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Representation of the visual streak in visuotopic maps of the cat's superior colliculus: Influence of the mapping variable
llsion Rcs. Vol. 23. No. 5. pp. 507-516. Printed in Great Britam
OK?-6989/83/05050710 SO3.0010 Pergamon Press Ltd
1983
REPRESENTATION OF THE VISUAL STREAK IN VISUOTOPIC MAPS OF THE CAT’S SUPERIOR COLLICULUS: INFLUENCE OF THE MAPPING VARIABLE JAMESI’. MCILWAIN Division of Biology and Medicine, Brown University, Providence. RI 02912. U.S.A. (Received 28 .Jurle 1982; in reoisedforrn 7 September 1982)
Abstract-A series of visuotopic maps has been prepared from recordings of electrical potentials related to W-cell aRerent activity in the cat’s superior colliculus. These maps clearly exhibit an expected exaggeration of the representation of the upper visual field, due to tilt of the retina’s visual streak in the ‘position of paralysis’. This asymmetry disappears when the visual field’s coordinate system is rotated by an angle equal to the tilt of the axis of the nasal streak. Previously published maps, based on recordings from postsynaptic colhcular units, have failed to reflect this tilt of the nasal visual streak, perhaps in part because the centers of unit receptive-fields are biased estimators of the retinal origin of axons terminating near a collicular recording site. Cat
Superior colliculus
Retinotopy
Visual streak
INTRODUCTION
maps based on physioiogi~l recordings have provided detailed information on the connectional geometry of the visual pathways and it is likely that such maps will continue to have a key role in studies of spatial processing in vision. Nonetheless, the interpretation of visuotopic maps is not a straightforward matter. The patterns of intersecting isopleths which form the maps can but poorly convey the complexity of spatial transformations that are occurring. Moreover, the maps are highly schematic summaries of experimental procedures which often involve essentially practical choices of stimulus parameters and response measures. For instance. it is common practice to use as mapping variable the geometric centers of neuronal receptive-fields plotted for a given recording site. One implication of the results reported here is that use of this mapping variable can have a significant effect on the coordinate structure of the resulting map. The experiments were concerned with the rep resentation of the retina’s fist& strt& in the superior colliculus of the cat. The visual streak. found in the retinas of cats and many other vertebrates. is a specialized region in which ganglion cells occur at higher frequency than elsewhere in the retina (Slonaker, 1897: Stone, 1965; Hughes, 1975). The visual streak contains the area centralis and extends temporally and nasally from it, but is most prominent in the nasal retina. According to Stone and coworkers (Rowe and Stone, 1976; Stone and Keens, 1980). the cat’s visual streak is formed principally by the smallest (W) ganglion cells. but the largest (Y) ganglion cells also contribute Visuotopic
(WPssIe et al., 197.5).It is not clear to what degree the medium size ganglion cells are involved (Rowe and Stone, 1976, Stone and Keens, 1980; Hughes, 1981). In keeping with its plethora of gang&on cells, the visual streak receives a Iarger representation in central visual structures than do surrounding regions of the retina. In the cat, this magnification of the region dividing dorsal and ventral retina may be seen in published visuotopic maps of the superior coiliculus (Apter, 1945; Straschill and Hoffmann. 1969; Hoffmann. 1970; Feldon ef a(., 1970: Berman and Cynader, 1972), the lateral geniculate nucleus (Sanderson, 1971) and the striate cortex (Bilge et al., 1967; Tusa er al., 1978). It is reasonable to assume that these regions of high magnification receive information from the visual horizon in waking cats, although the evidence for this is not conclusive (see Discussion in Cooper and Pettigrew, 1979b). On the other hand, it is now clear that, under the usual conditions of visuotopic mapping studies, the nasal limb of the cat’s visual streak is not oriented horizontally. Muscular paralysis by the commonly used agents causes intorsion of the upper margin of the cat’s eyeball (Bishop et al., 1962; Nelson et al., 1977; Cooper and Pettigrew. 1979b), an action which tilts the nasal streak inferiorly with respect to a nasotemporal (horizontal) axis through the area centralis (McII~in, 1977; Cooper and Pettigrew. 1979b). As a result, the upper visual field is served by more contralaterally projecting, nasal retinal ganglion cells than is the lower visual field. Thus, one might expect to find an exaggerated representation of the upper visual field in visuotopic maps made through the contralateral eye, particularly in the superior colliculus, whose di507
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rect retinal input consists largely of W-cell axons from the contralateral retina (Fukuda and Stone, 1974: Cleland and Levick, 1974; KelIy and Gilbert, 1975). As noted already, W-cells form a major component of the cat’s visual streak. In general, published visuotopic maps of the cat’s superior colliculus do not exhibit this expected exag geration of the representation of the upper visual field (Feldon et a[., 1970; Berman and Cynader. 1972).* However, in a map based on “unresolved neural activity” recorded just beneath the stratum zonale, the upper held’s magnification factors (Daniel and Whitteridge, 1961) exceed those of the lower field, especially in posterior regions of the map (see Fig. 2 in McIlwain, 1975). It is now known that these recordings were made in a collicular zone densely populated by the terminals of W-cell axons origjnating in the contralateral retina (Sterling, 1973; McIlwain, 1978; Itoh et a/., 1981). Extracellular electrodes in this “juxtazonal” region record potentials (“Juxtazonal Potentials” or JZPs) apparently associated with synaptic currents generated by the discharge of individual W-cell axons (McIlwain, 1978). Thus, a map based on such recordings may be essentially a map of the W-cell projection to the colliculus from the contralateral eye. Furthermore, the JZPs do not arise from regenerative responses in postsynaptic elements. so their spatial distribution would be little influenced by convergence networks within the collicuius itself. It is possible. then, that a JZP-based map would reveal the tilt of the visual streak because its topography is a direct reflection of afferent distribution patterns. To pursue this question further, a series of visuotopit maps of the colliculus was prepared from recordings of JZPs. All of these maps exhibited a disproportionate magni~cation of the upper visual field which disappeared when the visual fields coordinate system was rotated by an angle equal to the tilt of the axis of the nasal streak. It is shown how this feature of the retinotectal projection might fail to appear in a map based on the centers of receptive-fields of postsynaptic collicular neurons. METHODS
The maps described here are from 5 aduit cats and are based on data published in part in an earlier report (Mcllwain, 1977). Each animal was anesthetized with i.p. pentobarbital (40 mgikg) and mounted in a stereotaxic instrument modified to give the eye an unobstructed view of a tangent screen 75cm away. The skull and dura were removed near the midline to
*Maps published by Straschill and Hoffmann (1969) and by HotTmann (1970) also exhibit no exaggeration of the upper visual field. However. these maps were obtained with binocular stimulation and are not strictly comparable to the other maps cited here. which were based on stimulation through the contralateral eye.
