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Responses of the various types of cat retinal ganglion cells to moving contours
RESPONSES OF THE VARIOUS TYPES OF CAT RETINAL GANGLION CELLS TO MOVING CONTOURS B. B. LEE and D. J. WrLLsHAw Max Pianck Institute for Biophysicaf Chemistry. Department of Neurobiology, R.0.B. 968. D-3400 GSttingen-Nikolausberg. Federal Republic of Germany (Receiced 1 June 1977) Abstract-Brisk sustained and transient ganglion cells show sit&far response patterns to moving shapes of different sites and contrasts except for some minor differenccs attributable to the larger centres and weaker surrounds of brisk transient neurones. The responses of brisk sustained units are most vigurous at 204”/sec. Brisk transient units respond most vigorously at loO’/sec or more. Siuggish units are more variable in their properties than brisk units. Siuggish transient units only respond as the edge of a large target passes over the receptive field centre. and are selective for the length of moving targets. Sluggish sustained units respond as long as any stimulus covers the field.
KufRer (1953) was the first to investigate receptive field properties of retinal ganglion cells. Using stationary, flashing spots, he found two classes of
c&s. T%eactivity of an on-centre cell was increased
by a bright stimulus located in a small region of the visual field and suppressed if the stimulus was Sashed in an annuhr region su~oundin~ An off-centre cell had a suppressive centre and an excitatory surround for bright spots. There is now evidence that there are many more classes of ganglion cells in the cat’s retina than simply on- and off-centre neurones. On- and off-centre variee ties of brisk sustained (X). brisk transient (Y), sluggish sustained and transient (W), plus a number of more rarely-encountered types of units have been described. These various classes show characteristic features in their responses to visual stimuli. It is also possible to classify ganghon &Is by measuring the antidromic conduction latency following stimulation of the afferent pathway. By this means, c&s can be placed in one of three classes corresponding to brisk sustained, brisk transient and others (Cleland, Dubin and Levick, 1971; Cleiand and Levick, 1974a, b; Cletand, Levick and Sanderson, 1973; E~roth-~u~l1 and Robson, 1966; Fukuda, 1971; Rowe and Stone, 1976; Stone and Fukuda, 1974; Stone and ~0~~. 1972). Prior to the discovery of the multipIi~ty of ganglion cell types, the responses of retinal gangiion cells to moving stimuli were described by Rodieck and Stone (1965). Taking as a basis the centre-surround organization proposed by Ecuflier (1953). they formulated a model predicting responses to moving stimuti from the response to smail flashing spots assuming Jinear spatial su~ation across the agog cell’s receptive tield (Rodieck, 1965) This assumption is only valid for brisk sustained ganglion cells; brisk transient ganglion cells show marked deviations from linearity (Cleland and Enroth-CugelJ, 1968; EnrothCugefl and Pinto, i972; Enroth-CugeU and Robson, 1966; Ho&stein and Shapley, 1976a, b). AI&o, Rodieck and Stone were probably unable to record
from the slowly-conducting axons of sluggish gangiion cells, since such axons are probably too small to be picked up in the optic tract. We have therefore investigated the responses of ganglion c&s in these various classes to moving contours. Brisk transient cells tend to have larger receptive field centres and less powerful surround mechanisms than brisk sustained ceils from the same retinal area (Cleland ef at., 1971: Cleland et nZ.. 1973; Ikeda and Wright, 1972; Stone and Hoffmann. 1972). The responses of brisk transient gangiion cells to moving stimuli would thus be expected to be broader and less well defined than the responses of brisk sustained neurones at similar retinal loci. We have tested this with moving bars of various widths, and with moving edges. Secondly, one of the diagnostic features of brisk transient vs brisk sustained ceils is the larger response of transient neurones to fast moving targets (fueled et al., 1971. 19731 We have tested the responses of the various &I types to moving bars at various speeds to find the range over which this distinction holds. Lastly. at higher levels in the visual pathway, the length of a moving bar is often a critical determ~ant of unit responses (Hubel and Wiesei, I%& 19651 We have tested the response of brisk sustained and transient ganglion cells to moving bars of various lengths, in the antj~pation that the more powerful surround of brisk sustained ganglion cells would make this a more critical parameter for this cell type. METHODS
~e~~nar~ experiments were carried out on cats anaesthetized with pentobarbitone (i.p., ~rng~g) and tbereafter OaraMed and artifidallv resoired. The activitv of the axon; of r&a1 ganglion al& was recorded from the optic tract using varnish-in&a&d tungsten microelectredes inserted through a small aaniotomy over the optic chiasm. In order to compare properties of brisk sustained, transient and sluggish ganglion cells from the same retina1 region, a further series of experiments were performed
recording directly from the retina. Cats weighing betweta 2.3 and 3.5 kg were anaesthetized with Z-4% halothane in
758
B. B.
LEE
and
a mixture of 70?,, N02. 28.596 OI and 1.5”, CO:. After tracheal and venous cannulation. the animal was set up in a stereotaxic frame, paralysed with tO_i 5 mg galfamine triethiodide and artificially ventilated (30 strokes,min) with the stroke volume adjusted to keep end-tidal CO2 at 47;. The balothane concentration in the inspired gas mixture was set during further surgery at l&1.6”/;, and the EKG monitored for possible painful stimulation of the animal. After sewing a cuff of conjunctiva to a ring around the limbus. a tungsten-in-glass microelectrode was inserted through a cannula penetrating the sclera (Cleland er al.. 1971, 1973: Dubin and Cletand. 1977). A bioolar varnishinsulated stimulating electrode (1-m; tip separation) was stereotaxically inserted into the optic chiasm through a small craniotomy. enabling measurement of the antidromic conduction latency of the recorded ganglion cells. Currents between 0.2 and LOmA were used with pulse durations of 0.1-0.2 msec. Halothane administration was discontinued during recording. Paralysis was maintained with an iv. infusion of gallamine triethiodide (.5-lOmg,&g fir) together with Ringer’s solution. The corneae were protected with plastic contact lenses and the retina of the operated eye focussed on a tangent screen i m from the animal. The projection of the optic nerve head and the area centralis on the screen were determined (Fernald and Chase, 1971). A 3-mm artificial pupil was routinely used. Ganglion cell activity was amplified and single unit spikes gated in the conventional manner. Receptive fields were plotted on the tangent screen. Moving bright or dark contours were provided by rotating a mirror mounted on the axis of a galvanometer (General Scanning GP 300) in the light beam. This system provided a highly linear stimulus movement (hysteresis < 2%). Background luminance was 50cd/m’ and stimufus luminances were i log unit above or bebw this value. though weaker contrasts were sometimes used (0.1 log unit). Response histograms were constructed on-line and stored by means of a PDP I i-40 computer.
RESULTS
We first studied more than I50 ganglion ceil axons recorded from the optic tract. where visual response properties only were used to classify axons as belong ing to brisk transient or brisk sustained cell bodies. Due to the possibility that we sometimes erred in our classification of optic tract axons, especially near the aiea centralis (see Cleland and Levick, 1974a), we went on to record from retinal ganglion cells directly. With retinal recording we were able to use antidromic conduction latency foilo~ng optic tract stimuIation as conclusive confirmation of the response-determined cell classification. The data presented here are taken from a sample of 72 retinaI ganglion cells whose activity was recorded directly from the retina. AI1 these units were studied quantitatively in some detail. A cell was first classified as brisk transient, brisk sustained or sluggish using the tests described by Cleland, Levick and their co-workers (Cleland and Levick 1974a. b; Clehnd et a!., 1971). This classification was then checked by stimulating the optic tract at supra~r~hoid intensities and measuring latencies. Providing retinal locus is taken into account and only cell body spikes are accepted for analysis, latency appears to be a reliable method of separating the three groups (Cleland and Levick. 1974a; Rowe and Stone, 1976; Stone and Hoffmann, 1972). For brisk sustained (X) cells, the mean antidromic conduction latency was 3.78 msec (N = 40, S.D. = 0.4f mse~); for
D. J.
W~LLSHAU.
