extent those of Boycott and W&&e, arc claimed to be different. Some divisions into cefl types are based upon the level of branching of dendrite in the inner plexiform iayer: Famiglietti and Kolb suggested that on- and of%centre receptive fields have their dendritic fields in differ~t strata a proposal confirmed by Neison et of. (1978). The vertical organization of dendrites thus appears to be physiologically important, but it would be unwise to supplant Boycott and Wiissle’s framework until the morphological distinctions discerned in vertical sections can be more firmly related to the very clear ones that emerge from the examination of wholemounts. Several methods have been used to link the anatomically distinguished classes to the physiolo~cally distinguished ones. The first clue is that r-r&s have

the largest axons and 7-cells the smallest, so by imp& cation c-cells have the fastest-conducting fibres and y-cells the slowest. &ells then become the presumptive substrate of Y-cells, p-cells the substrate of X-cells, and y-cells, acknowledged to be a more heterogeneous group, may be the counterparts of the ‘sluggish“ cells and those with unusual receptive fields. No role has yet been found for Gcells. A second link has been forged berween the sizes of dendritic trees and the sizes of central areas of rccep tive fields. The argument that these are the appropriate comp~isoos (reviewed by Levick, 1975) rests principally on the observation that the overall extent of nearly all receptive fields (at any given eccentricity) is larger .-__. than the largest dendritic field. a-Cells have larger dendritic fields than do &cells (Boycott and Wlssle, 1974) and all workers agree that the receptive fields of Y-cells have larger central areas than do those of X-cells. y-cells have large dendritic Eelds, like a-ceils, but their small and presumably slow axons preclude their being the morpholo~c~ counterparts of Y-cells. Quantitative comparisons are discouraging. The central regions of Y-cells’ receptive fields at different eccentricities match well the sizes of dendritic fields of a-cells (Cleland and Levick, 1974a: Stone and Fukuda 1974a; Peichl and WPssle, 1979) which is odd in view of the fact that the “subunits” in the receptive field of a Y-cell should spuriously inflate estimates of centre size (p. 565). A more serious difficulty is introduced when a correction For shrinkage is made to the dendritic field dimensions published by Boycott and W&&e. W&ssle et al. (1978) estimate that the wholemounts of the kind used in the earlier work were shrunk to about 0.6 of their fulf area Central areas in the receptive fields of X-cells are appreciably (~Iel~d and Levick, lQ74a; Peichl and Wiissle, 1979), or slightly (Stone and Fukuda, 197-&a)larger than the dendritic fields of @-celis. A correction for shrinkage reduces the discrepancy. Dendritic fields of y-cells are not obviously well-matched to the sizes of centres of receptive fields of “sluggish” cells (Cleland and Levick, 1974a) and, as Cleland and Levick (1974b) point out, comparisons involving units with unusual receptive fields are vitiated by the difficulty of characterizing the dimensions of the receptive fields. Creutzfeidt ef al. (1970) made a rigorous (and quite successful) attempt to deduce the profile of sensitivity in the concent~calIy-or~nized receptive field of a cat’s ganglion cell by estimating the density of synap tic contacts at different parts of the dendritic tree and weighing their contributions by an appropriate space constant. This approach ought to be helpful in the attempt to link ceils that have unusual receptive fields to their morphological substrates. The strongest evidence linking physiology and morphology in the cat comes from the heroic experiments of Cieiand et ai. (1975) and W&Fe et al. (197%. W&&e er al. examined whote-mounted retinae stained with fresyl Violet to reveal the bodies of ganglion

Parallel visual pathways cells. They established. by comparisons of cell body sizes at comparable eccentricities, that the large cells that formed a distinct group must be a-cells; then they counted every one in the retina thereby showing that x-cells form a relatively constant 3-4% of ganglion cells everywhere except in the central area, where the proportion drops to about 2%. Cleland er al. then marked the position of the receptive field of every Y-cell they found in a patch of retina that they later stained to show the large cell bodies. By comparing the positions of receptive fields with the positions of a-cell bodies Cleland et al. showed that almost every Y-cell receptive field had a corresponding a-cell body. From these remarkable experiments we know that Y-cells make up 3-4x of the population of ganglion cells in the cat, a proportion strikingly close to the 4% deduced by Rodieck (1973) from quite different experimental results. Stone (1978) confirmed Wassle et al. in showing that the proportions of sr-cells fell to around 2% in the central area, but he put the overall proportion of a-cells at between 4 and 6%. Disagreement about the number of small ganglion cells in the peripheral retina (Hughes, 1975; Stone, 1978) is responsible for Stone’s higher percentage. Relative numbers and distributions of other cell types are more difficult to establish, since cell body size is a less reliable means of identification, Fukuda and Stone (1974) found, in retinal wholemounts stained with Methylene Blue, that the distribution of cell body sizes was trimodal in regions of retina more than about 4 mm (IS’) from the central area. Their interpretaion of these modes as corresponding (in order of increasing cell body size) to y-, /?- and r-cells suggests that the ratio of cell numbers is about 38 :55:7. Revision of the figure for a-cells in the light of the results of Wiissle et al. (1975) would alter the relative proportions of ?x-and /?-cells only trivially. In the central retina and visual streak, where ganghon cell density is higher (Stone, 1965; Hughes, 1975; Stone, 1978), the distribution of cell body diameters is unimodal and there is no consensus on relative numbers of /I- and y-cells. Fukuda and Stone (1974) calculated, by rather tortuous logic, that in the central retina supposed y-cells still constituted about 40% of the population, while the proportion of supposed p-cells rose to nearly SO”/, at the expense of sr-cells. Peichl and W%sle (1979) used a differential staining technique to segregate /?- and y-cells. They estimated that &celIs constitute 60-70% and ~-cells 30-4@A of units in the area central&; in the periphery these proportions were reversed. Similar difficulties hinder analysis of the cell population in the visual streak, where cell bodies generally are smaller than at corresponding eccentricities outside it. Rowe and Stone (1976) interpret this to indicate an increased proportion of y-cells although they acknowledge that it could mean only that /?-cells have smaller bodies. The distributions of /3- and y-cells are not yet satisfactorily described, but we may have some confidence

573

that the overall proportions fall close to the values suggested by the analysis of the compound action potential. As we shall see below, most, if not all, X-cells project to the LGNd, while most of the cells with slow-conducting axons project to the superior colliculus. This fact could be exploited to identify by anatomical means the distribution of different cell types. &Cells have so far claimed no physiological counterpart, probably because Boycott and Was&e encountered them too ~frequ~tly to characterize their morphology and its variation with eccentricity. By any technique that stains only cell bodies &cells would probably be confused with @ells. Unhappily this complicates the attempt to estimate the distribution of cell types. 2. Monkey Little can be said about the relationship between the physiology and morphology of the monkey’s ganglion cells. The power of Boycott and WHssle’s morphological observations on the cat rests largely upon the use of whole-mounted retinae (for example, it permits the distinction, otherwise hard to draw, between z- and fl-cells) but no equivalent observations have been made on monkey. One of the difficulties is, of course, that ganglion cells in the fovea1 region are thickly layered. The best available descriptions of morphology (Polyak, 1941; Boycott and Dowling, 1969), which are based on vertical sections of retina, suggests a greater diversity of cell types than has been identified in the cat. It must be borne in mind, however, that the morphology of the cat’s ganglion cells seen in vertical section appears more complicated than in flat mounts ~Fami~ietti and Kotb, 1976). “Midget” ganglion cells, apparently peculiar to primates, are readily distinguished from all others by their very small dendritic fields (generally less than 10 pm in diameter). In Golgi-stained retinae they are seen most often near the fovea. The closeness of their connections with the axon terminals of midget bipolar cells suggests a one-to-one connection with single cones: consequently they may be the substrates of some of the very small type I receptive fields (Gouras, 1968; de Monasterio and Gouras, 1975; de Monasterio, 1978bf Ganglion cells that had larger dendritic fields were divided by Polyak into five types, according to the pattern of branching of their dendrites. All cell types were present in every part of the retina. Boycott and Dowling found examples of all but the “giant” cells, although they characterized cells by the level at which dendrites branched in the inner plexiform layer. This scheme of classification is, literally, orthogonal to the scheme employed later by Boycott and Wiissle in the cat. Detailed comparisons of the extents of dendritic fields with the sizes of components of receptive fields would be helpful, but this awaits an analysis of the morphology of cells in retinal whole-mounts.

P. LENNIE

574

Stone (1965) and Bunt er nl. (1975) made some observations on the distribution of all body sixes in the retina of the rhesus monkey. Although cell body size increases with eccentricity there is no clear indication, in any part of the retina, of more than one mode in the distribution of sizes. In this connection it is worth noting that distinct modes in the distribution of cell body sixes in similarly stained retinae of the cat are seen as close as 4.5 mm (2W) from the central area (Fukuda and Stone, 1974). Thus ganglion cell classes in the primate, even if physiologically homologous with those in the cat, are unlikely to bear the same morphological relationships to one another. Crossed and Uncrossed Pathways In most mammals the optic nerve fibres from one eye project to both hemispheres. The division of the nerve occurs at the optic chiasm, with almost all (rat, rabbit) or slightly more than half (cat, primate) of the fibres crossing to the eontratateral optic tract (PoIyak, 1957). An interesting question examined by Stone and Fukuda (1974b) and Kirk et al. (1976ab) is whether the projections of the different physiological types in the cat are similar. Sine the crossed pathway is phylogenetic~Iy older (Polyak, 1957) we may, by examining projections, obtain some clues about the functions of the different types. Moreover, for at least one cell type (“sluggish”) we obtain corroborative support for the division into the subtypes “sustained” and “transient”. X-cells with receptive fields in retina temporal to the vertical meridian project ipsilaterally and those from the nasal retina project contralaterally. There is a small central strip, generally less than 1” wide, where receptive fields of cells with crossed and uncrossed projections overlap. The projections of Y-cells in the two halves of the retina are less sharply segregated. The ipsilateral projection arises from units with receptive fields in temporal retina, but the contralateral projection, while it arises principally from units with receptive fields in the nasal retina, also contains axons of units with receptive fields at

CENTRAL

least as far as 10’ temporal to the midline-well outside the range of any measurement error. The most interesting projections are those of sluggish cells: all the “sluggish-sustained” cells in the nasal retina and most in the temporal retina project contralaterally, regardless of the location of their receptive fields; their projection is almost wholly crossed. The projection of “sluggish-transient” cells is much like that of Y-ceils: the ipsilateral projection arises from units +th receptive fields in temporal retina but the contralateral projection, while mainly from nasal retina includes a number of fibres with receptive fields lying up to lo” into temporal retina (Kirk er al., 1976b). “On-off” units, or “local edge detectors”, and directionally selective units project, with rare exceptions, to the contralateral hemisphere. The projection to the contralateral hemisphere of units with receptive fields lying more than a few degrees temporal to midline raises interesting problems about their destinations, for the tempora1 retina is represented poorly, if at all, in contralateral visual cortex. All the small cells that project contralaterally from temporal retina apparently by-pass the LGN, for Cooper and Pettigrew (1979) showed that heavy injections of HRP into the LGN near the projection of the midline failed to label small cells in the contralateral temporal retina. Some direction-selective units in the superior colliculus have receptive fields in the contralateral temporal retina (Feldon et al., 1970). Bunt et al. (1977) showed that injections of Horseradish Peroxidase (HRP) into the LGNd of the macaque, while tabelling almost every cell in the contralateral nasal retina, label ganglion cells in the temporal retina up to 0.5” (sparsely to 2”) from the vertical midline. This finding was qonfirmed electrophysiologically by. de Monasterio (1978a). Cowey and Perry (1980) found no labelled ganglion cells in the “wrong” half of the rhesus monkey’s retina after injections of HRP into the superior colliculus. It seems therefore that any counterparts in the primate of the “sluggish-transient’: “on-off” and directionally selective cells found in the cat either project differently or are exceedingly rare.