provide access to the superior colliculus through the overlying occipital cortex. Scalp edges were secured to a metal ring and an oil pool was formed over the exposed cortex. Paralysis was achieved by intravenous infusion of Flaxedil (20 mg:hr). artificial respiration was provided. expired CO2 was monitored and maintained between 3.5 and 4.5”,, and body temperature was controlled at 3X C. In preparation for stimulation. the horizontal alignment of the stereotaxic frame was checked with a spirit level and the infraorbitaf bar was removed from beneath the stimulated eye. The axis of the slit pupil of this eye was measured repeatedly. as described elsewhere (McIlwain. 1977). until a stable value was reached. These angles with respect to gravitational vertical ranged from 5.5 to 8.0. (mean 6.8.. SD = 1.Y). If symmetry of the two eyes is assumed. the angle between the pupil axis. as they converge over the cat’s head, would range from 11 to 16 . which is comparable to values reported by others for the “position of paralysis” (Bishop er al.. 1962: Nelson et al., 1977; Olson and Freeman, 1978: Cooper and Pettigrew, 1979b). The pupil of the stimulated eye was then dilated with a&opine and the nictitating membrane was contracted with phenylephrine. The other pupil was not dilated and remained constricted for the duration of the experiment. Piano contact lenses were applied to both corneas and an opaque patch covered the unstimulated eye. Quality of focus was assured by substituting spectacle lenses before the stimulated eye while examining the retinal image of an illuminated grid located at the tangent screen, The tangent screen was diffusely illuminated at 5 cd/m’. The superior colliculus contralateral to the stimulated eye was explored with varnished tungsten microelectrodes in a series of vertical penetrations spaced 0.5 mm apart (Fig. I). Between 62 and 76 penetrations were made in each cat. The electrode tip was positioned in each track for optimal recording of JZPs (McIlwain, 1978) and electrolytic lesions at selected recording sites permitted subsequent reconstruction of the penetration grid from serial Nisslstained frozen sections (Fig. 1). JZPs were evoked by a small light spot (60-80 cd/m’) moved very slowly on the tangent screen. The response-fields. plotted for each track on a sheet of paper attached to the tangent screen, ranged in diameter from less than 0.5~ near the area centralis to about 5’ in more peripheral parts of the visual field.
Distances were measured from the geometric centers of the JZP response-fields to vertical and horizontal axes intersecting at a working reference pole on the tangent screen. For two cats, this pole was the intersection with the tangent screen of a normal from the eye. For three cats. the image of a prominent retinal vascular bifurcation was plotted on the screen at short intervals, using the method of Fernald and Chase (1971). Correction for residual eye movements
Fig. I. Histological section from a mapping experiment. The arrow points to an electrolytic lesion made just beneath the surface at,a recording site. Numerous descending electrode tracks may be seen in the cerebral hemisphere above the colliculus. Elevation data from the row of penetrations at this level are shown in Fig. 2. Calibration line: I mm.