brisk transient ganglion (Y) cells it was 1.91 msec (‘v = 23, S.D. = 0.36 msec); for sluggish (W) ceils. it was 7.1 msec (“V= 9. S.D. = 0.56 msec). These figures are similar to those found by other authors for the same retinal region, that is, within 10” of the area centralis contralateral to the optic disc. Siuggish cells were then separated into sustained and transient classes, on the basis of their responses to standing contrasts. Sluggish sustained neurones respond as long as a target is present in the cell’s receptive field, while sluggish transient neurones respond only on the introduction of a target, or as the edge of a large target entered or left the fietd (Cleland and Levick. 1976a; Stone and Hoffmann, 1972). Most units were studied with moving bright bars and with a IO:1 contrast ratio, though some units were studied with dark bars and with smaller contrasts to ensure that the quantitative relationships between response magnitude and stimulus speed, etc., were broadly the same irrespective of stimulus contrast, and for bright and dark stimuli (except that with contrast reversal the responses of on- and off-centre neurones are reversed). Rodieck and Stone (1965) also noted that the responses of on- and off-centre neurones were similar except that stimuli of the opposite contrast were required to produce a given response. They termed the responses of neurones to stimuli appropriate for excitation of the centre. centre-activated responses, and to stimuli appropriate for the surround. centresuppressed responses. These terms will be used here. Form
of responsesas
a function of‘stimulus width
&is& responding cells. Figure l(a) shows sponses of a typical on-centre brisk sustained
the recell to
moving bright bars of various widths. Stimulus speed was Z”/sec [which is near optimal for simple cells in the striate cortex (Movshon, 1975; Pettigrew, Nikara and Bishop, 1968)‘J. The form of these responses is very similar to those shown by Rodieck and Stone (1965). With a narrow siit (0.11% the unit responded vigorously as the slit passed over the field centre, followed by a suppression of activity as the sfit left the centre and entered the surround. As bar width was increased, the response changed little until the bar width approached and exceeded the cenfre size [moving bar widths of 0.8” or more; see Cleiand et al. (1973) and Hammond (197411. In these cases, a decrease in firing prior to the peak became apparent as the bar entered the surround. There followed a vigorous response as the edge of the bar crossed the receptive field centre, decreasing to a steady level only slightly above the spontaneous firing rate as the whole field, centre and surround, is covered by the slit. As the trailing edge of the slit left the surround, the firing rate increased once more and finally there was a brief cessation of firing as the trailing edge of the slit left the receptive field centre. Figure l(b) shows the typical responses of an oncentre brisk transient neurone to moving bright bars of various widths. Both units of Fig. 1 were approximately the same distance from the area centralis, yet the responses of the transient neurone are Si@Iificantly broader for a given stimulus width, reflecting the fact that the centres of brisk transient neufones are somewhat larger than the centres of brisk sus-
Ganglion cell responses to moving stimuli
Fig. 1. Response histograms of an on-cenlre brisk sustained (aj and an on-centre brisk transient unit (b) to moving bright bars of various widths. Reaptive fields of both cells were approximately 4” from the area centralis. Antidromic conduction latency (ADL) following OT stimulation was 3.2 msec for the brisk sustained cell and 1.6msec for the brisk transient cell. Ten stimulus sweeps were used to construct each histogram. stim&us turn-around point is indicated by the dashed fine. stimuius speed was Z*/sec. Stimulus width values are given in deg. between the histograms. Note the general similarity in the responses of the two cells. Responses to moving edges, (c) and (d), are also shown.
tained neurones from the same retinal region (Cleland et al.. 1973; Hammond. 1974). Three further features distinguished the responses of brisk transient from those of brisk sustained cells, and all these are apparent in Fig. 1. Firstly, response magnitude for brisk sustained units was similar, and near maximal, for slit widths between 0.11 and 0.8” (not included in Fig. 1). For brisk transient units, slit width for maximal responses was characteristically between 0.8 and 1.8’. whilst narrower slits produced substantially weaker responses. This corresponds again to the preference of brisk transient cells for larger targets than brisk sustained neurones, by virtue of their larger field centres (Cleland et al., 1973; Hammond, 1974). SecondIy, suppression of firing as a stimulus left the centre and entered the surround was less marked for brisk transient than for brisk sustained neurones, especially for narrower stimuli; and lastly, the increase in firing as the trailing edge of a wide bar leaves the proximal surround was weaker in brisk transient than in sustained units. Both these last two factors may be related to the weaker surround of brisk transient units in comparison with the brisk sustained variety (Cleland et al., 1973). Apart from these minor differences, however, the centre-activated responses of brisk sustained and transient neurones show a general similarity. Responses to a moving border are also shown for the on-centre cells of Fig. I@, d). The stimulus was a dark-bright edge moved forwards and backwards across the units’ rcceprive fields. In the forward direction the bright region preceded the dark. Both cells
show a peak in response to the bright edge passing over the receptive field centre (reverse direction of movement). and this peak is broader for the brisk transient neurone. Both cells show some increase in activity as the dark edge passes over the surround region prior to the centre (first direction of movement), though this is weaker for the transient cell, perhaps reflecting the weaker surround of this cell type. In both cells, passage of the dark edge across the receptive field centre results in a cessation of firing. sluggishly resFon~i~ cells. Centre-activated responses to moving bars of sluggish sustained and transient cells could be clearly distinguished from those of brisk units and from each other. Figure 2 gives one example of both types [2(a), sluggish sustained, 2(b) sluggish transient]. Response magnitude is markedly weaker than in brisk units (CIeland and Levick, 197%; Stone and Hogan, 1972). For the sluggish sustained cell of Fig. 2(a) the response to the narrowest bar is relatively weak, while with wider bars response magnitude increases. With the widest bars the response is maintained as iong as the stimutus covers the rceeptive field we. The pattern for sluggish transient units is quite different: response to the narrowest bar is almost maximal. For wider slits the neurone gives a burst of impulses as the leading edge of the bar enters the receptive field but a sustained component as the bar pass& across the receptive field centre is absent. A further characteristic of sluggish transient neurones was the ahnost complete suppression of their rather low spontaneous activity
B. B. LEE and D. J.
WILLSHAW
Fig. 2. Response histograms of an on-centre sluggish sustained unit (a) and an on-eentre sluggish transient unit (b) to moving bright bars of various widths. For ceil in (a). receptive field 1.5’ from area centralis, ADL 6.0msec. For cell in (b) receptive field 6.0” from area centralis. ADL 7.5 msec. Ten stimulus sweeps were used to construct each histogram. stimulus turn-around is indicated by the dashed line. stimulus speed was 2’/sec. The sluggish sustained unit responds as long as the stimulus covers the receptive field. the slu~~h transient unit only responds as the edge of the stimulus enters the field.
both before and after a stimulus passed across the receptive field centre, i.e. presumably as a stimulus passed across a broad surround region. Both these phenomena must reflect the presetxx of the powerful silent surround described (Cteland and Levick, 1974a) for this cell type. Centre suppressed response-brisk ceils. Centresuppressed response for brisk sustained and transient neurones are shown in Fig. 3. for narrow and broad bars. Again, for brisk sustained neurones (Fig 3a). responses are similar to those described by Rodieck and Stone (1965). in Fig 3(a), for the narrower stimu-
lus, firing is suppressed as the stimulus passes across
the receptive field centte, followed by a moderatefy vigorous discharge as the stimulus leaves the centre and enters the surround. With a wider bar there is some increase in activity as the leading edge enters the proximal surround, suppression as the leading edge crosses the receptive field centre. followed by a few impulses as the whole stimulus covers the recep tive field, then a second, almost complete cessation of firing as the trailing edge of the stimulus QOS.SW the surround, and finally a moderately vigorous discharge as the trailing edge of the stimulus leaves the
a
Fig. 3. Response‘s”ofoff-cenrre brisk &rained (a) and brisk transient (b) units to moving bright bars. For cell in (ah receptive field was 5” from the area centralis and ADL was 3.2mwc. for cell in (b). cell was 5.5” from area centralis and ADL was 2.4msec. Ten stimulus sweeps were used to construct each histogram, stimulus turn around point is indicated by the dashed line. stimulus speed was Z”/sec. Responses as the stimulus leaves the Fcntre and enters the surround are much more vigorous for the brisk sustained cell.