PROJECTiONS

Mammalian ganglion cells project directly to at least six areas of the brain (Rod&k, 1979), of which the two principal ones are the superior colliculus (SC) and ihe dorsal lateral geniculate nucleus (LGNd). Injections of HRP into the cat’s LGNd leave unlabelled a substantial fraction of small ganglion cells; some of these cells are labelled following injections into the SC (Kelly and Gilbert, 1975). A probable corollary is that the slow (ts) component of the compound action potential recorded from the optic nerve is clearly observed only when the SC is stimulated electrically (Bishop et al.. 1969). The obvious interpre-

tation, that the superior colliculus is the principal destination of small ganglion cells that have unusual receptive fields, has been confirmed by HoErnan (1973), Fukuda and Stone (1974) and Cleland and Levick (1974b). The largest gangiion cells also project to the SC, and measurements of conduction speed co&m that these must be Y-cells, many of which also project to the LGN (Fukuda and Stone, 1974; Cleland and Levi& 1974a). A very few X-cells may project to the midbrain (Cleland and Levi& 1974a), but the overwhelming majority of them project to the LGNd

575

Parallel visual pathways Almost all ganglion cells in the monkey project to the LGNd, and far fewer to the SC, the next most popular destination (Polyak, 1957; Bunt er al., 1975). There is some evidence that different groups of cells project to the two destinations. Schiller and Malpeli (1977a). and de Monasterio (1978a) found that type I units could not be activated by electrical stimulation in SC. This might occur because there is no projection of type I units, although it might simply reflect the poor representation of the fovea on the SC: the injection of HRP into the superior colliculus labels cell bodies of all sizes but the projection from the fovea1 region is very sparse (Bunt et al., 1975). This sparse fovea1 projection has also been shown autoradiographically (Hubel er al., 1975). The compound action potential recorded in the brachium of the SC reveals two groups of fibres having different conduction velocities. At least the faster of these also projects to the LGNd (Doty et al.. 1964). This is consistent with the

DORSAL

LATERAL

observations of Schiller and Malpeli (1977a) and de Monasterio (1978a) that type III units project to both destinations. Type IV units apparently project to the LGNd but not to the SC (de Monasterio, 1978a). Type II units. which have spectrally but not spatially opponent receptive fields, project to the LGNd but not SC: other units with unusual receptive fields seem to project to both destinations but relatively more of them can be activated from SC than is the case for other cell types (de Monasterio, 1978~; Schiller and Malpeli. 1977a). Because the projection to the LGNd is overwhelmingly preponderant in primates, and because only crude residual vision survives interruption of the primate’s geniculo-striate pathway (Pasik and Pasik, 1971; Weiskrantz er al., 1974) I propose in the remainder of this paper to discuss only the projection of information to the cortex via the LGN.

GENICULATE

The organization of the LGNd varies appreciably between species, depending upon the disposition of their eyes. In animals that have sizeable binocular visual fields (e.g. cat and monkey), the LGNd has clear laminations that reflect interleaved projections from the two eyes. In rat and squirrel, which have small binocular fields, the LGNd has fewer laminae and these are harder to discern (Kaas et al., 1972). Surprisingly, the number of distinct laminae in the cat and monkey that send projections to the cortex is still uncertain. Macaques and man are generally credited with six, although the four most dorsal laminae (each eye being representated in two) may be functionally a pair that, through “folding”, appears as four (Kaas et al., 1972, 1978). Recent work suggests that a further two very thin layers of cells lie between the optic tract and the previously recognized ventral layers (see Kaas er al., 1978. for a review). There are two well-defined dorsal laminae in the cat but the number of ventral relay laminae is less certain (Guillery, 1970; Hickey and Guillery, 1974). Fortunately, the exact number of distinct laminae is not important here, since our knowledge of LGN function is less refined than our knowledge of its structure. The clearest physiological distinctions concern differences between cells in the dorsal and ventral laminae, and mostly it will be unnecessary to examine substrata in any detail.

Dorsal Larninae Optic tract fibres from the contralateral eye of the cat terminate in the most dorsal lamina (A) and from the ipsilateral eye in the one ventral to it (A,). In laminae A and At, all receptive fields are concentrically organized (Hubel and Wiesel, 1961) and resem-

NUCLEUS

ble those of X- and Y-cells in the retina, but surround antagonism seems often to be stronger and geniculate units are less reponsive to diffuse illumination. X- and Y- ganglion cells have counterparts in the LGNd. This was shown first by Cleland er al. (1971) who applied the same battery of tests used to distinguish “sustained” from “transient” ganglion cells. Units in the LGNd are less easily dichotomized; some of the difficulty probably arises from the greater irregularity of the maintained discharge, but other factors must be important too. The “sustained-transient” distinction is less clear, for nearly- all geniculate relay cells give quite transient responses to steady stimuli. X- and Y-cells in the retina can be identified reliably by their different responses to moving gratings of high spatial frequency (p. 562) but Y-cells in the LGN seldom respond with a distinctive raised average discharge; instead, they gave a brief discharge at the onset of movement (Cleland er al., 1971; Hoffmann et al., 1972). The poor sensitivity of units in the LGN to stimuli of low temporal frequency probably explains this behaviour (see below). Distinctions based upon the linearity of spatial summation are more robust, and Y-cells can usually be distinguished by the way in which their responses to the exchange of a grating (especially one of high spatial frequency) or an edge for a uniform field of the same mean luminance vary with the spatial position of the stimulus (Shapley and Hochstein. 1975; Kratz et al.. 1978; So and Shapley, 1979; Derrington and Fuchs, 1979). It is hard to see how X-cells in the LGNd could summate linearly if they were driven by any but the axons of X-type ganglion cells (although Y-cells in the LGN might have input from retinal X-cells). It seems from the work of Cleland er al. (1971). in which the activity of an LGN unit was recorded simultaneously

576

I? LErjN1.s

with that of a ganglion cell driving it, that transmission from retina to cortex is usualfy via a ganglion cell and relay cell of the same type- Cieland et al. occasionally found a relay cell that was driven by several fibres having quite different conduction velocities: the properties of their receptive fields reflected this mixed input. Simifar (rare) “mixed” cells have been studied by So and Shapley (1979). Cleiand et ai. (1976) found a few “sluggish” cellss in the dorsal layers of the cat’s LGNd. The fullest description of the properties of cells in the LGNd of the rhesus monkey is provided by Wiesel and Hubel(i966). in the dorsal (parvoceliuiar) layers they distinguished three types of relay ceil, characterized by the chromatic and spatial organization of their receptive fields. Type 1 cells (77%) have, like their probable retinal counterparts, concentrically organized receptive fields, but centre and surround have different spectral sensitivities. Thus, for exampie, a ceil might be excited by red light on the centre of its receptive field and inhibited by green light on the surround. Type I receptive fields have a simple colour-opponent organization, so although their spatial structure can be revealed by mapping with spots of white light it is not easily revealed by mapping with spots of a single wavelength. The smallest receptive field centres are found among type I cells, which observation endorses the notion that they are the counterparts of the type I ganglion cells (see above). Since type I ganglion cells have X-like properties we might expect the same of type I relay ceils, Dreher et al. (1976) applied to units in the LGNd of the macaque several tests that have been used to discriminate X- from Y-cells in the cat: time course of response to steadiiy presented spots in the receptive field; Iatency of response to eiectrical stimulation: responsiveness to stimuli moving fast through the receptive field. By these measures, all type I cells in the LGNd are X-like. Type II cells in the monkey’s LGNd have a colouropponent organization in a spatially undifferentiated receptive field (Wiesei and Hubel, 1966; Dreher er al., 1976). They are refatively uncommon (about 157; of ceils found in the dorsal layers) and, by the tests applied by Dreher ef al,, all have the properties of X-ceiis. It is not known whether their spatial summation is linear but, even if it were, the poor responses of these units to achromatic stimuli and their lack of spatial selectivity are strong grounds for excluding them from the “X” category. The relatively higher frequency with which type II ceils are found in the LGN than in the retina suggests that the relay cells may be relatively larger. About 25% of units encountered in the dorsal layers are type III ceils. These have centre-surround organized receptive fields but lack any spectrally opponent org~i~tion. To this extent they are like receptive gelds of LGN units in the cat, although some units that otherwise might be classified as type

III are found to have spectrally opponent inputs when ii~t-adapted by coloured rather than by white light (Padmos and van Norren. 1975). All type III units studied by Dreher er al. in the dorsal layers of the LGN had X-like properties, and of all the units in the monkey’s LGNd these most resembIe the X-cells of the cat. The source of their inputs is puzzkng, since de Monasterio found that type III ganglion cells all had properties like those of Y-ceils in the cat. Maybe the type III units in the dorsal Iayers are driven by at least two type I ganglion cells that have different spectrai sensitivities. This would be consistent with the observation (discussed below) that centres of type III units in the dorsal layers are larger then those of type I units and the observation (Dreher et a[., 1976: Schiller and Malpeli, 1978) that the conduction velocities of all afferents to the parvoceflular Iayers fall into a single group. The hazards of relying upon time-course of response as a basis for classification are highlighted by the work of Marrocco (1976), who classified ceils in the parvoce~luIar layers using tests like those employed by Dreher er al. yet found quite different groupings of cells. Slightly more than half of Marrocco’s population of “non-opponent” (probably type III) and an unspecified fraction of spectrally opponent cells (probably mostly type I) gave “transient” responses. Sherman er al. (1976) measured receptive field sizes. latencies of response to electrical stimulation and time-courses of responses to standing contrast in ceils of the LGNd of the owl monkey. By these tests all ceils in the dorsal (parvoce~lular) laminae are X-like. Sherman ei al. (1975) used the same tests to identify X-hke and Y-like ceils in the LGN of the tree-shrew.