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Visual streak and collicular retinotopy
r
t
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Rostra1
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Caudal
IO” -
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P 2 w
HM
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I123412345 Distance from midline,
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Fig. 2. Typical data from which maps were constructed. Points correspond to the elevations, with respect to the visual axis and horizontal meridian, of JZP response-fields observed in two mediolateral rows of penetrations in the same cat. The curve marked “Rostral” is from a row of penetrations near the representation of the area centralis. The curve marked “Caudal” is from a row at the level of the histological section in Fig. I. The point marked by an asterisk corresponds to the recording site at the lesion in Fig. I. Ordinate: elevation in visual field above zero horizontal meridian. Abscissa: distance from the midline of the brainstem. HM : horizontal meridian of visual field. was achieved by stating a given response-field’s position with reference to the current projection of this retinal landmark. A PDP-I2 computer was employed to convert the tangent screen distances to spherical coordinates using the expressions of Bishop er al. (1962). From plots of these coordinates. the tangent screen locus corresponding to the region of highest magnification was located and assumed to be the projection of the area centralis. Thus. this reference point of the map was established from the internal structure of the map data and not by ophthalmoscopic estimation. The computer then made this point the origin of the response-field coordinate system. Similarly. the projection of the axis of the visual streak was determined by locating the region of highest vertical magnification at different distances from the projection of the area centralis (McIlwain. 1977: Fig. 2). The tilt of the visual streak with respect to the zero horizontal meridian of the visual held (henceforth called simply the horizontal meridian) was determined from the estimated loci of the streak axis using the expression: tan(Elevation) = A x sin(Azimuthl + B. The values of slope, A. obtained with this explicit expression were virtually identical to those calculated by assuming an approximately linear relationship between elevation and azimuth for points near the origin (Mcllwain, 1977). Combining response-field coordinates with the penetration grid yielded sets of curves for each animal which related collicular loci to visual field azimuths and elevations (Fig. 2). Selected isoazimuth and iso-
elevation lines derived from these curves were projected to a horizontal plane by normals to that plane. Thus, the maps are orthographic projections giving a dorsal view of the collicular visuotopic patterns. These maps were placed within profiles of the boundaries of the smmm yriseunl superjicialr determined by serial histological reconstruction. No shrinkage correction was applied to these profiles. An average map was also prepared after photographically normalizing the individual maps so that the anteroposterior diameters of the colliculi equalled 4.5 mm. The maps were then superimposed at azimuth 20’. elevation 0” and averaged by computer. A second series of five individual maps and their average was obtained following computer rotation of each set of map data by an angle equal to the tilt of the visual streak. All maps are presented as though they were obtained from the left superior colliculus. RESULTS
Figures 1 and 2 illustrate the nature of the data used to generate the present maps. The arrow in the histological section of Fig. I points to an electrolytic lesion made at one of the recording sites. Since the recordings were made with the microelectrode’s tip just beneath the collicular surface, it was usually impossible to see recording points at which lesions were not placed, although the tracks of the penetrations were evident in the overlying hemisphere (Fig. 1). Figure 2 shows a plot of the elevations of JZP response-fields recorded in this row of penetrations (curve marked “Caudal”) as well as those obtained in a more rostra1 row near the representation of the area centralis (curve marked “Rostral”). It may be seen that the region of highest vertical magnification (minimal slope) in the caudal curve lies above the horizontal meridian, suggesting that the nasal streak was tilted as predicted. Maps obtained from the five cats used in this study are presented in Fig. 3A. In each of these maps and in their average (Fig. 4A) it is evident that the upper visual field is disproportionately represented. This is most prominent posteriorly where there is marked asymmetry in the vertical magnification factors about the projection of the horizontal meridian (labelled HM) and crowding of the isoelevation lines in the posterolateral quadrant of the maps. If this asymmetry is due to tilt of the nasal streak. then rotation of the visual field’s coordinate system by an angle equal to the tilt should eliminate or greatly reduce the asymmetry. This follows from the assumption that magnification factors are proportional to retinal ganglion cell densities and from the fact that the nasal streak is an axis of symmetry for isodensity contours in topographic maps of ganglion cell distribution (Stone, 1965; Hughes, 1975, 1981; Stone and Keens, 1980). The results of rotation shown in Figs 3B and 4B are consistent with this prediction. The magnification factors become approximately equal at corre-
JAMES T. MCILWAIS
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A
medial
lmm Fig. 3. Topography of retinocollicular projection in five cats as determined from JZP recordings. Maps formed by connectmg selected coordinate points by line segments. Additional isoazimuth and isoelevation lines available for some maps deleted for clarity. Coordinate labels for all five pairs of maps correspond to those of the leftmost map of row A. Row A: The zero isoelevation line (HM in leftmost map) is the projection of the horizontal meridian of the visual field. Row B: Same dam as m A but rotated so that the zero isoelevation line corresponds to the projection of the itxis of tho nasal visual streak (VS in leftmost map).
sponding loci medial and lateral to the zero isoelevation line. which now represents the projection of the visual streak (VS) and which inclines medially as it runs from anterior to posterior across the colliculus and intercepts the isoazimuth lines at right angles. The projection of the streak axis can be seen to divide
the projected surface of the colliculus about equally between upper and lower visual tields. The isoazimuth projections are changed little by the rotation procedure. since near the horizontal meridian they are essentially parallel to the direction of rotation. Despite differences in the shape of the colliculnr
medtal A
1 mm
Fig. 4. Average maps of retmocollicular projection as determined from JZP recordmgs. (A) Normalized average of maps in Fig. IA, in which zero isoelevation line corresponds to horrzontal meridtan (HMI. (B) Normalized average of maps in Fig. IB, in which zero isoelevation line corresponds to projection of nasal visual streak (VS). Format as in Fig. 1. See Methods for normalization procedure. Ipsilateral field coordinates are not illustrated in these average maps.
Visual streak and coificular retinotopy borders. variations in ~ollicular surface curvature and a host of other inherent and experimental sources of v~~riability. the maps of Fig. 3B are rem~~rk~~blysimilar from animal to animal. For instance. the central 20 by 20’ region. bounded by isoazimuths 0 and 20. and isoelevations f lo’, occupies 30 + 2”, (mean f SD) of the total projection area of the superficial gray, even though the latter varies from 17.8 to 25.5 mm2 (mean 20.3. SD 2.9 mm2). The internal scaling of the maps also differs little from animal to animal. Other general features of the maps of Figs 3 and 4 are consistent with earlier reports and need not be treated in detail here. Requiring mention is the represent~~tion of the ipsilateral hemifield at the anterior margin of the colliculus. first noted by Straschill and Ho~rn~~nn (1969) and subsequently documented in detail by others (Berman and Cynader. 1972: Feldon et ul., 1972: Lane et ul.. 1974). The present maps agree with previous reports in allotting approximately the anterior I mm of the superficial gray to the ipsilateral visual field. but a caveat is warranted here. The zero isoazimuth lines in the present maps are arbitrarily defined with respect to tangent screen axes perpendicular either to the horizontal meridian or to the projection of the axis of the nasal visual streak. Therefore, the zero isoazimuth lines need not correspond to retinal features such as the nasotemporal raphe, which may not be per~ndicul~tr to the nasal streak (Cooper and Pettigrew. 1979b) or to the “zero meridian” of Cooper and Pettigrew ( f979a.b), which is defined by functional connections to binocular cortical units (see also Nikara er u/.. 1968: Joshua and Bishop, 1970; Sanderson. 1972).