761
Ganglion cell responses to moving stimuli
centre. Centre-suppressed responses thus seem to be the inverse of centre-activated responses. This was also approximately the case for brisk transient units. Centre-suppressed responses of an offcentre brisk transient unit to the same stimuli as in Fig. 3(a) can be seen in Fig. 3(b). It is apparent that the ccntre-suppressed responses of brisk transient units at the stimulus speed used are relatively weak. There is a poorly-defined decrease in firing as the narrower stimulus passes across the field centre and the later response peak as the stimulus leaves the field centre is very weak in comparison with that of the brisk sustained unit. With the broader stimulus. the cell’s firing is suppressed as long as the stimulus covers the field, but again there is little response as the trailing edge of the stimulus leaves the receptive field centre. These features may be correlated with the centre-activated responses of brisk transient units. that is, weaker response to narrower relative to wider stimuli, and secondly, weaker responses. relative to brisk sustained units, as stimuli leave the centre and enter the surround. Centre-suppressed responses for sluggish neurones were not recorded in sufficient number to draw general conclusions as to their behaviour. However, the observation of Stone and Fukuda (1974), that sluggish transient (W-phasic) cells give a burst of impulses as
Stimulus
a centre-suppressed stimulus leaves the centre while sluggish sustained (W-tonic) cells do not. could be confirmed. Response magnirude length
as a function
of stimulus speed and
One of the diagnostic features for brisk transient neurones is that when a stimulus of contrast appropriate for the surround is moved at high velocity across the receptive field (ca. ZOO”/sec) responses are more vigorous than for brisk sustained neurones (Cleland er al., 1971). We have tested the responses of neurones in the various classes encountered to a 0.46’ slit moving across the receptive field at various speeds for the various cell types. The relation between response magnitude and stimulus speed is plotted in Fig. 4. Response magnitude is expressed in terms of peak firing frequency during the response. In the case of centre-activated responses. this is for the peak as the stimulus moves across the field centre; for centresuppressed responses, as the stimulus leaves the centre and enters the surround. Centre-activated responses of brisk sustained units, plotted in terms of peak firing frequency as in Fig. 4, are clearly not maximal at the stimulus speeds most effective for stimulating simple cells in the striate cortex, which are in the region of Z”/sec (Movshon, 1975;
speed,
drg/src
Fig. 4. Response magnitude plotted against stimulus speed for various ganglion cell classes. A bright bar 0.44” wide was used as the stimulus, and the impulse frequency during the response peak less the spontaneous impulse frequency was used to construct the curves. Other measures of response magnitude yielded similar relationships. Centre-activated responses (left) are measured as the stimulus passes across the centrc and centre-suppressed responses as the stimulus left the centre and entered the surround (right). Distance from the area centralis is indicated for each unit. and in the case of sluggish (W) cell% whether the cell was sustained (S) or transient (T). Maximal stimulus velocity for brisk sustained (X) cells is 2G40°/sec. for brisk transient (Y) cells. 1oO’~sec or more. For sluggish cells the curves are more variable.
762
B. B. LEE and D. J.
WILLSHAW
IO 1.4* 4.d 4.6’
.I0 * I
IO Stimulus
speed,
100
degkec
Fig. 5. Response magnitude plotted against stimulus speed for various ganglion cell claws. Same cetls as in Fig. 4 Response magnitude was evaluated in this case by measuring the total number of impulses in the response. and dividing by the number of responses used to construct the histogram and then subtracting the spontaneous activity level. The response was judged to have started as the firing rate of the unit rose above the spontaneous firing rate. and to have finished as the czil’s firing rate reached the spontaneous level following the peak. Other details as in Fig. 4. Pettigrew ef al., 1968). The curves reach a maximum and flatten out between 20 and 4W/sec with a decrease in response magnitude at the highest speed used (lW/sec). The centre-activated responses of brisk transient units are of comparable vigour at low stimulus speeds. and increase in size with increasing stimulus speed. with a marked increase in response magnitude between 20 and W/see which contrasts with the behaviour of brisk sustained cells. Most brisk transient ceils showed still more vigorous responses at the highest stimulus speed used. Only for a few brisk transient cells near the area centralis, one of which is shown in Fig. 4. was there a decrease in response magnitude at the highest speed employed. A similar pattern appears when the ~ntrifu~i component of centre-suppressed responses is plotted against stimulus speed. except that at slow stimulus speeds centrifugal responses of brisk transient units f are very weak (cf. Fig. 3b). For brisk sustained units the curves plateau around 20 to 4O”/sec, whifst brisk transient units. showing a marked increase in response magnitude as stimulus speed increases, responded most vigorously at fOO’/sec or more. As pointed out above, Cleland et al. (1971) showed that brisk transient ceils respond more vigorously than sustained cells at fast stimulus speeds with target contrast appropriate for the particular cell’s surround. Unfortunately. the presence of non-linearities in the visual projection system above lOO”/sec prevented us testing with these very fast speeds. but it is apparent that the distinction between brisk sustained and transient neurones is also quantitatively reliable for centre activated responses. Response magnitude plotted as in Fig. 4, in terms of peak firing frequency, seemed to us to be correlated with the vigour of responses as judged over the loudspeaker. However, an alternative measure of response magnitude is the number of impulses generated by the
ceii. over and above its spontaneous activity level, per response, and this measure is phoned for the brisk sustained and transient cells of Fig. 4 in Fig. 5. Although the firing frequency of a unit in response to a slowly moving stimulus may be lower. the number of impulses per response may be higher. since a slower stimulus remains over the receptive field for a longer period and hence response duration is prolonged. This is strongly apparent in Fig. 4. All units deliver more impulses per response at the slowest stimulus speed used. For centre-activated responses, the curves for brisk units (X-ON and Y-ON) overlap except at the highest stimuius spzd used; since although the firing frequency for brisk transient units during the response is rather less than for brisk sustained units. the response peaks are somewhat broader, increasing the number of impulses per response. For the centrifugal components of centre-sup pressed responses (X-OFF and Y-OFF), at lower speeds impulses per response is similar; since although firing frequency changes during centre-sup pressed responses are smafl. response peaks are broad, resulting in a number of impulses per response comparable with that for brisk sustained neurones. At higher stimulus speeds. impulses per response for brisk transient neurones are systematically greater than for brisk sustained cells. The data presented in Figs. 4 and 5 are of interest in relation to responses to stimuli moving at different speeds at higher levels in the visual system, and the implications of these results are discussed below. A further striking feature of the brisk units of Fig. 4 is their similarity. In preparations in good condition, firing rates during responses were quite similar for a given cell class and stimulus, despite marked differences in spontaneous iiring rate. and responses in the two directions of movement were generally within 10% of one another. In contrast. the response magnitudes for sluggish neurones P;ere much more
Ganglion cell responses to moving stimuli
4.0. 6.0’ 8.6’
Stimulus
length,
dog
Fig. 6. Response magnitude plotted against the length of a 0.22” bright bar passing across the field centre for various on-centre cells. There is some decrease in response magnitude as longer slits are used with brisk sustained (X) cells when the ends of the slit pass over the surround. This effect is weak with brisk transient and sluggish sustained units but very marked for sluggish transient cells Response magnitudes calculated as for Fig 4.