The transient responses of both X- and Y- relay celfs to step changes in i~Iumination suggest that they are less sensitive than their retinal counterparts to stimuli of low temporal frequency. J. B. Troy (personal communication) has shown that X- and Y-cells in the cat’s LGNd are not obviously distinguished by their temporaf contrast sensitivities derived from responses to moving gratings of optimal spatial frequency, but both types are appreciably less sensitive to low temporal frequencies than X- and Y-gang&on cells. When gratings of high contrast are used (Derrington and Fuchs, 1979) the temporal frequency for optimum response is raised, but more for Y- than for X-cells. No corresponding observations have been made on the monkey. Sensitivity to speed of marement As in the retina, Y-type refay cefis in the LGN are more sensitive to the fast movement of objects that would evoke a discharge from the surround (Cleland cr d, 197t: Hoffmann er cl., 1972). Y-&s aIso respond better than do X-cells to the rapid movement

Parallel visual pathways across the receptive field of bars (Dreher and Sandersoa 19733 or grating patterns of optimai spatid frequency; to some extent this simpiy reflects the Y-ceils’ preferences for stimuli of lower spatial frequency (Derrington and Fuchs, 1979). Observations by Dreher et al. (1976) and Lee et al. (1979) show no distinguishable sub-groups of cells in the parvocellular layers of the macaque’s LGNd. The measurements of Lee et al. suggest that the (X-like) cells respond quite we11to slits moving at velocities of up to 80 deg see- ‘. Receptive field sire and spatial setectiuity As in the retina, Y-cells in the cat’s LGNd have larger receptive fields than do X-cells. Bearing in mind that attempts to characterize the dimensions of receptive fields of Y-cells are made more difficult by the activity of subunits (see p. 565), estimates obtained by different methods suggest that, within the central 15” of visual field central regions of X-type receptive fields have diameters that range between 0.5 and IS” while those of Y-type range between 1 and 4” {~rr~ngton and Fuchs, 1979; Hoffmann et al., 1972). There is a slight su~~tion from this work that, at any one eccentricity, the ratio of centre diameters Y:X is a little greater in the LGN than in the retina. Y-cells in the LGNd respond better than X-c&s to uniform iiIlumination of their receptive fields partly because, as in the retina, the subunits in their recep tive fields generate responses at the onset and offset of diffuse illumination. However, a more important factor is the very much stronger surround in X- relay cells. This is seen particularly clearly in measurements of spatial contrast sensitivity (Derrington and Fuchs, 1979; J. B. Troy, personal ~~unication) which show a sharper loss of sensitivity in X- than in Y-ceils as the spatial frequency falls below the optimum; curves obtained from Y-cells in the LGNd are not unfike those obtained froni Y-cells in the retina (J. 3. Troy, personal ~mmunication). Wiesel and Hubel (1966) found that type I cells in the macaque had centre sizes ranging from 2 min arc to 1 deg arc; centre size was loosely correlated with eccentricity. Dreher et al.2 (1976) measurements, which show resolution of 5.6c,fdeg, were probably obtained from units with more peripheral receptive fields. Type III cells studied by Wiesel and Hubel had slightty larger centres (8min arc to 1 deg arc diameter) but this difference is not evident in Dreher et aL’s me~urem~ts of spatial resolution.

The peripherally-evoked responses (“periphery effect”rshift effect”) that characterize Y-type ganglion cells probably arise from the subunits distributed throughout and beyond the receptive field (p. 566). The activity of subunits therefore ought to be evident in responses of Y-&Is in the LGN. Cleland er al. (1971f found a periphery effect in most, but not ail, Y-cells in the cat’s LGNd. Most Y-ceils @ut not v.i. 20,7--e

577

X-cells) also give pronounced responses (*shift effect”) to the abrupt shift of grating in regions surrounding but excluding the classical receptive field (Derrington and Fuchs, 1979). Fischer and Kriiger (1974) found that nearly all the cells they studied (106 of 112) showed a “shift effect”; this may reflect the selectivity of electrodes. Kriiger (1977) studied the “shift-effect” in cells of the dorsal layers of the rhesus monkey’s LGNd. Less than 30”/, of &Is responded to stimutation by a grating moving well beyond the classical receptive fielQ and only 5% of &Is responded cIeariy, This observation is consistent with there being few Y-cells in the parvoceiiular layers of the LGNd Maintained discharge

The rates of maintained discharge in the cat’s Xand Y-relay cells are lower than in X- and Y-ganglion cells, those in X-cells being reduced to the extant that they may fall below the rates in Y-cells (Fukuda and Stone, f976; BuUier and Norton, 1979). These observations hint at the action of some inhibitory mechanism that infiuences X-cells more than it does Y. I deal with this on p. 578,

Ventral Layers of the LGNd The pattern of lamination in the ventral part of the cat’s LGNd is not easily discerned. The most authoritative view is that three distinct ventral laminae receive retinal input (Guiliery, 1970; Hickey and Guillery, 1974). The most dorsal of these (lamina C), which is relatively thick and Icontains the largest cells, receives a projection from the contralateral eye. Within this lamina the largest cell bodies tend to lie most dorsaify, near the simiiar-sized ce& of layer Al. Lamina C,, lying ventral to kunina C, is appreciably thinner, contains smaller cells, and receives only an ipsiiateral projection. Lamina Cf. lying ventral to C,, is also thin, contains small cells, and receives a projection from the contralateral eye. Lamina Cz discerned by Hickey and GuiUery (1974) is more circumscribed than the lamina originally discovered by ‘&illery (1970). The difference is accounted for by the recently recognized lamina Cs (Hickey and Guillery, 1974) which has not yet been shown to receive any retinal projection. Most higher primates, including macaques and man, have two ventrai ~rn~~llul~~ laminae (Walls, 1953; but see Kaas et a/., 1978 and Norden and Kaas, 1978). The more dorsal receives a projectioh from the ipsilateral eye and the more ventral a projection from the contralateral eye. Both laminae are of comparable thickness to the dorsal (parvocellular) ones, but contain larger cells. Cats and primates thus have quite different patterns of lamination in the ventral part of the LGNd_

578 Physiologically

P. L!?J?Z distinctice cell types

Both X- and Y-cells (distinguished by the timecourse of response to standing contrast, responses to moving gratings or discs, and differences in latency of response to electrical stimulation of the optic chiasm) are found in lamina C of the cat, but the putative Y-cells are encountered much more frequently than in the dorsal laminae. and therefore probably constitute a relatively larger fraction of the cell population (Wilson et al., 1976; Cleland et al., 1976). Wilson et al. noticed that X- and Y-cells were confined to the more dorsal part of lamina C. Hubel and Wiesel(1961) found a number of cells in the ventral layers of the cat’s LGNd that had sluggish, long-latency responses and large receptive fields. Such units have been studied more extensively by Wilson er al. (1976) and Cleland et al. (1976). Units with concentrically organized receptive fields like those of “sluggish” ganglion cells (p. 567) are seen relatively often in lamina C, mostly in the more ventral part. About 30% of cells studied fall into this category, although estimated proportions of the sub-groups “sustained” and “transient” are not agreed (Cleland et al., 1976; Wilson er al., 1976). This is not surprising in view of the relatively small numbers of cells studied. Sluggish cells are driven by slowly-conducting afferents. Cells that have unusual receptive fields, and resemble the rarely encountered ganglion cells discussed earlier (p. 568) are also found in lamina C, but too infrequently for their proportions to be guessed reliably. Lamina Ct, lying ventral to C, contains smaller cells that have not been much studied. What is known of them (Wilson et al., 1976; Cleland et al., 1976) suggests that all have receptive fields like those of “rarely” encountered ganglion cells. These too are driven by slowly-conducting afferents. Even less is known about the cells in lamina C,; they appear to behave like units in lamina Ct. Centres of receptive fields of sluggish units are larger than those of X-cells and in the range found for Y-cells (1-3” in diameter; Wilson et al., 1976). The diameters of the central regions of unusual receptive fields seem to fall within’ this range. Two distinct cell types are found within the ventral (parvocellular) layers of the monkey’s LGNd (Wiesel and H&e!, 1966). Type III cells are like type III units in the dorsal layers in having spatially though not spectrally opponent receptive fields but they are Y-like by the tests applied by Dreher et al. (1976): they give transient responses to maintained contrasts, short, latency responses to electrical stimulation and they respond to fast-moving objects. Their receptive field centrcs are larger than those of type III cells in the dorsal layers. Like Y-cells in the cat’s LGN, these units give no unmodulated discharge to the passage of fine grating patterns across their receptive fields. Nothing is known about the linearity of spatial summation within their receptive fields, although if they are driven by type III ganglion cells, it will be nonlinear.

Type IV cells, seldom encountered, are found only with on-centre receptive fields, and show rather crude colour-opponency. Receptive field centres are relatively large (0.2545’ in diameter) and are enclosed by a powerful suppressive surround that is particularly sensitive to long-wavelength light. Type IV cells respond transiently to steady illumination of the receptive field centre, but any discharge is strongly and persistently depressed by a long-wavelength spot that covers the whole receptive field. Type IV units are driven by fast-conducting afferents and are readily excited by fast-moving stimuli (Dreher et al., 1976). To that extent they resemble Y-cells in the cat. If they are driven by afferents from type IV ganglion cells. they should show non-linear spatial summation. The resemblance of types III and IV to Y-cells is reinforced by the observation (Kruger, 1977) that the “shift-effect”, a distinctive behaviour of Y-cells in the cat (p. 566). is commonly seen in ceils of the ventral. layers when regions beyond the classical receptive field are stimulated by movement of grating patterns. Y-like cells have also been found by Sherman et al. (1976) in the ventral layers of the LGNd of the owl monkey. The ~Medinl Interhminar Nucleus In cats, but not in primates, the medial interlaminar nucleus (MIN) occurs as a segment of the LGNd lying medial to the laminar part. Although not obviousy laminated, the MIN does receive projections from both eyes: that from the contralateral eye is 1971: overwhelmingly predominant (Sanderson. Kratz et al.. 1979). Virtually all cells in the MIN are Y-cells (Mason, 1975; Kratz et al., 1979; Dreher and Sefton. 1979) but, except in the part of the MIN that represents the central area (about which Kratz et al. and Dreher and Sefton are not agreed), receptive fields are appreciably larger than are those of Y-cells in the laminated part of the LGNd. Inhibitory Influences on Different Cell Types The relatively decreased sensitivity to low spatial frequencies (more marked in X-cells) suggests the presence of some powerful inhibitory influence in the LGN. The mechanism of this “increased peripheral antagonism” (Hubel and Wiesel, 1961) or “suppressive field” (Levick et al., 1972) is distinguished from the classical surround partly by its greater extent, partly by its purely suppress&e effect, and also by the interesting property that local variations in contrast beyond the classical surround bring about strong suppression (Levick er al., 1972; Fukuda and Stone, 1976). A second sign of inhibition is the reduced maintained discharge of units (particularly X-cells) in the LGN. The higher rates of maintained discharge in X-ganglion cells may be responsible for this: Suzuki and Ichijo (1967) showed that, if the spontaneous discharge of ganglion cells was abolished by raising intraocular pressure, units in the LGN became more