DISCUSSlOX
When the cat‘s eye is in the “position of paralysis”. the nasal limb of the visual streak is not horizontal but is tilted downward on the retina. This tilt is apparent in maps of the retinocollicular projection based on recordings of synaptic activity generated by the crossed W-cell input. This result is not due to distortion of the data sample by one exceptional animal. since the phenomenon is present in each of the maps of Fig. 3A. It is also unlikely that a fortuitous selection of animals with marked ocular intorsion was studied, since the range of pupil angles observed in these cats was comparable to that reported by others. Tangent screen distortions were eliminated by calculating the spherical coordinates of the response-fields and possible effects of eye movements were reduced by periodic monitoring of eye position and by appropriate tr~lnsformation of the dnta. Finally. since the representation of the area centralis was estimated from the internal structure of the map. errors stemming from ophthalmoscopic estimates were avoided. Thus. the asymmetries of the map of Fig, 4A are probably not attributable to the more common sources of manning errors and mav_ be oresumed to .. _ .
513
reflect the tilt of the visual streak in the “position of paralysis”.
Earlier maps agree that the representation of the horizontal meridian begins anteriorly about midway between medial and lateral borders of the colliculus and drifts medially as it proceeds posteriorly. In the present maps. this trajectory corresponds to the projection of the visual streak, whereas that of the horizontal meridian drifts laterally. giving a disproportionate representation to the upper visual field. This is the most striking discrepancy between the present map and those published previously. Small errors in estimating the tangent screen projection of the area centralis can produce relatively large errors in visuotopic maps because of the large magnification factors at central representations of this retinal zone. It is unlikely, though. that this is the major source of the differences between Fig. JA and earlier maps, because such errors should not have been in the same direction in all previous studies and because the resulting discrepancies should have been more conspicuous in anterior than in posterior regions of the map, while just the converse was found. Earlier work was also carried out in paralyzed cats and, with the exception of one study. the animal’s eyes were presumably in the ‘position of paralysis”. Feldon er al. (1972) state that in their study “The contralateral (right) eye was aligned by attaching sutures to the conjunctiva, [and ] orienting the vertical slit pupil in the proper axis. . . ” (p. 135).The map resulting from this study exhibits an exceptionally steep medial drift of the projection of the horizontal meridian and an exaggerated representation of the irlfrrior visual field. This coordinate pattern would result were the nasal streak rotated so that its tangent screen projection lay in the lower visual field. a situation which may possibly have occurred during attempts to orient the slit pupil vertically. Under this condition, the projection of the horizontal meridi~tn would lie increasingly medial to the line marked VS in Fig. 4B for increasing values of eccentricity.
Yet another factor which may account for differences between the present and earlier visuotopic maps of the colliculus is related to the practice of using as mapping variable the centers of the receptive-fields of post-synaptic neurons. It is well established that microelectrode penetrations through the colliculus are likeiy to encounter cells with relatively large receptive-fields, ~rti~ularly in caudal regions representing the periphery of the visual field (McIlwain and Buser, 1968; Sterling and Wickelgren, 1969). These receptivefields can incorporate areas of visual space having disparate magnifications in the afferent map, with the result that collicular regions equidistant from the cell body do not have equal representation in the recep tive-field. Thus, the center of the receptive-field may
514
JAMES T. MC~LWAIS
AZIMUTH Fig. 5. Influence of receptive-field center measurements on estimated projection of horizontal meridian (A) Typical map from Fig. IA (second from left in that figure) based on horizontal meridian projection as determined from JZPs. Projection of axis of visual streak indicated by dashed line. Elliptical profiles are hypothetical RFIs of cells recorded at penetration sites indicated by large dots. (B) Receptive-fields of cells I-3 of part A. as mapped on the tangent screen. HM-horizontal meridran.