variable, as can be seen from Fig. 4. Generally, sluggish neurones did not show sharp tuning for stimulus speed. However, some sluggish neurones which demonstrated a centre-surround receptive field organization and thus would be placed in the sluggish rather than one of the more rarely encountered groups (Cleland and Levick, 1974b), often gave rather asymmetrical responses to the two directions of movement, which varied somewhat with stimulus speed. For example, one sluggish transient neurone gave a centre-activated response to both directions of movement at low stimulus velocities (2”/sec), was highly direction selective at higher stimulus velocities (m”/sec) but responded equally well to both directions of stimulus movement at lOO”/sec. In some cells in the striate cortex and the lateral geniculate nucleus, response magnitude falls OK significantly when the length of a moving bar exceeds a certain value (Dreher, 1972; Dreher and Sanderson. 1973; Hubel and Wiesel, 1962, 1965; Rose, 1974). To determine how far this phenomenon is present in the retina, we measured the centre-activated responses of the various cell types to moving bars of various lengths. With short bars, even though the cell might respond vigorously as the bar passed over the centre, decreases in firing before and after the peak were much less pronounced than with longer stimuli, since with small stimuli insufficient spatial summation is present to evoke these effects from the surround region. Figure 6 shows the relationship between bar length and response magnitude for the various cell types Brisk sustained cells show an increase in response magnitude up to bar length of OS-l.O”, followed by a small but definite decrease with longer stimuli whose ends swept over the surround. Mean- decrease in response to longest bar relative to maximal response was 22% Dreher and Sanderson (1973) show
that much a more marked decrease in response with increasing bar length may occur in the lateral geniculate nucleus, presumably due to inhibitory interactions within that nucleus. For brisk transient neurones, increasing the stimulus length produced a more gradual increase in response magnitude, corresponding to the larger centres of these cells. Only in one neurone, shown in Fig. 6, was there a substantial decrease in response magnitude with longer bars and this cell’s receptive field was very near the area central& where brisk transient units have a stronger centre-surround organization (Cleland and Levick. 1974a). For other cells, response magnitude showed only a slight decrease for bar lengths longer than optimal (mean decrease 8%). Unfortunately, comparable data are not available for transient cells in the lateral geniculate nucleus, but it would be expected that intrageniculate inhibition would make bar length a more critical variable for these cells also. For sluggish cells, bar length was a critical determinant of response magnitude for sluggish transient neurones (mean decrease 72%) and this is apparent in Fig. 6. For sluggish sustained neurones, increasing bar length beyond an optimal value did not substantially decrease response magnitude (mean decrease 6%). DISCUSSION
Neuronal responses to moving contours at lower levels in the visual pathway have received relatively little attention despite the importance of this type of stimulus in the striate cortex. Rodieck and Stone (1965) studied the response of retinal ganglion cells to moving stimuli. The histograms they show are very similar to those of brisk sustained ganglion cells in the present study, so it is likely that the bulk of their sample was from this cell type. A further description
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B. B. LEEand D. J.
of retinal ganglion cell responses to moving stimuli was provided by Hamasaki. Campbell. Zengel and Hazelton (1973). who classified ganglion ceils according to the prssence or absence of a dip in that part of the response histogram associated with the surround prior to the centre-activated peak. This classification may be related to the weaker surround mechanism of brisk transient relative to brisk sustained neurones. but in out experience the presence or absence of a dip was a poor predictor of whether a cell was sustained or transient. since the dip was highly dependent on stimulus shape. and also, for brisk transient cells. on retinal locus of the receptive field: transient cells near the area centralis have stronger surrounds than more peripherally situated neurones of this type (Cleland and Levick. 1974). Linear spatial summation within the receptive fields of brisk sustained (X) cells has now received substantial experimental confirmation. at least near threshold. under quite stringent conditions (C)eland and Enroth-CugeiL 1968; Enroth-Cugell and Pinto. 1972; Enroth-Cugell and Robson. 1966; Hochstein and Shapley. 1976a). and Rodieck’s model. based on this property. effectively generates the centre-activated responses of brisk sustained units (Rodieck, 1965). However, although brisk transient ganglion cells clearly have a non-linear element in their receptive field structure [Enroth-Cup11 and Robson, (1966) and Hochstein and Shapley, (1976a. b) though in the latter reference it is suggested that this non-Enear element is superimposed on a linear centre-surround organization], responses of brisk sustained and transient units are qualitatively similar. Further. we found that for both brisk sustained and transient cells, centresuppressed responses are approximately inverted images of centre-activated responses (assuming that some of the components of the response are hidden below the baseline of the response histogram). This is another property of a spatially-linear model. Whatever model is constructed to account for the behaviour of a brisk transient cell. it must (I) be spatially symmetrical (whether linear or non-linear) since the responses to both directions of movement are identical; (1) the excitatory and inhibitory components of the model must combine in such way that centre sup pressed are inverted centre-activated responses. A linear combination law is a simple way of satisfying these conditions. The results presentzd here allow us to draw certain conclusions concerning the transfer of information to higher levels in the visual pathway. When stimulus speeds suitable for simple striate cortical neurones are used. the centre-activated responses of brisk sustained and transient neuronss are comparable in magnitude. On the other hand. firing frequency during the response peak as the stimulus leaves the centre and enters the surround in centre-suppressed responses is much higher in brisk sustained units than in brisk transient cells. though the number of impulses delivered per response is similar. Now the optimal stimulus velocity for complex cortical cells is greater than that for simple cortical cells [IQ” compared to 7.?/sec; Movshon (1975)] and a correlation with the brisk transient and brisk sustained pathways has been suggested. However. it is clear from Figs. 4 and 5 that the centre-activated responses of brisk transient
WILLSHAN
cells are more vigoroIrs than those of brisk sus:amed cells only at speeds higher than those effectiw in striate cortex. Differences between ~ntre-suppressed responses of brisk sustained and transient ceils are more marked. but seem to be quantitative rather than qualitative. Presumably both the number of impulses per response and the frequency with which they are delivered play a role in determining the optima) stimulus speed for neurones in the lateral geniculate nucleus and cortex. Though some information is available concerning transformations in optimal stimufus speed between retina and striate cortex (Fig. 5: Dreher and Sanderson. 1973: &lovshon. 1975) differences in speed selectivity at these various levels
clearly require further study. The slowly-conducting sluggish pathway provides a major input to the superior colliculus (Cleland and Levick. 1974,; Fukuda and Stone. 1974). Lzaving aside the rarely-encountered types of retinal ganglion ceils (Cleland and Levick. 1974b). our results suggest that two different types of information are carried by sluggish transient and sustained axons. The former cell type responds optimally to small stimuli, and responds phasically as the edges of large targets pass across the receptive field. Sluggish sustained cells are less selective; they respond as long as a target covers the receptive field centre. irrespective of target size.
rlcfcnolvle~~e~~~enis--During part of this work B.B.L. was supported by the Wellcome Trust and D.J.W. by the Alexander von Humboldt Stiftung. We would like to thank B. G. Cleland for introducing us to direct retinal recording techniques and 0. D. Creutzfeldt for critical reading of the manuscript.
REFERENCES
Cleland B. G.. Dubin M. W. and Levick W. R. (1971) Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. J. Physioi.. Land. 217. 473-496.
Cletand 8. G. and Enroth-Cugell C. (1968) Quantitative aspects of sensitivity and summation in the cat retina. J. Physiol. Land. 198, 17-38. Cieland B. G. and Levick W. R. (1974a) Brisk and sluggish concentrically organised cells in the cat’s retina. J. Physiol.. Lond. 240, 421-456. Cleland B. G. and Levick W. R. (1974b) Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. J. Physiol.. Lond. 240, 457-492.
Cleland B. G., Levick W. R. and Sanderson K. J. (1973) Properties of sustained and transient ganglion cehs in the cat retina. J. Pkysiol., Lond. 228. 649-680. Dreher B. (1972) Hypercompfex ce-lis in the cat’s striate cortex. Itwest. Ophrhalmol. 11. 3.55-356.
Dreher B. and Sanderson K. J. (1973) Receptive field analysis: responses to moving contours by single lateral geniculate neurones in the cat. J. Physiol.. Land. 2X 95-I 18. Dubin M. W. and Cleland 3. G. (1977) The organisation of visual inputs to interneurones in the lateral geniculate nucleus of the cat. J. .~~u~op~~sio~.40. 410-427.
Ganglion
cell responses to moving stimuli
Enroth-Cugei) C. and Pinto L. H. (1972) Properties of the surround response mechanism of cat retinal ganglion cells and Lmtre-surround interaction. J. Physiol., Lond. 220.403-140.
Enroth-Cugell C. and Robson J. G. (1966) The contrast sensitivity of retinal ganglion cells of the cat. J. PhysioL. Lond.
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Femald R. and Chase R. (1971) An improved method for plotting retinal landmarks and focussing the eyes. Vision Res.