Parallel visual pathways

responsive to electrical stimulation in the optic tract. This suggests that normally some tonic inhibitory influence is maintained by the spontaneous activity of ganglion cells. One would therefore expect it to be greater for X- than for Y-cells. Interncurons in the LGNd may mediate both effects just described (Singer et al.. 1972; Dubin and Cleland, 1977); to the extent that interneurons are involved there is potential for cells of different classes to influence each other. Hoffmann et af. (1972) showed that the responses to electrical stimulation of both X- and Y-cells could be inhibited by prior “conditioning” stimuli that were too weak to excite X-cells, and that inhibition (on both types of cell) grew stronger as the “conditioning” shocks became strong enough to excite X- as well as Y-cells. Their conclusion, that both X- and Y-cells receive inhibition from both X- and Y-afferents, may be unnecessary, for it overlooks possible interactions between the effects of electrical stimulation and the tonic inhibitory influences that arise from the maintained discharges of X-afferents. When electrical stimuli are applied to the optic disc, shock-induced suppression of excitability in the macaque’s LGNd is confined to cells in the laminae that receive inputs from the stimulated eye (Schiller and Malpeli, 1977b). Interactions between X- and Y-like cells are therefore unlikely. Singer and Bedworth (1973) showed that, following electrical stimulation of the optic tract and radiation, IPSPs recorded intracellularly from X-type relay cells were often as fast as EPSPs. If IPSPs are transmitted through interneurons, IPSPs must therefore originate in fit-conducting (Y) afferents. Singer and Bedworth found little evidence that X-cells can influence Y-cells. Noda (1975) also described an observation that might be thought to demonstrate the inhibition of X-cells by Y-cells: he classified relay cells in awake cats as “s” or “T” types, according to the time-courses of their responses and their latencies to electrical stimulation. When cats made saccades across a patterned field T-cells gave brief discharges that were matched by a suppression of discharge in S-cells. Since this did not occur when saccades were made in the dark, but did occur when the eyes were stationary and a patterned field was moved, the inhibition arises in some visual mechanism. The segregation of X- and Y-like cells in the monkey’s LGNd makes similar interactions improbable. The puzzling feature of these findings in the cat is that any influence of Y-cells upon X-cells, if not entirely trivial, should cause X-cells to fail tests that reveal linear spatial summation. A further difficulty is caused by the observation (Lennie, 1980) that the threshold responses of X-tract fibres to the onset of a grating pattern have latencies no longer than do the responses of Y-frbres. I think therefore that crosstalk between X- and Y-cells in the cat’s LGNd must be very weak. There is a relatively weak binocular interaction in the cat’s LGNd (Sanderson et uf., 1%9), which is

579

manifest as a diffuse inhibitory field in the nondominant eye. Xsells whose dominant input is from the ipsilateral eye have stronger “non-dominant sup pression” than Y-cells or contralaterally-driven X-cells. but the difference is not large (Rodieck and Dreher, 1979). Rodieck and Dreher also found “nondominant” suppression in some of the monkey’s Y-like cells, but not in any X-like cells.

Conductian Velocities of Radiation Fibres Y-cells in the dorsal layers of the cat’s LGNd have faster-conducting axons than do X-cells. This was first shown by Cleland et al. (1971) and has since been confirmed by Stone and Hoffmann (1971X Hoffmann et al. (1972) and Cleland et al. (1976). The conduction velocities of radiation fibres are faster than those of optic tract fibres and the improvement is more pronounced for X-frbres than for Y (CIeland et at., 1971, 1976; Hoffmann et al., 1972). Cells (except Y-cells) that project to the cortex from the ventral layers have slowly-conducting axons like those of the afferents that drive them (Wilson and Stone, 1975). The addition of geniculwortico conduction times to retina-geniculate conduction times suggests that an action potential from a Y- ganglion cell might arrive at the cortex in about 4msec, that from an X-cell in 6-7 msec, and that from a ganglion celi with a slowly-conducting axon in about 15 msec, although this last value is quite variable. Lee et nf. (1977) confirmed these estimates by recording simultaneously from a cortical cell and a ganglion cell that excited it. Optic tract fibres in the monkey have appreciably slower conduction velocities than do those of the cat (p. 571). but in the optic radiation the difference is much reduced, largely because the conduction velocity of radiation fibres in the monkey is greatly increased. The two principal radiation fibre groups in the squirrel monkey have conduction velocities of 2&24m see-i and 33-40m set-’ (Doty er al., 1964Fabout three times faster than their presumed counterparts in the optic tract. These conduction velocity groups probably reflect the differences between cells in the parve- and magnocellular layers: the antidromic responses of Y-like cells in the parvocellular layers have appreciably shorter latencies than do responses of X-like cells in the parvocellular layers (Schiller and Malpeli, 1978). Although there are no published measurements of conduction times from retina to visual cortex. the observations of Schiller and Malpeli (1977a), Dreher et al. (1976) and Schiller and Ma&Ii (1978) taken together suggest that impulses travelling in fibres of the fast-conducting group (mostly spectrally non-opponent) might take about 6 msec to travel from retina to cortex, while impulses travelling in the siowly~onducting group (mostly spectrally opponent) take about 10msec.

580

P. LENME Distribution of Cell Types

X-cells are the most common in the dorsal layers of the cat’s LGNd, forming between 70 and go”,; of the units encountered in layer A and between 50 and 60”,; of the units found in At. Most of the remaining units are Y-cells (Wilson et al., 1976; Cleland er al., 1976). Electrodes probably prefer Y-cells, which are larger (see below), so the true percentages of X-cells in the dorsal layers may be appreciably higher than the figures suggest. A recent analysis of local potentials evoked in the LGNd by electrical stimulation of the optic discs or optic chiasm (Mitzdorf and Singer, 1977) suggests that longer-latency potentials (associated with the activity of X-cells) predominate in the upper parts of Iaminae A and At, while the shorter-latency potentials (which reflect the activity of Y-cells) arise mainly in a thin region close to the ventral borders of the laminae. Moreover, the potentials thought to reflect the activity of Y-cells are relatively weaker in lamina A than in A,. X-cells are the most commonly found type in the part of the LGNd that represents the area centralis (around 90%; So and Shapley, 1979) but the frequency drops to 30% at 20-25” from the area centralis. The much higher percentage of Y-cells found by Hoffmann et al. (1972) presumably reflects a different electrode bias. Y-cells and “sluggish” ceils each form about 407; of the units studied in lamina C; other types are infrequently found (Cleland et al., 1976). Little is known about the distribution of types in the more ventral layers. Physioio~cal observations provide no indication of how different classes of cells in the monkey’s LGNd cover the visual field. However, anatomical observations provide some clues: in the anterior part of the macaque’s LGNd, which represents the peripheral visual field, the magnocellular layers occupy a larger fraction of the nucleus than they do elsewhere. Moreover, the visual field is represented in four dorsal layers (which contain X-like cells) only out to the eccentricity of the optic disc, and beyond that in two (Malpeli and Baker, 1975). Both these observations suggest that Y-like cells give relatively denser coverage to the peripheral visual field. Morphological Counterparts of Physiological Classes A pleasingly simple correlation between the physiology and morphology of relay cells in the cat’s

CORTICAL

Summary There are substantial differences between retinal and LGNd units (cat) in the rate of maintained discharge, and in sensitivity to low spatiai and temporal frequencies (more marked for X-cells), but otherwise the information transmitted by different ganglion cell classes seems to be propagated through the LGNd without major change and without significant crosstalk between pathways.

PROJECI’IONS

1. Cat ~orphoiogicul

LGNd has been suggested by LeVay and Ferster (1977). They showed that, in the dorsal layers of the LGNd the three cell classes 113 distinguished by Guiltery (I%61 in Golgi-stained material. could also be distinguished on the joint criteria of cell body size and the presence or absence of a “laminar body” in the neuron. Circumstantial evidence suggests that class 1 cells are the substrates of Y-cells: they have larger (fasterconducting) axons (Ferster and LeVay, 1978) and the largest of them project to area 18, to which X-cells appear not to project (see next se$on). By exclusion, class 2 cells are X-cells. Class 3 cells are intemeurons. LeVay and Ferster (1977) found that the relative proportions of cfasses 1 and 2 change in a cow way with eccentricity from the area centralis, class i cells in lamina A forming about 20% of relay cells in the area centralis and 50-607; in the far periphery. This high proportion of (presumed) substrates .of Y-cells (even higher in the measurements of Kalil and Worden, 1978) makes it unlikely that LeVay and Ferster’s suggestion can be correct, for even the acknowledged electrode bias in favour of Y-cells does not yield enough of them to fit LeVay and Ferster’s scheme. It seems that some cells that lack laminar bodies must be X-cells. In lamina C of the LGNd most relay cells are large, Iike class 1, but a few contain the “laminar bodies” characteristic of class 2 (presumed X) cells. In laminae Ct-C, there are many small cells which LeVay and Ferster suggested were Guillery’s class 4 cell. Since their axons appear to be very fine (Ferster and LeVay, 1978) they are the presumptive substrates of ceils with slow-conducting axons. The parvocellular and magnocellular laminae of the monkey’s LGNd contain morphologically different relay cells; the main cell type in the ventral laminae resembles the class 1 cell in the cat, and in the dorsal laminae it resembles the class 2 cell (Szent~goth~, 1973).

evidence

The LGNd in the cat projects directly to the ipsilateral cortical areas 17 and 18 (Garey and Powell,

FROM THE LGNd

1967; Rosenquist et al., 1974; LeVay and Gilbert, 1976; Holliinder and Vanegas, 1977) to area 19 and to the lateral suprasylvian region, but not all parts of the nucleus project to each corticai area. Laminae A and A, have very similar projections,