not provide an accurate estimate of the retinal origin of axons terminating near the recording site. The
potential effect of this phenomenon on a visuotopic map of the colliculus is illustrated in Fig. 5 with the aid of a graphical device which summarizes the relationship between a recording site and the boundaries of the receptive-fields of cells recorded there. It has been shown elsewhere (McIlwain. 1975: Capuano and McIlwain. 1982) that when collicular receptive-fields are plotted in a map based on JZPs, the resulting profiles are centered on the recording site and are generally oval and maximally 2 x 3 mm in size. with their long axes oriented mediolaterally. The interpretation of these profiles. called ReceptiveField Images or RFIs. does not concern us here, but we may take advantage of the empirical fact that their form and location with respect to a recording site are known. By drawing hypothetical RFls of the expected dimensions on :I JZP-based map. one can infer the shapes and locations of receptive-fields likely to be observed at ;I particular recording site. A typical map from Fig. 3A is reproduced in Fig. SA with the projection of the nasal streak indicated by a dashed Ime. lsoazimuth lines have been added at I5 ;md 50 Large dots mark the sites of three mapping penetrations. two of which fall on the projection of the horizontal meridian. Centered on these dots are k~porl~ricul RFls of moderate size, as might be observed for cells recorded in each mapping penetration. In Fig. 5B are shown the corresponding receptivefields 01 these cells. The receptive-field of cell I is centered near the horizontal meridian. but since the RFI of cell 2 encompasses more of the lower than the upper visual held. the center of its receptive-field lies below the horizontal meridian. Thus. a mapping ex-
periment based on locations of receptive-held centers would assign the locus of cell 2 to the lower quadrant of the visual field. The RF1 of cell 3 has been positioned so that the corresponding receptive-lield in Fig. SB is approximately centered on the horizontal meridian. The center of this receptive-held would indicate that the locus of ceil 3 receives the projection of the horizontal meridian. whereas it actually lies near the projection of the visual streak. Because of the marked asymmetry in vertical magnification about the projection of the horizontal meridian. only penetrations medial to it and near the projection of the vislral streak’s axis are likely to yield receptive-fields centered on the horizontal meridian. particularly in posterior regions of the map. As suggested in Fig. 5. if receptive-fields such as these were used to generate ;I visuotopic map, the apparent prqjection of the horizontal meridian would tend to “track” the projection of the visual streak ;IS it moves posteriorly and medially. Other consequences of this phenomenon may be appreciated by placing RF1 boundaries in different parts of the map of Fig. 5A. For instance. penetrations 0.5 mm medial and lateral to that containing cell 3 would yield receptive-fields centered about IO‘ above and below the horizontal meridian. respectively. This would have the effect of reducing the asymmetry in the vertical magnification factors for this while shifting the isoelevation contours region, toward the zero isoelevation line. Such exercises are useful for visualizing potential interactions between cell location. magnilication factors and the resulting map measurements. but it should be emphasized that the RFls in Fig. 5 were chosen to illustrate the point of this discussion. They
515
Visual streak and collicular retinotopy
do not correspond to the smallest or the largest RFls observed for collicular cells. nor are they necessarily representative of cells encountered in earlier mapping experiments. It is clear, though, that the larger the receptive-field. the larger will be the effect of the phenomenon illustrated in Fig. 5. Moreover. the direction of the bias introduced by the large receptivefield will vary depending on where in the map the penetration occurs. This phenomenon may account in part for the considerable dissimilarities in coordinate structure apparent in earlier maps based on samples of coilicular receptive-fields. Differences are particularly striking between studies which included data from the deep collicular laminae (Straschill and Hoffmann, 1969; Hoffmann. 1970), where most cells have very large receptive-fields (Gordon, l973), and those in which recordings were limited to the superficial layers (Feldon et al., 1970; Berman and Cynader, 1972), where small-field cells may be encountered. The present map (Fig. 4B) closely resembles that of Berman and Cynader ( 1972). except that their map places the representation of the horizontal meridian where Fig. 4B shows that of the nasal visual streak. Since Berman and Cynader used receptive-fields up to 30” in diameter to develop the peripheral parts of their map, the phenomenon described above may account in large part for the differences between our results.
These results indicate that the choice of mapping variable can have a significant effect on the coordinate pattern of a visuotopic map of the superior colliculus. Analogous phenomena may occur in other visual structures where unit receptive-fields are very large, such as the lateral supr~lsyivian cortex (Spear and Baumann, 1975; Palmer er nl.. 1978), and the visual areas of the posterior thalamus (Suzuki and Kato, 1969; Godfraind er ul., 1972: Chalupd and Fish, 1978; Mason. 1978). The choice of mapping variable may make little difference if one is interested only in detecting an
orderly representation of the visual field or in the general form and boundaries of a projection. Its importance increases as quantitative information is needed about the spatial distribution of magnification factors. The present experiments offer an instance where such information permitted a more accurate assessment of the projection of the nasal streak than has hitherto been possible. Of greater interest is the possibility that visuotopic maps. and their constituent magnification factors, can be used to analyze the spatial distribution of neural activity produced by visual stimuli. For instance. inverse correlations between magnification factors and receptive-field Dimensions in striate cortex and superior collicuius have suggested that a relatively constant volume of tissue in each of these structures analyzes information from any visual point. regardless of its position in the visual field (Hubel and Wiesel, 1974: Albus, 1975; McIlwain, 1975. 1976: but cf. Dow et at., 1981). For the
superior colliculils, this neural “point image” has been shown to have a regular geometric relationship to the receptive-field images of the large-field cells, if these are plotted in a JZP-based map (McI~wain, 1975; Capuano and Mcilwain, 1981). Discovery of such relationships depends on having the appropriate map or spatial distribution of magnification factors and, since different mapping procedures can lead to different coordinate patterns, not all maps will be equivalent in this respect. Perhaps one useful index of the “validity” of a particular map might be its capacity, when combined with other information such as receptive-field size, to reveal invariance relationships such as those just mentioned. AcX-ilo~fpdyetttertrs-Ithank Drs David M. Eerson and Jonathan Stone for valuable comments. Dr Joseph Corless for help with computer chores and MS Anne Boyd for typing this paper. Drs W. C. Hall. C.-S. tin and Nell Cant also provided useful comments and generous hospitality during the phase of the work carried out at Duke University. This research was supported by PHS Grant EY 02505, by bequests from the Grass Foundation and by a Faculty Scholar Award from the Josiah Macy Jr Foundation.