11. 95-96.
Fukuda Y. (1971) Receptive field organisation of cat optic nerve fibres with special reference to conduction velocity. Vision
Res.
11. 209-226.
Fukuda Y. and Stone J. (1974) Retinal distribution and central projections of Y-. X- and W-cells of the cat’s retina. J. Neurophysiol. 37. 749-772. Hamasaki D. I.. Campbell R.. Zengel J. and Hazelton L. R.. Jr. (1973) Response of cat retinal ganglion cell to moving stimuli. Vision Res. 13. 1421-1432. Hammond P. (1974) Cat retina) ganglion cells: size and shape of receptive field centres. J. Physiol.. Land. 242. 99-l
18.
Hochstein S. and Shapley R. M. (1976a) Quantitative analysis of retinal ganglion cell classifications. J. Physiol..
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Hcchstein S. and Shapley R. M. (1976b) Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J. Physiol..
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265-284.
Hubel D. H. and Wiese) T. N. (1962) Receptive fields. binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. Lond. MO. 106154. Hubel D. H. and Wiesel T. N. (1965) Receptive fields and
765
functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophpiol. 28. 22S289. Ikeda H. and Wright M. J. (1972) Receptive field organisation of sustained and transient ganglion ceils which sub serve different functional robe. J. Physiol.. Lond. 227. 769-800.
KutBer S. W. (1953) Discharge patterns and functional organisation of the mammalian retina. /. Nuurophysiol. 16. 37-68. Movshon J. A. (1975) The velocity tuning of single units in cat striate cortex. J. Physiol.. Lond. 249. 445-468. Pettigrew J. D., Nikara T. and Bishop P. 0. (1968) Responses to moving slits by single units in cat striate cortex. Expl Brain Res. 6, 373-390. Rodieck R. W. (1965) Quantitative analysis of cat retinal ganglion ce)) response to visual stimuli. Vision Rrs. 5. 563-601. Rodieck R. W. and Stone J. (1965) Response of cat retinal ganglion cehs to moving visual patterns. J. Neurophysiol. 28,
833-849.
Rose D. (1974) The hypercomplex cell classification in the cat’s striate cortex. J. Physiol.. Lond. 242 I23-125P. Rowe M. H. and Stone J. (1976) Conduction velocity groupings among axons of cat retina) ganglion cells, and their relation to retinal topography. Expl Brain Rrs. 25. 339-357.
Stone J. and Fukuda Y. (1974) Properties of cat retinal ganglion cells; a comparison of W-cells with X- and Y-cells. J. Ncwonhrsiol. 37. 722 -748. Stone J. and Hoffmann K.-P. (1972) Very slow conducting ganglion cells in the cat’s retina: a major, new functional type. Brain Res. 43. 610-616.
KufRer (1953) was the first to investigate receptive field properties of retinal ganglion cells. Using stationary, flashing spots, he found two classes of
c&s. T%eactivity of an on-centre cell was increased
by a bright stimulus located in a small region of the visual field and suppressed if the stimulus was Sashed in an annuhr region su~oundin~ An off-centre cell had a suppressive centre and an excitatory surround for bright spots. There is now evidence that there are many more classes of ganglion cells in the cat’s retina than simply on- and off-centre neurones. On- and off-centre variee ties of brisk sustained (X). brisk transient (Y), sluggish sustained and transient (W), plus a number of more rarely-encountered types of units have been described. These various classes show characteristic features in their responses to visual stimuli. It is also possible to classify ganghon &Is by measuring the antidromic conduction latency following stimulation of the afferent pathway. By this means, c&s can be placed in one of three classes corresponding to brisk sustained, brisk transient and others (Cleland, Dubin and Levick, 1971; Cleiand and Levick, 1974a, b; Cletand, Levick and Sanderson, 1973; E~roth-~u~l1 and Robson, 1966; Fukuda, 1971; Rowe and Stone, 1976; Stone and Fukuda, 1974; Stone and ~0~~. 1972). Prior to the discovery of the multipIi~ty of ganglion cell types, the responses of retinal gangiion cells to moving stimuli were described by Rodieck and Stone (1965). Taking as a basis the centre-surround organization proposed by Ecuflier (1953). they formulated a model predicting responses to moving stimuti from the response to smail flashing spots assuming Jinear spatial su~ation across the agog cell’s receptive tield (Rodieck, 1965) This assumption is only valid for brisk sustained ganglion cells; brisk transient ganglion cells show marked deviations from linearity (Cleland and Enroth-CugelJ, 1968; EnrothCugefl and Pinto, i972; Enroth-CugeU and Robson, 1966; Ho&stein and Shapley, 1976a, b). AI&o, Rodieck and Stone were probably unable to record
from the slowly-conducting axons of sluggish gangiion cells, since such axons are probably too small to be picked up in the optic tract. We have therefore investigated the responses of ganglion c&s in these various classes to moving contours. Brisk transient cells tend to have larger receptive field centres and less powerful surround mechanisms than brisk sustained ceils from the same retinal area (Cleland ef at., 1971: Cleland et nZ.. 1973; Ikeda and Wright, 1972; Stone and Hoffmann. 1972). The responses of brisk transient gangiion cells to moving stimuli would thus be expected to be broader and less well defined than the responses of brisk sustained neurones at similar retinal loci. We have tested this with moving bars of various widths, and with moving edges. Secondly, one of the diagnostic features of brisk transient vs brisk sustained ceils is the larger response of transient neurones to fast moving targets (fueled et al., 1971. 19731 We have tested the responses of the various &I types to moving bars at various speeds to find the range over which this distinction holds. Lastly. at higher levels in the visual pathway, the length of a moving bar is often a critical determ~ant of unit responses (Hubel and Wiesei, I%& 19651 We have tested the response of brisk sustained and transient ganglion cells to moving bars of various lengths, in the antj~pation that the more powerful surround of brisk sustained ganglion cells would make this a more critical parameter for this cell type. METHODS
~e~~nar~ experiments were carried out on cats anaesthetized with pentobarbitone (i.p., ~rng~g) and tbereafter OaraMed and artifidallv resoired. The activitv of the axon; of r&a1 ganglion al& was recorded from the optic tract using varnish-in&a&d tungsten microelectredes inserted through a small aaniotomy over the optic chiasm. In order to compare properties of brisk sustained, transient and sluggish ganglion cells from the same retina1 region, a further series of experiments were performed
recording directly from the retina. Cats weighing betweta 2.3 and 3.5 kg were anaesthetized with Z-4% halothane in
758
B. B.
LEE
and
a mixture of 70?,, N02. 28.596 OI and 1.5”, CO:. After tracheal and venous cannulation. the animal was set up in a stereotaxic frame, paralysed with tO_i 5 mg galfamine triethiodide and artificially ventilated (30 strokes,min) with the stroke volume adjusted to keep end-tidal CO2 at 47;. The balothane concentration in the inspired gas mixture was set during further surgery at l&1.6”/;, and the EKG monitored for possible painful stimulation of the animal. After sewing a cuff of conjunctiva to a ring around the limbus. a tungsten-in-glass microelectrode was inserted through a cannula penetrating the sclera (Cleland er al.. 1971, 1973: Dubin and Cletand. 1977). A bioolar varnishinsulated stimulating electrode (1-m; tip separation) was stereotaxically inserted into the optic chiasm through a small craniotomy. enabling measurement of the antidromic conduction latency of the recorded ganglion cells. Currents between 0.2 and LOmA were used with pulse durations of 0.1-0.2 msec. Halothane administration was discontinued during recording. Paralysis was maintained with an iv. infusion of gallamine triethiodide (.5-lOmg,&g fir) together with Ringer’s solution. The corneae were protected with plastic contact lenses and the retina of the operated eye focussed on a tangent screen i m from the animal. The projection of the optic nerve head and the area centralis on the screen were determined (Fernald and Chase, 1971). A 3-mm artificial pupil was routinely used. Ganglion cell activity was amplified and single unit spikes gated in the conventional manner. Receptive fields were plotted on the tangent screen. Moving bright or dark contours were provided by rotating a mirror mounted on the axis of a galvanometer (General Scanning GP 300) in the light beam. This system provided a highly linear stimulus movement (hysteresis < 2%). Background luminance was 50cd/m’ and stimufus luminances were i log unit above or bebw this value. though weaker contrasts were sometimes used (0.1 log unit). Response histograms were constructed on-line and stored by means of a PDP I i-40 computer.