Parallel visual pathways which terminate only in areas 17 and 18 (with the possible exception of a very few cells projecting from A, to area 19 (HolHnder and Vanegas, 1977). The projection to area 17 is the most substantial; Lin and Sherman (1978) and Geisert (1978) showed that between 70 and 80% of all cells in the dorsal laminae project there. This projection comes from cells of slightly smaller than average size (Hollander and Vanegas, 1977; Lin and Sherman, 1978) presumably because the bulk of the unlabelled cells consists of intemeurons. By the technique described earlier (p. 580) LeVay and Ferster (1977) inferred that Guillery’s class 2 cells (which have small cell bodies) project only to area 17. Most class 1 cells also project to area 17. Different types of cell appear to project to different cortical layers: LeVay and Gilbert (1976) showed, by autoradiographic labelling, that the A laminae have two projections, one extending from the bottom of layer IV up to the lower part of layer III, and the other terminating in layer VI. Ferster and LeVay (1978) later showed that there were two distinct projections within layer IV: one to layer IVab that arises from cells with large afferents (almost certainly class 1 neurons) and the other to layer WC from cells with distinctly smaller axons that have the same diameters as, and therefore presumably are, the axons of class 2 relay cells. Axons of both types have collaterals that terminate in layer VI. The projection to area 18 from laminae A and A, appears to arise from large cells (probably class 1). Lin and Sherman (1978) and Geisert (1978) found that these ceils form between lO and 15% of the population in the dorsal laminae. A much smaller percentage of labelled cells was found by LeVay and Ferster (1977) possibly because’ they used small injections of HRP. By the use of a double tracer technique Geisert (1978) found that most of the cells that project to area 18 also project to area 17: only 1% of cells in the dorsal laminae project exclusively to area 18. The projection to area 18 from the dorsal laminae thus seems to be rather small, but the stratification of axon terminals is like that found in area 17 (LeVay and Gilbert, 1976). Laminae A and Ar send very small projections to area 19 (HolEnder and Vanegas, 1977). Projections from the C laminae are more complex. Geisert (1978) found that 707; of cells in lamina C proper project to area 17: there is also a sizeable projection from laminae C&. These projections arise from cells of representative size (Holliinder and Vanegas, 1977). The projection to area 17 terminates at the borders between cortical layers IV and V and in the upper part of layer IVab. There appears to be no projection to layer VI, although there is a small one to layer I (LeVay and Gilbert, 1976). Ferster and LeVay (1978) showed, by injection of HRP into the optic radiation, that the projection to layer 1 arises from LGNd units with very fine axons and so probably originates in the relay cells in layers Cr.-C,. Some of these thin axons have coilaterals to area 18.

581

The projection to layer IVab probably arises from the class 1 cells in lamina C proper; that to the deeper part of layer IV may arise from different cells. Sixty percent of cells in lamina C project to area 18, but five-sixths of these (507; of all cells in the lamina) also project to area 17 (Geisert, 1978). The projection to area 18 arises from large cells (HollZnder and Vanegas, 1977) which resemble mo~holo~~y the large class 1 cells that project to the same area from the dorsal laminae (LeVay and Ferster, 1977). Cells in laminae Ci-CI project to area 18. but insubstantially (Hollander and Vanegas, 1977): their principal destination appears to be area 19. Cells in the MIN project moderately’ heavily to area 18 and substantially to area 19 (Holllnder and Vanegas, 1977); they also project to the Glare-Bishop area (Rosenquist et al., 1974). LeVay and Ferster (1977) found that the projection to area 18 arises from very large class 1 ceils; those that project to area 19 are on average slightly smaller (Holllnder and vanegas, 1977). Ph~sjo~ogical evidence on cortical projections

Since the receptive fields of most cortical cells are very different from those of units in the LGNd, there are no obvious counterparts in the cortex to cell classes distinguished in the LGN. However, antidromic activation of cells in the LGNd from different sites in the cortex allows one to infer their destinations. Stone and Dreher (1973) stimulated cortical cells in areas 17 and I8 and found that Y-cells in the LGNd could be activated readily from both areas. About 25% of Y-cells could be driven by pulses of current in either area, which suggests the presence of bifurcating axons, Mitxdorf and Singer (1978) showed, from an analysis of current source density in the visual cortex following electrical shocks to the optic radiation and chiasm, that the afferents to area 18 are conspicuously faster than the fastest to area 17. This may mean that larger branches project to area 18, or simply that the preponderant input to 18 arises from the large cells in MIN, which sends no projection to area 17. Mitzdorf and Singer’s (1978) observations also confirm the anatomical observations that in area 18 the fast afferents terminate principally in layer IV and in area 17 both in the upper part of layer IV and layer VI. X-cells in the LGNd can be activated with weak stimulating currents from area 17 but not area 18 (Stone and Dreher, ,1973). This finding supports the inference from anatomical work that X-cells project only to area 17. Mitzdorf and Singer (1978) and Bullier and Henry (1979c) underlined the agreement between anatomy and physiology with the observation that the slower afferents to area 17 terminate in the lower part of layer IV and in layer VI.

If we accept provisionally

that most of LeVay and

581

P. hNWlE

Ferster’s (1977) class 1 cells are the substrates of Y-cells and class 2 cells the substrates of X-cells, we can summarize the cortical projections as follows: X-cells project only to area 17, where they terminate in layers IVc and VI. This projection arises principally from laminae A and A,, although small numbers of X-cells project from lamina C proper and the MIN. Y-cells project to areas 17, 18 and 19. The projection to area 17 arises from smaller class 1 cells in laminae A and A,, and ends in layers IVab and VI. Y-cells from lamina C proper also project to area 17. probably to layer IVab. This projection arises in Y-cells that are among the largest class 1 neurons in the LGNd. and conceivably are physiologically distinguishable from the Y-cells of the dorsal Iaminae. The projections of Y-cells to area 18 arise from the dorsal laminae, lamina C proper and the MIN. Many Y-cells project to both areas 17 and 18. “Sluggish” cells and those with unusual receptive fields lie in the C laminae. The sluggish units, relatively common in the ventral part of lamina C proper, might be those that project to the deeper part of layer IV of area 17. The principal projection from the unusual cells in laminae Ci-Cj is probably to area 19, although some of these cells project to area 17 (where they terminate in layer I) and area 18 (Ferster and LeVay, 1978). 2. Monkey The projection of the LGNd to the cortex of the * The numbering of layers in the monkey’s striate cortex and the positions of their boundaries varies from one report to another. My usage follows Lund’s (1973) because this seems to have become standard; have been translated where necessary.

other conventions

PROPERTIES Striate

macaque is substantially simpler than in the cat: anatomical evidence shows that all afferents from the LGNd project exclusively to the striate cortex (c’l) (Wilson and Cragg. 1967: Garey and Powell, 1971: Hendrickson er ai., 1978). Although the distinctive cell groups in the LGNd project in parallel to Vl, they terminate in different layers. Hubel and Wiesel (1972) observed the disposition of degenerating axon terminals in the cortex following small lesions placed in different parts of the LGNd. Lesions in the dorsal (parvocellular) layers led to the appearance of degenerating terminals principally in cortical layer IV& and some in IVa, while lesions in the magnocellular layers caused degeneration in the lower part of layer 1Vc.z extending into the upper part of IV@.* Lund (1973) found that some large axons of (presumed) LGN cells also projected to layer IVa. Autoradiographic techniques show a weak projection from the parvocellular layers of the LGNd to the upper part of layer VI and a less certain projection from the magnocellular layers to the lower part of layer VI (Hendrickson er al.. 1978). To the extent that X-like cells are found only in the parvocellular layers and Y-like cells only in the magnocellular layers, X-like cells project to layers IV@. IVa and VI of striate cortex, and Y-like cells project to layer IVcu and possibly to layer VI. The conclusions from anatomical work are largely confirmed by Mitzdorf and Singer’s (1979) analysis of current source density in the cortex: fast-conducting afferents induce monosynaptically delayed activity in layer IVca and in layer VI: slow-conducting afferents induce corresponding activity in layers IV@? and VI. Thus, despite the very much more complex projection of the cat’s LGNd to other cortical areas, the projections to Vl of X-like and Y-like cells are similarly ordered in the cat and macaque.

OF CORTICAL

Cortex

The best-developed scheme for classifying striate cortical cells is due to Hubel and Wiesel (1962, 1965, 1968). Although it was developed before the distinction between X- and Yicells had been discovered, and probably is not simply related to the distinction between X- and Y-cells (see below) it is wellestablished and provides a useful framework within which to discuss the destinations of parallel pathways. Units with receptive fields that lack orientation sensitivity Units that have concentrically organized receptive fields like those in the retina and LGNd are seldom found in the cat’s striate cortex, but some interesting ones have been studied in the monkey. Hubei and Wiesel (1968) found in layers IVa and IVca of the macaque cortex units that had “double-opponent”

CELLS

receptive fields; for example, a unit would be excited by long-wavelength light in the centre of the receptive field and inhibited by shortwavelengths, while in the surround the arrangement was reversed. Units with similar properties have been described by Michael (1978). Hubel and Wiesel point out that such receptive fields are arranged as if they received inputs from an on-centre type III LGNd unit maximally sensitive to long wavelengths and an off-centre unit maximally sensitive to short wavelengths. Since some type 111 units are X-like and some Y-like. it is not clear which forms the more probable input to these cells. No units with similar receptive fields have been found in the LGNd. so it seems likely that the “double-opponent” units are cortical ceils and not LGNd afferents. Units with receptive fields like those of type II LGNd units have been found in the cortex by Dow and Gouras (1973): there is some uncertainty that they were cortical cells.