REFERENCES Apter J. (1945) Projection of the retina on the superior colliculus of cats. J. ~e~rop~z~sio~.8, 12%134. Berman N. and Cynader M. (1972) Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats. J. Physiol. 224. 363389. Bilge M., Bingle A., Seneviratne K. N. and Whitteridge D. (1967) A map of the visual cortex of the cat. J. Ph#o/. 191, 116-l ISP. Bishop P. O., Kozak W. and Vakkur G. J. (1962) Some quantitative aspects of the cat’s eye: axis and plane of reference, visual field coordinates and optics. J. Phrsiol. 163.466-502. Capuano U. and McIlwain J. (1981) Reciprocity of receptive field images and point images in the superior colliculus of the cat. J. conip. Neural. l%, 13-24. Chalupa L. M. and Fish S. E. (1978) Response characteristics of visual and extravisual neurons in the pulvinar and lateral posterior nuclei of the cat. Esp/ Neural. 61. 96-120. Cleland B. G. and Levick W. R. (1974) Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. J. Physiol. 240, 457-492. Cooper M. L. and Pettigrew J. D. (1979a) A neurophysiological determjnation of the vertical horopter in the cat and owl. J. coitt,e. Neuroi. l&I. l-26. Cooper M. L. and Pettigrew J. D. (1979b) The decussation of the retinothalamic pathway in the cat, with a note on the major meridians of the cat’s eye. J. camp. Neural.
187, 285-312. ltoh K., Conley M. and Diamond I. T. (1981) Different distributions of large and small retinal gangiion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior~coll~culus. Bruits Res. 207, 147- 152. Joshua D. E. and Bishop P. 0. (1970) Binocular single vision and depth discrimination. Receptive field disparities for central and peripheral vision and binocular interaction on peripheral single units in cat striate cortex. E.upf Brain Res. 10, 389-416.
Kelly J. P. and Gilbert C. D. (1975) The projection of different morphological types of ganglion c&s in the cat retina. J. cornp. Nrtcrol. 163. 65-X I. Lane R. H.. Kaas J. H. and Allman J. M. (IY74) Visuotopic organization of the superior colliculus in normal and Siamese cats. &f&i Res. 70. 4 13-430. Mason R. (1978) Functional organization of the cat‘s pulvinar complex. E.ypl Bruits Rex 31. 51-66. Mcllwain J. T. (1975) Receptive fields and their images in the superior colliculus of the cat. J. .~ettropl!~,~ioi. 38, 2 19-730. McIlwain J. T. (19761 Large receptive Gelds and spatial transfor~tions in the visual system. Iut. Rc. Plrysiol. 10. 223-248. McIlwain J. T. (1977) Orientation of slit pupil and visual streak in the eye of the cat. J. camp. .A’cwrol. 175, 337-344. Mcllwain J. T. and Buser P. (196X) Receptive fields of single cells in the cat’s superior colliculus. Ezpf Bwir~ Res. 5, 314-325. Nikara T., Bishop P. 0. and Petiigrew J. D. (1968) Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Erpl Brain Res. 6, 353-372. Olson C. R. and Freeman R. D. (1978) Eye alignment in kittens. J. Neuroph.&ol. 41, 848-859. Palmer L. A., Rosenquist A. C. and Tusa R. J. (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J. camp. New-of. 177, 237-256. Rowe M. H. and Stone J. (1976) Properties of ganglion cells in the visual streak of the cat’s retina. J. corrrp. &eurol. 169, 99- 126. Sanderson K. J. (1971bThe projection of the visual field to
the lateral prntculate and medial Interlamln:ir nuclct 111 143. IO- IIR. Sanderson. K. J. ( 1972) Does rolling of the c>e 11ccur1n the anesthetized paralysed cat” t.i,s;rt~!RP\. 12. IO-15 iO.iO Slonaker J R. (1x97) A comparatl\c stud! of the ~uc‘t 01 acute vision m vertebrate,. J. .\lwp/r. 13, I-Ii St).? Spear P. D. and Baumann T. P. (lY??l Rcccptnc-held characteristics of s~nyle ncurom tn lateral hupras! I\ 1~1 visual area of the cat. J. .\ m~~p/~~~.~ir~/. 3X. I-LO.? Il3). Sterling P. (1973) Quantitative mapptng with the clcctron microscope: retinal terminals rn the superior ct~llrculu> the cat. J. t&np. ,Swro/.
&via Rrs. 54, 347-221.
Sterling P. and Wickelgren 3. G. (IYhY) Vtsu:tl receptitc fields in the superior collicuius of the c;it. .f \ ~~rtr~~{~i~ \siol. 32. I 1.5. Stone _I.( IYh5) A quantitative anal!sls of the dlstrihutt<)n 01 ganglton cells in the cat‘s retma. J. IYW~. \ wan/. 12-I. 337-331. Stone J. and Keens J. ( IYStJ) Dtstrihution of sm;tll and medium-sized ganglion cells in the citt‘s retina J. r~~n~~. Yrtrrol. 192. :35-246. Straschill M. and Hoffmann K.-P. ( 19691Functmnal aspects of localization in the cat’s tectum opttcum. Hr[ri~t Rrs. 13. 274--‘82. Suzuki H. and Kato H. j 1969) Neurons \\ith Gual properties in the posterior group of the thalumic nuclei. Ev,li ,%‘e~t&.23, 353--365. Tusa R. J.. Palmer L. A. and Rosenquist A. c‘. (IY7SI The retinotoplc organization of area I 7 tstriate cortex) ui the cat. J. CY~~~J,,~rrrro/. 177. 2 I3 236. WBssle H.. Levick W. R. and Clcland B. G. (I’)751 The distribution of the alpha type of g;mglion cells in the cat’s retina. J. c’ornp. .l’cwoi. 159. -1lY-4.3s.