RESULTS
We first studied more than I50 ganglion ceil axons recorded from the optic tract. where visual response properties only were used to classify axons as belong ing to brisk transient or brisk sustained cell bodies. Due to the possibility that we sometimes erred in our classification of optic tract axons, especially near the aiea centralis (see Cleland and Levick, 1974a), we went on to record from retinal ganglion cells directly. With retinal recording we were able to use antidromic conduction latency foilo~ng optic tract stimuIation as conclusive confirmation of the response-determined cell classification. The data presented here are taken from a sample of 72 retinaI ganglion cells whose activity was recorded directly from the retina. AI1 these units were studied quantitatively in some detail. A cell was first classified as brisk transient, brisk sustained or sluggish using the tests described by Cleland, Levick and their co-workers (Cleland and Levick 1974a. b; Clehnd et a!., 1971). This classification was then checked by stimulating the optic tract at supra~r~hoid intensities and measuring latencies. Providing retinal locus is taken into account and only cell body spikes are accepted for analysis, latency appears to be a reliable method of separating the three groups (Cleland and Levick. 1974a; Rowe and Stone, 1976; Stone and Hoffmann, 1972). For brisk sustained (X) cells, the mean antidromic conduction latency was 3.78 msec (N = 40, S.D. = 0.4f mse~); for
D. J.
W~LLSHAU.
brisk transient ganglion (Y) cells it was 1.91 msec (‘v = 23, S.D. = 0.36 msec); for sluggish (W) ceils. it was 7.1 msec (“V= 9. S.D. = 0.56 msec). These figures are similar to those found by other authors for the same retinal region, that is, within 10” of the area centralis contralateral to the optic disc. Siuggish cells were then separated into sustained and transient classes, on the basis of their responses to standing contrasts. Sluggish sustained neurones respond as long as a target is present in the cell’s receptive field, while sluggish transient neurones respond only on the introduction of a target, or as the edge of a large target entered or left the fietd (Cleland and Levick. 1976a; Stone and Hoffmann, 1972). Most units were studied with moving bright bars and with a IO:1 contrast ratio, though some units were studied with dark bars and with smaller contrasts to ensure that the quantitative relationships between response magnitude and stimulus speed, etc., were broadly the same irrespective of stimulus contrast, and for bright and dark stimuli (except that with contrast reversal the responses of on- and off-centre neurones are reversed). Rodieck and Stone (1965) also noted that the responses of on- and off-centre neurones were similar except that stimuli of the opposite contrast were required to produce a given response. They termed the responses of neurones to stimuli appropriate for excitation of the centre. centre-activated responses, and to stimuli appropriate for the surround. centresuppressed responses. These terms will be used here. Form
of responsesas
a function of‘stimulus width
&is& responding cells. Figure l(a) shows sponses of a typical on-centre brisk sustained
the recell to
moving bright bars of various widths. Stimulus speed was Z”/sec [which is near optimal for simple cells in the striate cortex (Movshon, 1975; Pettigrew, Nikara and Bishop, 1968)‘J. The form of these responses is very similar to those shown by Rodieck and Stone (1965). With a narrow siit (0.11% the unit responded vigorously as the slit passed over the field centre, followed by a suppression of activity as the sfit left the centre and entered the surround. As bar width was increased, the response changed little until the bar width approached and exceeded the cenfre size [moving bar widths of 0.8” or more; see Cleiand et al. (1973) and Hammond (197411. In these cases, a decrease in firing prior to the peak became apparent as the bar entered the surround. There followed a vigorous response as the edge of the bar crossed the receptive field centre, decreasing to a steady level only slightly above the spontaneous firing rate as the whole field, centre and surround, is covered by the slit. As the trailing edge of the slit left the surround, the firing rate increased once more and finally there was a brief cessation of firing as the trailing edge of the slit left the receptive field centre. Figure l(b) shows the typical responses of an oncentre brisk transient neurone to moving bright bars of various widths. Both units of Fig. 1 were approximately the same distance from the area centralis, yet the responses of the transient neurone are Si@Iificantly broader for a given stimulus width, reflecting the fact that the centres of brisk transient neufones are somewhat larger than the centres of brisk sus-
Ganglion cell responses to moving stimuli
Fig. 1. Response histograms of an on-cenlre brisk sustained (aj and an on-centre brisk transient unit (b) to moving bright bars of various widths. Reaptive fields of both cells were approximately 4” from the area centralis. Antidromic conduction latency (ADL) following OT stimulation was 3.2 msec for the brisk sustained cell and 1.6msec for the brisk transient cell. Ten stimulus sweeps were used to construct each histogram. stim&us turn-around point is indicated by the dashed fine. stimuius speed was Z*/sec. Stimulus width values are given in deg. between the histograms. Note the general similarity in the responses of the two cells. Responses to moving edges, (c) and (d), are also shown.
tained neurones from the same retinal region (Cleland et al.. 1973; Hammond. 1974). Three further features distinguished the responses of brisk transient from those of brisk sustained cells, and all these are apparent in Fig. 1. Firstly, response magnitude for brisk sustained units was similar, and near maximal, for slit widths between 0.11 and 0.8” (not included in Fig. 1). For brisk transient units, slit width for maximal responses was characteristically between 0.8 and 1.8’. whilst narrower slits produced substantially weaker responses. This corresponds again to the preference of brisk transient cells for larger targets than brisk sustained neurones, by virtue of their larger field centres (Cleland et al., 1973; Hammond, 1974). SecondIy, suppression of firing as a stimulus left the centre and entered the surround was less marked for brisk transient than for brisk sustained neurones, especially for narrower stimuli; and lastly, the increase in firing as the trailing edge of a wide bar leaves the proximal surround was weaker in brisk transient than in sustained units. Both these last two factors may be related to the weaker surround of brisk transient units in comparison with the brisk sustained variety (Cleland et al., 1973). Apart from these minor differences, however, the centre-activated responses of brisk sustained and transient neurones show a general similarity. Responses to a moving border are also shown for the on-centre cells of Fig. I@, d). The stimulus was a dark-bright edge moved forwards and backwards across the units’ rcceprive fields. In the forward direction the bright region preceded the dark. Both cells
show a peak in response to the bright edge passing over the receptive field centre (reverse direction of movement). and this peak is broader for the brisk transient neurone. Both cells show some increase in activity as the dark edge passes over the surround region prior to the centre (first direction of movement), though this is weaker for the transient cell, perhaps reflecting the weaker surround of this cell type. In both cells, passage of the dark edge across the receptive field centre results in a cessation of firing. sluggishly resFon~i~ cells. Centre-activated responses to moving bars of sluggish sustained and transient cells could be clearly distinguished from those of brisk units and from each other. Figure 2 gives one example of both types [2(a), sluggish sustained, 2(b) sluggish transient]. Response magnitude is markedly weaker than in brisk units (CIeland and Levick, 197%; Stone and Hogan, 1972). For the sluggish sustained cell of Fig. 2(a) the response to the narrowest bar is relatively weak, while with wider bars response magnitude increases. With the widest bars the response is maintained as iong as the stimutus covers the rceeptive field we. The pattern for sluggish transient units is quite different: response to the narrowest bar is almost maximal. For wider slits the neurone gives a burst of impulses as the leading edge of the bar enters the receptive field but a sustained component as the bar pass& across the receptive field centre is absent. A further characteristic of sluggish transient neurones was the ahnost complete suppression of their rather low spontaneous activity
B. B. LEE and D. J.
WILLSHAW
Fig. 2. Response histograms of an on-centre sluggish sustained unit (a) and an on-eentre sluggish transient unit (b) to moving bright bars of various widths. For ceil in (a). receptive field 1.5’ from area centralis, ADL 6.0msec. For cell in (b) receptive field 6.0” from area centralis. ADL 7.5 msec. Ten stimulus sweeps were used to construct each histogram. stimulus turn-around is indicated by the dashed line. stimulus speed was 2’/sec. The sluggish sustained unit responds as long as the stimulus covers the receptive field. the slu~~h transient unit only responds as the edge of the stimulus enters the field.