Paralki visual pathways Orienruriun-selectic units

~fie vast majorityof cortical &is have receptive fields that are distinguished from those of units in the retina and LGNd by their selectivity for the orientation of visual stimuli. The cardinal property of a simple cell is that its receptive field contains distinct excitatory and inhibitory regions, within each of which there is some spatial summation, so that the larger the fraction of one region that is filted with Iight, the greater the influence on the discharge of the unit. It is commonly possible to predict the response of a simple cell to any stationary stimulus from a map of the excitatory and inhibitory regions, which are usually arranged in parallel stripes, in even or odd symmetry (HubeI and Wiesei. 1962). This arrangement makes a simple cell selective for the orientation as well as the position (and often the direction of motion) of the edge or slit to which it is most responsive. 77% of the units studied by Hubel and Wiesel were simple cells. Simple ceits are also found in the monkey’s striate cortex. They formed a relatively small proportion (9%) of the units studied by HubeI and Wiesel(i96Q but 35% of the visually responsive cells classified by Schiller et al. (1976a). The higher proportion may in part be due to Schiller et at. including as “simple” many units that Hubet and Wiesel would have termed “hypercomplex” (see below). Sampling biases, about which we know little, doubtless influence the proportions of different cell classes eqcountered by different workers. Although showing orientation-selectivity, receptive fields of complex cells are distinguished from those of simple cells by the fact that it is usually hard to make a map of the receptive field with flashing spots and, if ir can be made. the map does not permit the prediction of responses to other dmuli. Moreover, the optimal stimulus (an edge or a slit of the appropriate orientation. often moving in a particular direction) is usuaiiy much smaller than the receptive field. About 23% of Hubel and Wiesel’s (1962) sample of cells in cat were complex. Complex cells were the commonest (6.5%)encountered by Hubel and Wiesel (1968) in the monkey’s striate cortex; they formed about 50% of the units classified by Schiller et al. (1976a). The proportions of simple and complex cells found in the anaesthetized monkey seem to be representative of those found in the cortex of the conscious animal (Poggio er al., 1977). Other units that have more complicated receptive fields have been studied in striate cortex of both cat and monkey. They can share with simpIe cefls selectivity for the orientation and position of a bar or an edge, and with complex cells very poor responsiveness to spots and very restricted spatial summation. One of their distinctive properties is that they show “endinhibition”, whereby a stimulus longer than optimal evokes a reduced respanse. HubeI and Wiesel (1968) called these “lower-order hy~r~ompIex cells”, but more recent work (Bishop and Henry. 1972: Dreher. 1972: Rose. t977: Gilbert, 1977) suggests that many of

583

these units [at least in the cat) may lie on the end of a continuum with respect to “end-inhibition”, in both simple and complex groups. SchiIIer er nl. (1976a) have similar& re-assigned the lower-order hypercomplex cells in the monkey’s striate cortex (20% of the units studied by Hubel and Wiesel). Hubel and Wiesel (1977) accept that these units fall into two groups, but prefer to retain the term “hypercomplex” to distinguish them from units that fack .‘~d-inhibition”. inputs to simple cells Four kinds of experiment provide information about the afferents that drive simpte cells, although uncertainty about the classification of &Is by different inv~tigators diminishes the precision of the answers. 1. Properties ‘of receptive fields. Several of the criteria that help distinguish cell classes at lower levels in the visual pathway are less helpful in revealing their possible cortical counterparts: striate cortical neurons (especially simpie &Is) often have Iittle or no maintained discharge (Pettigrew er ai.. 1968; Rose and Blakemore, 1974) and their responses are commonly more transient than are those of units in the LGNd (Ikeda and Wright, 1975a). Since X-cells show linear spatiai summation and Y-cells do not, a strong indication of X-input to a co&a1 cell would be if it showed linear spatial summation. Movshon et al. (1978a) showed, by analysis of responses of cells in the cat’s cortex to stationary gratings flickering in different positions on the receptive field (see p, 563). that most simple cells had linear spatial summation and gave modulated responses (at the frequency of stimufationf to gratings moving steadily across the receptive field. Both of these features are characteristic of X-cells and suggest that the simple cells are driven by X-afferents. It is imprdbable that the non-linearity in inputs from Y-cells could be removed. Andrews and Pollen (1979) also found approximately linear spatial summation in the receptive fields of simple cells. A minority of the units studied by Movshon et al. showed non-linear spatial summation and gave unmodulated responses to gratings moving across the receptive field. This behaviour is reminiscent of that of Y-c&, but since the nonlinear simple cells were not distinguished from linear &Is by their preferred spatial frequency (which we would expect fo be lower, were they driven by Y-afferents) it seems more likely that the non-linearity arises within the cortex (Movshon et al., 1978c). Simple ceils in the monkey’s striate cortex respond to moving gratings with a modulated discharge that follows the passage of individual bars across the receptive field @chiller et al., 1976b: Poggio er al., 1977). Ikeda and Wright (1975a) distinguished two classes of simple cell in the cat based upon the time-courses of their responses to the step onset of a stimulus: “transient” units were insensitive to gratings moving slowty across the receptive fieid and preferred gratings of Iow spatial frequencies. while “sustained” cells were

584

P. LNsn

quite sensitive to low temporal t?equencies and preferred higher spatial frequencies. Moreover, the visual latencies of “sustained” cells were longer (Ikeda and Wright, 1975b). The natural conclusion is that the “sustained” and “transient” groups are driven by Xand Y-a&rents respectively, but in view of the fact that Movshon et al. (1978~) found cells resembling those of the “transient” group only in area 18, there is some doubt that such a distinct “transient” group exists in area 17. In the monkey’s cortex Schiller et al. (1976a) distinguished several sub-types of simple cell, based upon their responses to moving edges, but since the sub-types apparently do not reveal their distinctive features when moving gratings are used to measure spatial selectivity @chiller et al., 1976b) I doubt that the distinctions are related to inputs from different classes of afferents. The smallest sub-regions of simple receptive fields in the cat (which may be compared with the centres of receptive fields of LGNd units) are 10-15 min arc in width (Hubel and Wiesel, 1962), which is close to the diameters of the smallest centres of X-relay cells in the central area, and 2-3 times smaller than those of Y-cells (p. 577). Ikeda and Wright (1975a) used grating patterns to measure the spatial selectivity of simple cells in cat, from which measurements one can readily infer the approximate dimensions of the subregions of receptive fields. Their results show that the smallest sub-regions (approx 0.12’ wide) are smaller than any found for Y-cells in the LGNd. However it is equally clear from the work of Ikeda and Wright and that of Movshon et al. (1978~) that many simple cells have preferred spatial frequencies well within the range of those of Y-cells in the LGNd. Thus, although we can be confident that some simple cells in the cat cannot be driven by Y-cells, very many could. It is clear from the work of Hubel and Wiesel (1968) and Schiller er al. (1976b) that some, but by no means all, simple cells in the monkey’s striate cortex have sub-regions too small to be compatible with their being driven by Y-like afferents (types III and IV) from the ventral layers of the, LGNd (p. 578). 2. Conduction velocities of afferents. Hoffmann and Stone (1971) found that, of the small fraction of simple cells that could be activated by electrical stimulation of the cat’s optic chiasm or optic radiation, none had latencies consistent with their being monosynaptically driven by fast-conducting (Y) afferents from the LGNd, although the latencies of some units were consistent with their being driven by slower (X) afferents. Stone and Dreher (1973) confirmed these observations, but Singer et al. (1975) asserted that 40% of simple cells are driven by fast afferents. Bullier and Henry (1979a) found that the bulk of their sample of simple cells were monosynap tically activated, and (1979b) that half the simple cells were activated by fast afferents and half by slow ones. It is difficult to draw firm conclusions from this evidence since large numbers of cortical cells cannot be driven orthodromically and (except in the work of

Bullier and Henry) it is hard to tell if a unit with a long latency to electrical stimulation is activated via fast afferents through several synapses or via slow afferents through one or a few synapses. No similar measurements of response latency have been made on the monkey’s cortical cells. 3. Stratification of simple cells. The activity of simple cells in the cat is most frequently recorded in layers III, IVab, IVc and VI, rarely in layers II and V and never in layer I (Hubel and Wiesel, 1962). Moreover, in layer IV, simple cells are the only units that are at all frequently encountered. These observations have been confirmed by Kelly and Van Essen (1974) and Gilbert (1977). There is no evidence that simple cells are more common in layer IVc than in IVab, as would be expected if they were driven only by X-afferents, although those in layer IVab have larger recep tive fields than do those in layer IVc (Gilbert and Wiesel. 1979; Bullier and Henry, 1979~). Gilbert (1977) and Leventhal and Hirsch (1978) found that simple cells in layer VI had the largest receptive fields. and those in layer IV the smallest. Leventhai and Hirsch also found that layer VI cells were sensitive to faster-moving stimuli. These observations suggest a greater influence of inputs from Y-cells on simple cells in layers IVc and VI. but no evidence points clearly to distinctive sub-types of simple cell that might be associated with exclusive X or Y input. Simple cells in the monkey were most commonly found by Hubel and Wiesel (1968) and Dow (1974) in layer IVb (IVcu in the revised terminology) and by Schilier et al. (1976a) in the IVc layers. They are found less often, but with fairly uniform frequency, in the other layers. Thus simple cells are most common where afferents from the LGNd terminate, but we have no information precise enough to indicate how they are disposed in relation to the afferents from the dorsal and ventral layers of the LGN. 4. Simultaneous recording. For six simple cells in the cat’s striate cortex Lee et al. (1977) were able concurrently to record the activity of one or more ganglion cells that provided part of their excitatory input. Three simple ceils were each excited by an X-cell, one by a Y-cell, and for one unit two inputs were found, one X and one Y. Inputs to complex cells 1. Properties of receptive fields. Movshon et al. (1978b) showed that, when stimulated by stationary gratings flickering in different positions on the recep tive field, complex cells in the cat’s striate cortex gave responses at twice the temporal frequency of stimulation. This behaviour indicates a pronounced nonlinearity in spatial summation, and sharply distinguishes complex cells from the majority of simple cells. Movshon et al. found that the non-linearities shown by complex cells were much more marked than those shown by non-linear simple cells. Complex cells in cat respond to moving grating patterns of low spatial frequency by giving modulated discharges. but

Parallel visual pathways as the spatial frequency is raised the modulated responses give way to an unmodulated elevation of average discharge (MatTei and Fiorentini, 1973; Ikeda and Wright, 1975a; Movshon et al., 1978b). Complex cells in the monkey respond in the same way to moving gratings @chiller et al., 1976b; Poggio et at., 1977); indeed the unmodulated response to gratings of high spatial frequency provides a rather reliable means of ~stin~ishing them from simple cells. Thus far the behaviour of complex cells is what would be expected were they driven by Y-a&rents. However, although the receptive field of a complex oell is substantially larger than that of a simple cell, the dimensions of the preferred stimulus, which provide an estimate of the size of the functional units in the receptive field, fit better the notion that both classes of cell are driven by the same alTerems. Hubel and Wiesel(l962) found that the most effective stimuli for some complex cells in the cat were as small as the smallest effective ones for simple cells; Ikeda and Wright (1975a) and Movshon et al. (1978c) confirmed this and found in addition that the populations of simple and complex cells in striate cortex were not distinguishable by the spatial frequencies of their optimal stimuli. The same is true of complex cells in the monkey’s striate cortex: in the sample of units studied by Schiller et al. (1976b) the distributions of spatial frequencies optimal for simple and complex cells overlapped substantially with the complex cells, if anything, preferring slightly higher spatial frequencies. It therefore seems that some complex cells must receive inputs from the X-system. The question then arises how complex receptive fields are constructed Since several aspects of the behaviour of complex cells are strongly reminisoent of the behaviour of Y-cells, it is natural to suppose that the receptive 8elQ of a complex cell might contain “subunits” (see p. 563 for discussion of subunits in Y-cells). This idea has been pursued by Movshon et al. (1978b) in elegant experiments to explore local interactions in the recep tive field. In these experiments a bar fixed in one position was flashed simultaneously with a second bar (of the same or opposite polarity) that could appear in one of several positions around the location of the fixed bar. By measuring the influence of the second bar upon the response to the first, Movshon er al. were able to map “receptive field” profiles of “subunits”. The experiments showed that “subunits” had spatially antagonistic regions within their “receptive fields” and summated their inputs linearly. The behaviour of a complex cell is then best explained by assuming that (as for Y-cells in the retina and LGNd) the outputs of all the (linear) subunits in the receptive field are rectified before being combined to generate the response.of the cell. The source of these subunits could be either relay cells in the LGNd or simple cells. Movshon et al.3 experiments do not bear upon the point, although some earlier experiments suggest that complex cells may be activated directly by LGN afferents: Movshon (1975) showed that complex cells