OK?-6989/83/05050710 SO3.0010 Pergamon Press Ltd
1983
REPRESENTATION OF THE VISUAL STREAK IN VISUOTOPIC MAPS OF THE CAT’S SUPERIOR COLLICULUS: INFLUENCE OF THE MAPPING VARIABLE JAMESI’. MCILWAIN Division of Biology and Medicine, Brown University, Providence. RI 02912. U.S.A. (Received 28 .Jurle 1982; in reoisedforrn 7 September 1982)
Abstract-A series of visuotopic maps has been prepared from recordings of electrical potentials related to W-cell aRerent activity in the cat’s superior colliculus. These maps clearly exhibit an expected exaggeration of the representation of the upper visual field, due to tilt of the retina’s visual streak in the ‘position of paralysis’. This asymmetry disappears when the visual field’s coordinate system is rotated by an angle equal to the tilt of the axis of the nasal streak. Previously published maps, based on recordings from postsynaptic colhcular units, have failed to reflect this tilt of the nasal visual streak, perhaps in part because the centers of unit receptive-fields are biased estimators of the retinal origin of axons terminating near a collicular recording site. Cat
Superior colliculus
Retinotopy
Visual streak
INTRODUCTION
maps based on physioiogi~l recordings have provided detailed information on the connectional geometry of the visual pathways and it is likely that such maps will continue to have a key role in studies of spatial processing in vision. Nonetheless, the interpretation of visuotopic maps is not a straightforward matter. The patterns of intersecting isopleths which form the maps can but poorly convey the complexity of spatial transformations that are occurring. Moreover, the maps are highly schematic summaries of experimental procedures which often involve essentially practical choices of stimulus parameters and response measures. For instance. it is common practice to use as mapping variable the geometric centers of neuronal receptive-fields plotted for a given recording site. One implication of the results reported here is that use of this mapping variable can have a significant effect on the coordinate structure of the resulting map. The experiments were concerned with the rep resentation of the retina’s fist& strt& in the superior colliculus of the cat. The visual streak. found in the retinas of cats and many other vertebrates. is a specialized region in which ganglion cells occur at higher frequency than elsewhere in the retina (Slonaker, 1897: Stone, 1965; Hughes, 1975). The visual streak contains the area centralis and extends temporally and nasally from it, but is most prominent in the nasal retina. According to Stone and coworkers (Rowe and Stone, 1976; Stone and Keens, 1980). the cat’s visual streak is formed principally by the smallest (W) ganglion cells. but the largest (Y) ganglion cells also contribute Visuotopic
(WPssIe et al., 197.5).It is not clear to what degree the medium size ganglion cells are involved (Rowe and Stone, 1976, Stone and Keens, 1980; Hughes, 1981). In keeping with its plethora of gang&on cells, the visual streak receives a Iarger representation in central visual structures than do surrounding regions of the retina. In the cat, this magnification of the region dividing dorsal and ventral retina may be seen in published visuotopic maps of the superior coiliculus (Apter, 1945; Straschill and Hoffmann. 1969; Hoffmann. 1970; Feldon ef a(., 1970: Berman and Cynader, 1972), the lateral geniculate nucleus (Sanderson, 1971) and the striate cortex (Bilge et al., 1967; Tusa er al., 1978). It is reasonable to assume that these regions of high magnification receive information from the visual horizon in waking cats, although the evidence for this is not conclusive (see Discussion in Cooper and Pettigrew, 1979b). On the other hand, it is now clear that, under the usual conditions of visuotopic mapping studies, the nasal limb of the cat’s visual streak is not oriented horizontally. Muscular paralysis by the commonly used agents causes intorsion of the upper margin of the cat’s eyeball (Bishop et al., 1962; Nelson et al., 1977; Cooper and Pettigrew. 1979b), an action which tilts the nasal streak inferiorly with respect to a nasotemporal (horizontal) axis through the area centralis (McII~in, 1977; Cooper and Pettigrew. 1979b). As a result, the upper visual field is served by more contralaterally projecting, nasal retinal ganglion cells than is the lower visual field. Thus, one might expect to find an exaggerated representation of the upper visual field in visuotopic maps made through the contralateral eye, particularly in the superior colliculus, whose di507
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rect retinal input consists largely of W-cell axons from the contralateral retina (Fukuda and Stone, 1974: Cleland and Levick, 1974; KelIy and Gilbert, 1975). As noted already, W-cells form a major component of the cat’s visual streak. In general, published visuotopic maps of the cat’s superior colliculus do not exhibit this expected exag geration of the representation of the upper visual field (Feldon et a[., 1970; Berman and Cynader. 1972).* However, in a map based on “unresolved neural activity” recorded just beneath the stratum zonale, the upper held’s magnification factors (Daniel and Whitteridge, 1961) exceed those of the lower field, especially in posterior regions of the map (see Fig. 2 in McIlwain, 1975). It is now known that these recordings were made in a collicular zone densely populated by the terminals of W-cell axons origjnating in the contralateral retina (Sterling, 1973; McIlwain, 1978; Itoh et a/., 1981). Extracellular electrodes in this “juxtazonal” region record potentials (“Juxtazonal Potentials” or JZPs) apparently associated with synaptic currents generated by the discharge of individual W-cell axons (McIlwain, 1978). Thus, a map based on such recordings may be essentially a map of the W-cell projection to the colliculus from the contralateral eye. Furthermore, the JZPs do not arise from regenerative responses in postsynaptic elements. so their spatial distribution would be little influenced by convergence networks within the collicuius itself. It is possible. then, that a JZP-based map would reveal the tilt of the visual streak because its topography is a direct reflection of afferent distribution patterns. To pursue this question further, a series of visuotopit maps of the colliculus was prepared from recordings of JZPs. All of these maps exhibited a disproportionate magni~cation of the upper visual field which disappeared when the visual fields coordinate system was rotated by an angle equal to the tilt of the axis of the nasal streak. It is shown how this feature of the retinotectal projection might fail to appear in a map based on the centers of receptive-fields of postsynaptic collicular neurons. METHODS
The maps described here are from 5 aduit cats and are based on data published in part in an earlier report (Mcllwain, 1977). Each animal was anesthetized with i.p. pentobarbital (40 mgikg) and mounted in a stereotaxic instrument modified to give the eye an unobstructed view of a tangent screen 75cm away. The skull and dura were removed near the midline to
*Maps published by Straschill and Hoffmann (1969) and by HotTmann (1970) also exhibit no exaggeration of the upper visual field. However. these maps were obtained with binocular stimulation and are not strictly comparable to the other maps cited here. which were based on stimulation through the contralateral eye.