both before and after a stimulus passed across the receptive field centre, i.e. presumably as a stimulus passed across a broad surround region. Both these phenomena must reflect the presetxx of the powerful silent surround described (Cteland and Levick, 1974a) for this cell type. Centre suppressed response-brisk ceils. Centresuppressed response for brisk sustained and transient neurones are shown in Fig. 3. for narrow and broad bars. Again, for brisk sustained neurones (Fig 3a). responses are similar to those described by Rodieck and Stone (1965). in Fig 3(a), for the narrower stimu-
lus, firing is suppressed as the stimulus passes across
the receptive field centte, followed by a moderatefy vigorous discharge as the stimulus leaves the centre and enters the surround. With a wider bar there is some increase in activity as the leading edge enters the proximal surround, suppression as the leading edge crosses the receptive field centre. followed by a few impulses as the whole stimulus covers the recep tive field, then a second, almost complete cessation of firing as the trailing edge of the stimulus QOS.SW the surround, and finally a moderately vigorous discharge as the trailing edge of the stimulus leaves the
a
Fig. 3. Response‘s”ofoff-cenrre brisk &rained (a) and brisk transient (b) units to moving bright bars. For cell in (ah receptive field was 5” from the area centralis and ADL was 3.2mwc. for cell in (b). cell was 5.5” from area centralis and ADL was 2.4msec. Ten stimulus sweeps were used to construct each histogram, stimulus turn around point is indicated by the dashed line. stimulus speed was Z”/sec. Responses as the stimulus leaves the Fcntre and enters the surround are much more vigorous for the brisk sustained cell.
761
Ganglion cell responses to moving stimuli
centre. Centre-suppressed responses thus seem to be the inverse of centre-activated responses. This was also approximately the case for brisk transient units. Centre-suppressed responses of an offcentre brisk transient unit to the same stimuli as in Fig. 3(a) can be seen in Fig. 3(b). It is apparent that the ccntre-suppressed responses of brisk transient units at the stimulus speed used are relatively weak. There is a poorly-defined decrease in firing as the narrower stimulus passes across the field centre and the later response peak as the stimulus leaves the field centre is very weak in comparison with that of the brisk sustained unit. With the broader stimulus. the cell’s firing is suppressed as long as the stimulus covers the field, but again there is little response as the trailing edge of the stimulus leaves the receptive field centre. These features may be correlated with the centre-activated responses of brisk transient units. that is, weaker response to narrower relative to wider stimuli, and secondly, weaker responses. relative to brisk sustained units, as stimuli leave the centre and enter the surround. Centre-suppressed responses for sluggish neurones were not recorded in sufficient number to draw general conclusions as to their behaviour. However, the observation of Stone and Fukuda (1974), that sluggish transient (W-phasic) cells give a burst of impulses as
Stimulus
a centre-suppressed stimulus leaves the centre while sluggish sustained (W-tonic) cells do not. could be confirmed. Response magnirude length
as a function
of stimulus speed and
One of the diagnostic features for brisk transient neurones is that when a stimulus of contrast appropriate for the surround is moved at high velocity across the receptive field (ca. ZOO”/sec) responses are more vigorous than for brisk sustained neurones (Cleland er al., 1971). We have tested the responses of neurones in the various classes encountered to a 0.46’ slit moving across the receptive field at various speeds for the various cell types. The relation between response magnitude and stimulus speed is plotted in Fig. 4. Response magnitude is expressed in terms of peak firing frequency during the response. In the case of centre-activated responses. this is for the peak as the stimulus moves across the field centre; for centresuppressed responses, as the stimulus leaves the centre and enters the surround. Centre-activated responses of brisk sustained units, plotted in terms of peak firing frequency as in Fig. 4, are clearly not maximal at the stimulus speeds most effective for stimulating simple cells in the striate cortex, which are in the region of Z”/sec (Movshon, 1975;
speed,
drg/src
Fig. 4. Response magnitude plotted against stimulus speed for various ganglion cell classes. A bright bar 0.44” wide was used as the stimulus, and the impulse frequency during the response peak less the spontaneous impulse frequency was used to construct the curves. Other measures of response magnitude yielded similar relationships. Centre-activated responses (left) are measured as the stimulus passes across the centrc and centre-suppressed responses as the stimulus left the centre and entered the surround (right). Distance from the area centralis is indicated for each unit. and in the case of sluggish (W) cell% whether the cell was sustained (S) or transient (T). Maximal stimulus velocity for brisk sustained (X) cells is 2G40°/sec. for brisk transient (Y) cells. 1oO’~sec or more. For sluggish cells the curves are more variable.
762
B. B. LEE and D. J.
WILLSHAW
IO 1.4* 4.d 4.6’
.I0 * I
IO Stimulus
speed,
100
degkec
Fig. 5. Response magnitude plotted against stimulus speed for various ganglion cell claws. Same cetls as in Fig. 4 Response magnitude was evaluated in this case by measuring the total number of impulses in the response. and dividing by the number of responses used to construct the histogram and then subtracting the spontaneous activity level. The response was judged to have started as the firing rate of the unit rose above the spontaneous firing rate. and to have finished as the czil’s firing rate reached the spontaneous level following the peak. Other details as in Fig. 4. Pettigrew ef al., 1968). The curves reach a maximum and flatten out between 20 and 4W/sec with a decrease in response magnitude at the highest speed used (lW/sec). The centre-activated responses of brisk transient units are of comparable vigour at low stimulus speeds. and increase in size with increasing stimulus speed. with a marked increase in response magnitude between 20 and W/see which contrasts with the behaviour of brisk sustained cells. Most brisk transient ceils showed still more vigorous responses at the highest stimulus speed used. Only for a few brisk transient cells near the area centralis, one of which is shown in Fig. 4. was there a decrease in response magnitude at the highest speed employed. A similar pattern appears when the ~ntrifu~i component of centre-suppressed responses is plotted against stimulus speed. except that at slow stimulus speeds centrifugal responses of brisk transient units f are very weak (cf. Fig. 3b). For brisk sustained units the curves plateau around 20 to 4O”/sec, whifst brisk transient units. showing a marked increase in response magnitude as stimulus speed increases, responded most vigorously at fOO’/sec or more. As pointed out above, Cleland et al. (1971) showed that brisk transient ceils respond more vigorously than sustained cells at fast stimulus speeds with target contrast appropriate for the particular cell’s surround. Unfortunately. the presence of non-linearities in the visual projection system above lOO”/sec prevented us testing with these very fast speeds. but it is apparent that the distinction between brisk sustained and transient neurones is also quantitatively reliable for centre activated responses. Response magnitude plotted as in Fig. 4, in terms of peak firing frequency, seemed to us to be correlated with the vigour of responses as judged over the loudspeaker. However, an alternative measure of response magnitude is the number of impulses generated by the
ceii. over and above its spontaneous activity level, per response, and this measure is phoned for the brisk sustained and transient cells of Fig. 4 in Fig. 5. Although the firing frequency of a unit in response to a slowly moving stimulus may be lower. the number of impulses per response may be higher. since a slower stimulus remains over the receptive field for a longer period and hence response duration is prolonged. This is strongly apparent in Fig. 4. All units deliver more impulses per response at the slowest stimulus speed used. For centre-activated responses, the curves for brisk units (X-ON and Y-ON) overlap except at the highest stimuius spzd used; since although the firing frequency for brisk transient units during the response is rather less than for brisk sustained units. the response peaks are somewhat broader, increasing the number of impulses per response. For the centrifugal components of centre-sup pressed responses (X-OFF and Y-OFF), at lower speeds impulses per response is similar; since although firing frequency changes during centre-sup pressed responses are smafl. response peaks are broad, resulting in a number of impulses per response comparable with that for brisk sustained neurones. At higher stimulus speeds. impulses per response for brisk transient neurones are systematically greater than for brisk sustained cells. The data presented in Figs. 4 and 5 are of interest in relation to responses to stimuli moving at different speeds at higher levels in the visual system, and the implications of these results are discussed below. A further striking feature of the brisk units of Fig. 4 is their similarity. In preparations in good condition, firing rates during responses were quite similar for a given cell class and stimulus, despite marked differences in spontaneous iiring rate. and responses in the two directions of movement were generally within 10% of one another. In contrast. the response magnitudes for sluggish neurones P;ere much more
Ganglion cell responses to moving stimuli
4.0. 6.0’ 8.6’
Stimulus
length,
dog
Fig. 6. Response magnitude plotted against the length of a 0.22” bright bar passing across the field centre for various on-centre cells. There is some decrease in response magnitude as longer slits are used with brisk sustained (X) cells when the ends of the slit pass over the surround. This effect is weak with brisk transient and sluggish sustained units but very marked for sluggish transient cells Response magnitudes calculated as for Fig 4.