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may respond to stimuli moving too fast to evoke responses from simple cells, and Hammond and MacKay (1977) found that complex cells can respond well to fields of noise that fail to excite simple cells. It is clear from the analysis of Movshon et al. (1978b) that the properties of most complex cells in the cat are consistent with their having inputs that show linear spatial summation. To that extent they are more likely to be derived from the X- than from the Y-system. No corresponding analysis has been undertaken on the monkey’s complex cells, but since in most other respects they seem to be like those in the cat, it would not be surprising if their inputs were similarly organized. 2. Conduction velocities of afirents. Hoffmann and Stone (1971) found that about 30% of their sample of complex cells in cat could be activated by electrical stimulation at the optic chiasm or in the optic radiation with latencies so short as to require direct inputs from the fastest-conducting fibres in the radiation. Stone and Dreher (1973) later confirmed that some units of this type exist in striate cortex. Some complex units were activated with longer Iatencies. Singer et al. (1975) agreed that some complex cells in striate cortex (a”/, of those that are excitable) were activated by fast-conducting (Y) afferents, but they also found many units that had latencies consistent with activation by slower afferents (or fast afferents via more than one synapse). Bullier and Henry (1979ab) found that, although many complex cells appeared to be activated monosynaptically by fast afferents, a huge fraction of the same units receive other inputs, routed through additional synapses. Many cortical cells (especially in layer VI; Gilbert and Kelly, i975; Gilbert, 1977) project to the LGNd, and therefore can be antidromically activated by electrical stimulation in the optic radiation. Although this difficulty has been recognized (e.g. Stone and Dreher, 1973; Bullier and Henry, 1979a) antidromic activation could be the cause of short-latency responses in some cortical cells. 3. Strati,fication of complex cells. Complex cells are frequently encountered in layers II, III, V and VI, and rarely in layers IVab and IVc of the cat’s cortex (Hubel and Wiesel, 1962; Gilbert, 1977); they form the most substantial class in layers II and III. Two sub-classes of complex cell that are differently distributed have been distinguished by their different responses to the lengthening of an optimally-oriented bar stimulus. “Standard” complex cells (Gilbert 1977) give responses that increase as the stimulus is lengthened to fill the receptive field whereas “special” complex cells, first described by Palmer and Rosenquist (1974), have receptive fields that are substantially longer than the optimal stimulus. “Special” cells appear to be especially sensitive to visual noise (Hammond and MacKay, 1977). “Standard” complex cells are most common in layers II, III and VI. while “special” cells predominate in layer V and occur less frequently in layers III and IV. These distributions are

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not obviously related to the distributions of X- and Yaxon terminals, although the “standard” complex cells in layer VI have very large receptive fields (Gilbert, 1977); this observation is consistent with the notion that they receive inputs from Y-tierents. The paucity of complex cells in layer IV argues against the bulk of them being driven directly by LGNd afferents although, if measurements of orthodromic latency have been interpreted correctly, some must be. Most of these may be in layer VI, where axon collaterals from both X- and Y- radiation fibres terminate and complex cells are not uncommon (Gilbert and Wiesel, 1979; Bullier and Henry, 1979~). Complex cells in the monkey are rarely found in layers IVcu or IV@, but are relatively uniformly distributed in other layers (Hubel and Wiesel, 1968; Dow, 1974; Schiller et al.. 1976a). Thus, in both cat and monkey, complex cells are uncommon in the layers that are the principal destinations of fibres from the LGN.

Other Cortical Areas The evidence reviewed so far suggests that the Xand Y-systems lose their separate identities (or have them substantially transformed) in the striate cortex, so this might be an appropriate place to stop tracing the “parallel pathways”. However. since in both cat and macaque the striate cortex is a relay station to other cortical visual areas, it seems worthwhile to pursue the notion of parallel pathways one stage further, in the hope of understanding better why these pathways exist at all. Extra-striate

cortex

In addition to the map on the striate cortex there appear to be 12 other partial or complete maps of the visual field on the cortex of the cat (Tusa et al., 1979) and at least five others in the rhesus monkey (Zeki, 1978a; Van Essen, 1979). $ittle is known about the physiology of cells in extra-striate cortex so I shall discuss only the properties of units in the second visual area (V,), about which most is known. In the cat (Hubel and Wiesel, 1965) but not the macaque (Van Essen and Zeki, 1978) V2 is co-extensive with Brodmann’s area 18. The striate cortex in the monkey provides almost ail the afferent input to V2 (p. 582X but in the cat there is also a substantial direct projection from the LGN (p. 580). In both cat (Gilbert and Kelly, 1975) and squirrel monkey (Spatz er al., 1970) the projection from striate cortex to V2 arises principally in layers II and III, so in cat (and macaque, if its cortical projection to V2 is like that of the squirrel monkey) this input to V2 is predominantly from complex cells (p. 585). In the squirrel monkey the projection terminates mainly in layer IV and to a lesser degree in the lower part of layer III and the upper part of layer VI (Martinez-Millin and HollPnder. 1975). Mitzdorf and

Singer’s (1979) analysis of current source density in V2 of the macaque suggests that the ceils are activated monosynaptically through Vl, which implies inputs principally through layer IV of Vl. Hubel and Wiesel (1965) found no simple cells in V2 of tlie cat, but later workers (e.g. Tretter et al.. 1975; Orban et al., 1975; Dreher and Cottee.. 1975; Movshon et al.. 1978~) described units that had receptive fields like those of simple cells in the striate cortex, but much larger. The observation that units in V2 fall into two groups depending on whether their responses to moving gratings are modulated or unmodulated (Orban et al., 1975; Movshon et al., 1978~) and that many of their receptive fields have distinct excitatory and inhibitory regions. suggests a strong resemblance to simple cells of Vl. Some of the “simple” cells in V, may have been ones classified as lower-order hypercomplex by Hubel and Wiesel (1965) but since these were estimated to constitute 10% of Hubel and Wiesel’s sample, and units like simple cells about 40% of the sample of Tretter er al.. some confusion remains. Movshon et al. (1978~) found that the preferred spatial frequencies of units in V2 were about 4 times lower than those preferred by units in striate cortex that had receptive fields at corresponding eccentricities. As was the case in Vl, units with receptive fields of different types were distinguishable neither by their preferred spatial frequencies nor by their selectivity for spatial frequency. The presence of units with large receptive fields in V2 of the cat argues for the influence of Y-afferents (especially in view of the evidence that the direct projection to V2 arises from Y-cells that have the largest and fastest-conducting axons (p. 581). However, units in V2 of the monkey also have receptive fields that are much larger than are those of Vl (see below) and such receptive fields certainly do not depend upon a direct projection from the LGNd. Units in V2 of the cat are more sensitive than units in Vl to bars and slits that move at high velocity (Riva-Sanseverino et al., 1973; Dreher and Cottee, 1975), but this preference could be a trivial consequence of their having larger receptive fields. More informative comparisons come from measurements of temporal contrast sensitivity made using moving gratings (Movshon et al., 1978~). Such measurements show that units in both Vl and V2 are most sensitive to gratings moving at 2-8 Hz and show similar losses of sensitivity at high temporal frequencies: units in V2 are generally a good deal less sensitive than those in Vl to low temporal frequencies. The presumptive influence of Y-afferents is evident in the work of Dreher and Cottee (1975) who found that the visually-evoked responses of units in V2 were barely altered by acute bilateral ablation of striate cortex. This very remarkable result. corroborated by Sherk’s (1978) observation that cooling the striate cortex reduces the responsiveness but not the selectivity of units in V2. suggests that the projection from Vl to

Parallel visual pathways V2 in the cat may have rather subtle effects upon the sensitivities of cells in V2. Very little is known about the visual sensitivities of units in V2 of the monkey. Hubel and Wiesel (1970) described units whose responses were like those of the complex and lower-order hypetcomplex cells found in Vl, but others depended more acutely upon being driven binocularly by stimuli positioned appropriately on the receptive fields. Zeki (1978b) found some units that lacked orientation-selectivity. Receptive fields of units in V2 are substantially larger than those of corresponding units in Vl (Van Essen and Zeki, 1978) but since many of the units probably have complex receptive fields it is not clear whether preferred stimuli are also larger. Cooling of the striate cortex abolishes the visual responses of units in the topographically corresponding region of V2 (Schiller and Malpeli. 1977c), which argues for striate cortex as the principal source of input to V2.

Convergence of parallel pathways?

In the striate cortex and in V2 the properties of units make it hard to tell how X- and Y-afferents contribute to their inputs. The first question to consider is how the distinction between X- and Y-pathways relates to the distinction between simple and complex cells. One view, most strongly associated with Stone (1972) and his colleagues, is that the Xand Y-systems in the cat drive simple and complex cells respectively. Two propositions are contained here: one that simple and complex cells receive parallel inputs, and the other that these are X- and Y-cells. Evidence in favour of the first proposition comes from the observations (p. 585) that some complex cells have shortlatency responses to electrical stimulation, but it is not compelling One cannot assume that electrical stimulation of any part of the visual pathway mimics the effect of any visual stimuli (electrical phosphenes resemble nothing so much as the effects of a blow on the head!). Although the short-latency responses to electrical stimulation demonstrate that some units in striate cortex must be excited directly by Y-afferents, they do not show that the fast afferents are the only

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or principal input (cf. the difficulty of activating cortical cells presumed to be driven by small afferents, and the observation of Singer et al. (1975) and Bullier and Henry (1979a) that some cortical cells respond with multiple impulses of varying latency to a single electric shock to the visul pathway). Movshon’s (1975) and Hammond and MacKay’s (1977) observations that simple cells do not respond to some stimuli that will excite complex cells provide good evidence for direct input, but they carry no implication that this is the only or principal one. Against this evidence stands the observation (p. 585) that few complex cells are found in layer IV, the principal destination of radiation fibres, and that they are common in layers II and III, which derive their inputs from layer IV. It seems likely, both from their location in striate cortex and from the direct evidence of Lee et al. (1977), that simple cells are the primary destinations of both X- and Y-afferents. The puzzle though is that the population of simple cells, in both cat and macaque, cannot obviously be sub-divided into groups that might reflect distinctive X- and Y-inputs. It is clear that X-afferents must be the primary input to many simple cells (because of their small receptive fields), but it is not obvious that Y-afferents provide the primary input to any. As far as striate cortex is concerned, it seems difficult to avoid the conclusion, discussed first by Hubel and Wiesel (1962). that most complex cells are driven by inputs from simple cells. Y-ceils may be the primary input to units in V2 of the cat-Dreher and Cottee’s (1975) observation that ablation of striate cortex, and Sherk’s (1978) that cooling of it, has little effect on the behaviour of units in V2 encourages one to suppose that Y-afferents are important here-but the same cannot be true of the primate. The differences between the cortical organization of cat and primate are revealed very clearly by the different effects on visual behaviour of ablation of striate cortex: monkeys are virtually blind (Weiskrantz and Cowey, 1970; Pasik and Pasik, 1971), while it is often ditlicult to find any severe impairment of a cat’s pattern vision or visually-guided behaviour unless V2 is also extensively damaged (Doty, 1971: Sprague er ul.. 1977).

THE ROLE OF Y-CELLS The small receptive fields of X-cells, and their concentration in the central retina, make it difficult to doubt that they are important for spatial vision (and also perhaps for colour vision, in the monkey), but it is not so easy to see why we need a Y-system. Contribution to stereopsis

Y-cells from the region around the area centralis in the cat project almost entirely to the contralateral hemisphere. and not until one moves about 2 temporal to the area centralis does the projection from

the ipsilateral eye reach 50% (p. 574). Levick (1977) pointed out that this would be likely to arise if cortical inputs from the two Y-pathways were organized to represent a plane closer to the cat than the plane of fixation (which would be well represented by the X-system). The large receptive fields of Y-cells, and the greater sensitivity of Y-cells to stimuli moving at high velocity. are consistent with this suggestion, but I can think of no reason why the cat would want this arrangement. except perhaps to enlarge the range of midline stereopsis over that available through the

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X-system. If that were the reason it seems odd that Y-cells should become relatively more numerous in the peripheral retina Vision at low luminances The larger receptive fields of Y-cells give them an advantage in detecting stimuli when the retina is fully dark-adapted (Harding and Enroth-Cugell, 1978X but since this advantage is lost as soon as the retina becomes at all light-adapted (Enroth-Cugell and Shapley, 1973b) and Y-cells certainly receive inputs from cones (Enroth-Cugell et al., 1977a), they prob ably do something more important. Pattern- and movement-sensitive mechanisms

Interesting hypotheses about the function of Y-cells have come from psychophysicists. The most influential of these is due to Tolhurst (1973) and Kulikowski and Tolhurst (1973). who attached special importance to the larger receptive fields of Y-cells and their commonly more transient responses to step changes in the luminance of stimuli. Tolhurst suggested that the Y-system might be the substrate of a transientlyresponding mechanism, sensitive to low spatial frequencies, that was specialized to convey information about movement at the expense of information about form. The existence of such mechanisms has been inferred from several psychophysical experiments. One important piece of evidence comes from the observation (Robson, 1966; Kelly, 1977) that the shape of the curve relating human contrast sensitivity to spatial fequency depends upon the temporal frequency of the stimulus. When a (sinusoidal) grating pattern is stationary or moves or flickers slowly, contrast sensitivity generally falls quite rapidly as the spatial frequency of the grating falls below about 1 c/deg. However, when the patterns move or flicker more rapidly the sensitivity to low spatial frequencies is relatively much improved. Variations in temporal frequency seem to have similar effects on the spatial contrast sensitivity of the cat (Blake and Camisa, 1977). This is consistent with the idea (Tolhurst, 1973) that there exists some mechanism (plausibly the Y-system) sensitive to patterns of low spatial frequency and relatively insensitive to low temporal frequencies (i.e. it has a transient response to steps). However, when the temporal contrast sensitivities of X- and Y-ganglion cells (in the cat) are measured with stimuli of the sort used in psychophysical experiments, one finds (Lennie, 1980) that Y-cells are no less sensitive than X-cells to stimuli of low temporal frequency. A second line of evidence linking X- and Y-cells psychophysical with “sustained” and “transient” mechanisms has concentrated upon the supposed greater speed of response of the Y-system. Several psychophysical results (Brietmeyer, 1975: Vassilev and Mitov, 1976; Lupp et al., 1976; Harwerth and Levi, 1978) show that the simple reaction time to the onset of a grating pattern is shorter the lower the

spatial frequency of the grating The faster conduction-velocities of Y-fibres in the optic tract and optic radiation suggest a ready explanation for this observation, but the difference between conduction times in X- and Y-pathways is orders of magnitude too small to account for the psychophysical results, and in any case it is not clear that the Y-cells’ responses to light are reliably faster than are those of X-cells (Ikeda and Wright, 1972; Lennie, 1980). The strongest evidence against the idea that X- and Y-cells respectively are the substrates of the “sustained” and “transient” mechanisms distinguished psychophysically is that cortical cells (save perhaps some in V2 of the cat) do not form distinct groups according to their sensitivity to spatial or temporal frequency. The weight of the evidence seems to me to point to Y-afferents (at least in the striate cortex) not being involved directly in representing on the cortex the visual world that one observes through the microelectrode. They may have another function, perhaps to regulate the activity of the X-system, which is primarily responsible for the properties of the receptive fields of cortical cells. A background role for FcelIs?

One striking feature of simple cortical cells is how quiet most of them are until excited by their appropriate stimuli. This silence might reflect some tonic inhibitory influence, the effects of which are clearly seen in the “threshold” behaviour of simple cells when they are stimulated by patterns of low contrast. The presumptive inhibition is clearly useful if it keeps the cortex quiet in the absence of appropriate stimuli, but unless it provides a finely balanced threshold mechanism it will needlessly inpair sensitivity to the right stimulus. Perhaps Y-cells, with their large receptive fields and greatly extended peripheral region that is sensitive to local variations in contrast, provide input to a mechanism that regulates the tonic inhibition locally, reducing it as stimuli approach the sensitive region and maintaining the reduction as long as the stimulus continues to move in the region. The benefit of having a special (Y) system to accomplish this is that no network of long-range connections (which would be very large in the fovea1 representation) is required within the striate cortex. In this scheme, a Y-afferent does not contribute directly to the spatial or temporal sensitivity of cortical cells, but instead regulates the sensitivity of cells in the small region of cortex to which it projects. To achieve this end there has to be a distinct pathway up to the cortex. but there is no need for an independent Y-pathway to be retained within the cortex. Since the numbers and retinal distribution of Y-cells are known. and SO are the area of striate cortex and its magnification factor. we can deduce the size of the cortical region that might be influenced by a single Y-agerent. In each hemi-retina of the cat there are about 3100 Y-cells (WIssle et al.. 1975: Stone. 1978) that locally

Parallel visual pathways are quite regularly arranged (WPssle and Reimann, 1978). If we consider on- and off-centre units as distinct (equally numerous) populations, each hemiretina is represented on the cortex by 1500 Y-cells of each type. The area of the cat’s striate cortex is about 380 mm’ (Bilge er at., 1967: Tusa er cl., 1978) and it is clear from comparison of the distribution of Y-cells with the cortical ~~i~cation factor that the projections of Y-cells must be ~ifo~ly dense on the cortex. From Albus’ (1975) observations it appearsthat a complete sequence of orientation columns (representing 180”) occupies a cylinder with a surface diameter of about 5OO~m. About 1900 of these (representing

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both eyes) could be fitted into the striate cortex. Thus each eye is represented by perhaps 950 “hypercolumns” (Wubel and Wiesel, 1974). each of which might receive a projection from at most 2 on-centre and 2 off-centre Y-cells. Since many Y-cells in the cat may not project to the striate cortex, it seems not at all unlikely that, on average, each “hyper-column” receives an input from one on-centre Y-cell and one off-centre one. This is the sort of ~rang~~t we might expect were the function of a Y-ceil to regulate the sensitivity of a group of cortical cells (and, for that matter, cells in the superior coiliculus) that sample a restricted region of visual space.

REFERENCES Albus K. (1975)A quantitative study of the projection area of the central and paracentral visual field in area 17 of the eat-4. The spatial organization of the orientation domain. Expl Bra& Res. Z& 181-202. Andrews B. W. and Pollen D. A. 11979) Relationshio between spatial frequency selectivity and’receptive field profile of simple cells. J. Pkysfof. t87, 163-176. Barlow H. B. and Levick W. R. (1965) The mechanism of directionally selective units in rabbit’s retina. J. Physiol. 178.447-504. Barlow H. B. and Levick W. R. (1%9) Changes in the maintained discharge with adaptation level in the cat retina. J. Ptrysiol. 202, 699-718. Barlow H. B.. Hill R. M. and Levick W. R. (1964) Retinal

ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. 173, 377-407. Barlow H. B., Derrington A. M., Harris L. R. and Lennie P. (1977) The effects of remote retinal stimulation on the responses of cat retinal ganglion cells. J. Physiol. Zas, 177-194. Bilge M., Bingle A., Senevirame K. N. and Whitteridge D. (1967) A map of the visual cortex in the cat. J. PhysioL 191, 116P-118P. Bishop P. 0. and Henry G. H. (1972) Striate neurones: receptive field concepts. Iricest. Ophrhaf. 11, 346-354. Bishop P. 0. and McLeod J. G. (1954) Nature of potentials associated with synaptic transmission in the lateral geniculate of cat. J. Neurophysiol. 17, 387-414. Bishop P. 0, Jeremy D. and Lana J. W. (1953) The optic nerve. Properties of a central tract. J. Physiol. 12f, 415-432. Bishop G. H., Glare M. H. and Landau W. M. 0969) Further analysis of fiber groups in the optic tract bf the cat. EXD~ NewoL 24368-399. ’ Blake R. and Car&a ‘J. M. (1977) Temporal aspects of spatial vision in the cat. Expel Brain Res. 28, 325-333. Boycott B. B. and Dowling J. E. (1969) Organization of the primate retina: light microscopy. Phi!. Trans. R. Sot. 8255, 109-184. Boycott B. B. and Wkssle H. (1974) The morphological types of ganglion alls of the domestic cat’s retina J. Physiol. 240, 397-419.

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