variable, as can be seen from Fig. 4. Generally, sluggish neurones did not show sharp tuning for stimulus speed. However, some sluggish neurones which demonstrated a centre-surround receptive field organization and thus would be placed in the sluggish rather than one of the more rarely encountered groups (Cleland and Levick, 1974b), often gave rather asymmetrical responses to the two directions of movement, which varied somewhat with stimulus speed. For example, one sluggish transient neurone gave a centre-activated response to both directions of movement at low stimulus velocities (2”/sec), was highly direction selective at higher stimulus velocities (m”/sec) but responded equally well to both directions of stimulus movement at lOO”/sec. In some cells in the striate cortex and the lateral geniculate nucleus, response magnitude falls OK significantly when the length of a moving bar exceeds a certain value (Dreher, 1972; Dreher and Sanderson. 1973; Hubel and Wiesel, 1962, 1965; Rose, 1974). To determine how far this phenomenon is present in the retina, we measured the centre-activated responses of the various cell types to moving bars of various lengths. With short bars, even though the cell might respond vigorously as the bar passed over the centre, decreases in firing before and after the peak were much less pronounced than with longer stimuli, since with small stimuli insufficient spatial summation is present to evoke these effects from the surround region. Figure 6 shows the relationship between bar length and response magnitude for the various cell types Brisk sustained cells show an increase in response magnitude up to bar length of OS-l.O”, followed by a small but definite decrease with longer stimuli whose ends swept over the surround. Mean- decrease in response to longest bar relative to maximal response was 22% Dreher and Sanderson (1973) show
that much a more marked decrease in response with increasing bar length may occur in the lateral geniculate nucleus, presumably due to inhibitory interactions within that nucleus. For brisk transient neurones, increasing the stimulus length produced a more gradual increase in response magnitude, corresponding to the larger centres of these cells. Only in one neurone, shown in Fig. 6, was there a substantial decrease in response magnitude with longer bars and this cell’s receptive field was very near the area central& where brisk transient units have a stronger centre-surround organization (Cleland and Levick. 1974a). For other cells, response magnitude showed only a slight decrease for bar lengths longer than optimal (mean decrease 8%). Unfortunately, comparable data are not available for transient cells in the lateral geniculate nucleus, but it would be expected that intrageniculate inhibition would make bar length a more critical variable for these cells also. For sluggish cells, bar length was a critical determinant of response magnitude for sluggish transient neurones (mean decrease 72%) and this is apparent in Fig. 6. For sluggish sustained neurones, increasing bar length beyond an optimal value did not substantially decrease response magnitude (mean decrease 6%). DISCUSSION
Neuronal responses to moving contours at lower levels in the visual pathway have received relatively little attention despite the importance of this type of stimulus in the striate cortex. Rodieck and Stone (1965) studied the response of retinal ganglion cells to moving stimuli. The histograms they show are very similar to those of brisk sustained ganglion cells in the present study, so it is likely that the bulk of their sample was from this cell type. A further description
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B. B. LEEand D. J.
of retinal ganglion cell responses to moving stimuli was provided by Hamasaki. Campbell. Zengel and Hazelton (1973). who classified ganglion ceils according to the prssence or absence of a dip in that part of the response histogram associated with the surround prior to the centre-activated peak. This classification may be related to the weaker surround mechanism of brisk transient relative to brisk sustained neurones. but in out experience the presence or absence of a dip was a poor predictor of whether a cell was sustained or transient. since the dip was highly dependent on stimulus shape. and also, for brisk transient cells. on retinal locus of the receptive field: transient cells near the area centralis have stronger surrounds than more peripherally situated neurones of this type (Cleland and Levick. 1974). Linear spatial summation within the receptive fields of brisk sustained (X) cells has now received substantial experimental confirmation. at least near threshold. under quite stringent conditions (C)eland and Enroth-CugeiL 1968; Enroth-Cugell and Pinto. 1972; Enroth-Cugell and Robson. 1966; Hochstein and Shapley. 1976a). and Rodieck’s model. based on this property. effectively generates the centre-activated responses of brisk sustained units (Rodieck, 1965). However, although brisk transient ganglion cells clearly have a non-linear element in their receptive field structure [Enroth-Cup11 and Robson, (1966) and Hochstein and Shapley, (1976a. b) though in the latter reference it is suggested that this non-Enear element is superimposed on a linear centre-surround organization], responses of brisk sustained and transient units are qualitatively similar. Further. we found that for both brisk sustained and transient cells, centresuppressed responses are approximately inverted images of centre-activated responses (assuming that some of the components of the response are hidden below the baseline of the response histogram). This is another property of a spatially-linear model. Whatever model is constructed to account for the behaviour of a brisk transient cell. it must (I) be spatially symmetrical (whether linear or non-linear) since the responses to both directions of movement are identical; (1) the excitatory and inhibitory components of the model must combine in such way that centre sup pressed are inverted centre-activated responses. A linear combination law is a simple way of satisfying these conditions. The results presentzd here allow us to draw certain conclusions concerning the transfer of information to higher levels in the visual pathway. When stimulus speeds suitable for simple striate cortical neurones are used. the centre-activated responses of brisk sustained and transient neuronss are comparable in magnitude. On the other hand. firing frequency during the response peak as the stimulus leaves the centre and enters the surround in centre-suppressed responses is much higher in brisk sustained units than in brisk transient cells. though the number of impulses delivered per response is similar. Now the optimal stimulus velocity for complex cortical cells is greater than that for simple cortical cells [IQ” compared to 7.?/sec; Movshon (1975)] and a correlation with the brisk transient and brisk sustained pathways has been suggested. However. it is clear from Figs. 4 and 5 that the centre-activated responses of brisk transient
WILLSHAN
cells are more vigoroIrs than those of brisk sus:amed cells only at speeds higher than those effectiw in striate cortex. Differences between ~ntre-suppressed responses of brisk sustained and transient ceils are more marked. but seem to be quantitative rather than qualitative. Presumably both the number of impulses per response and the frequency with which they are delivered play a role in determining the optima) stimulus speed for neurones in the lateral geniculate nucleus and cortex. Though some information is available concerning transformations in optimal stimufus speed between retina and striate cortex (Fig. 5: Dreher and Sanderson. 1973: &lovshon. 1975) differences in speed selectivity at these various levels
clearly require further study. The slowly-conducting sluggish pathway provides a major input to the superior colliculus (Cleland and Levick. 1974,; Fukuda and Stone. 1974). Lzaving aside the rarely-encountered types of retinal ganglion ceils (Cleland and Levick. 1974b). our results suggest that two different types of information are carried by sluggish transient and sustained axons. The former cell type responds optimally to small stimuli, and responds phasically as the edges of large targets pass across the receptive field. Sluggish sustained cells are less selective; they respond as long as a target covers the receptive field centre. irrespective of target size.
rlcfcnolvle~~e~~~enis--During part of this work B.B.L. was supported by the Wellcome Trust and D.J.W. by the Alexander von Humboldt Stiftung. We would like to thank B. G. Cleland for introducing us to direct retinal recording techniques and 0. D. Creutzfeldt for critical reading of the manuscript.
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