provide access to the superior colliculus through the overlying occipital cortex. Scalp edges were secured to a metal ring and an oil pool was formed over the exposed cortex. Paralysis was achieved by intravenous infusion of Flaxedil (20 mg:hr). artificial respiration was provided. expired CO2 was monitored and maintained between 3.5 and 4.5”,, and body temperature was controlled at 3X C. In preparation for stimulation. the horizontal alignment of the stereotaxic frame was checked with a spirit level and the infraorbitaf bar was removed from beneath the stimulated eye. The axis of the slit pupil of this eye was measured repeatedly. as described elsewhere (McIlwain. 1977). until a stable value was reached. These angles with respect to gravitational vertical ranged from 5.5 to 8.0. (mean 6.8.. SD = 1.Y). If symmetry of the two eyes is assumed. the angle between the pupil axis. as they converge over the cat’s head, would range from 11 to 16 . which is comparable to values reported by others for the “position of paralysis” (Bishop er al.. 1962: Nelson et al., 1977; Olson and Freeman, 1978: Cooper and Pettigrew, 1979b). The pupil of the stimulated eye was then dilated with a&opine and the nictitating membrane was contracted with phenylephrine. The other pupil was not dilated and remained constricted for the duration of the experiment. Piano contact lenses were applied to both corneas and an opaque patch covered the unstimulated eye. Quality of focus was assured by substituting spectacle lenses before the stimulated eye while examining the retinal image of an illuminated grid located at the tangent screen, The tangent screen was diffusely illuminated at 5 cd/m’. The superior colliculus contralateral to the stimulated eye was explored with varnished tungsten microelectrodes in a series of vertical penetrations spaced 0.5 mm apart (Fig. I). Between 62 and 76 penetrations were made in each cat. The electrode tip was positioned in each track for optimal recording of JZPs (McIlwain, 1978) and electrolytic lesions at selected recording sites permitted subsequent reconstruction of the penetration grid from serial Nisslstained frozen sections (Fig. 1). JZPs were evoked by a small light spot (60-80 cd/m’) moved very slowly on the tangent screen. The response-fields. plotted for each track on a sheet of paper attached to the tangent screen, ranged in diameter from less than 0.5~ near the area centralis to about 5’ in more peripheral parts of the visual field.
Distances were measured from the geometric centers of the JZP response-fields to vertical and horizontal axes intersecting at a working reference pole on the tangent screen. For two cats, this pole was the intersection with the tangent screen of a normal from the eye. For three cats. the image of a prominent retinal vascular bifurcation was plotted on the screen at short intervals, using the method of Fernald and Chase (1971). Correction for residual eye movements
Fig. I. Histological section from a mapping experiment. The arrow points to an electrolytic lesion made just beneath the surface at,a recording site. Numerous descending electrode tracks may be seen in the cerebral hemisphere above the colliculus. Elevation data from the row of penetrations at this level are shown in Fig. 2. Calibration line: I mm.
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Visual streak and collicular retinotopy
r
t
20” I
Rostra1
\
Caudal
IO” -
s
5
P 2 w
HM
0' *
-10” -
\
I-20”
\ \
t
I123412345 Distance from midline,
mm
Fig. 2. Typical data from which maps were constructed. Points correspond to the elevations, with respect to the visual axis and horizontal meridian, of JZP response-fields observed in two mediolateral rows of penetrations in the same cat. The curve marked “Rostral” is from a row of penetrations near the representation of the area centralis. The curve marked “Caudal” is from a row at the level of the histological section in Fig. I. The point marked by an asterisk corresponds to the recording site at the lesion in Fig. I. Ordinate: elevation in visual field above zero horizontal meridian. Abscissa: distance from the midline of the brainstem. HM : horizontal meridian of visual field. was achieved by stating a given response-field’s position with reference to the current projection of this retinal landmark. A PDP-I2 computer was employed to convert the tangent screen distances to spherical coordinates using the expressions of Bishop er al. (1962). From plots of these coordinates. the tangent screen locus corresponding to the region of highest magnification was located and assumed to be the projection of the area centralis. Thus. this reference point of the map was established from the internal structure of the map data and not by ophthalmoscopic estimation. The computer then made this point the origin of the response-field coordinate system. Similarly. the projection of the axis of the visual streak was determined by locating the region of highest vertical magnification at different distances from the projection of the area centralis (McIlwain. 1977: Fig. 2). The tilt of the visual streak with respect to the zero horizontal meridian of the visual held (henceforth called simply the horizontal meridian) was determined from the estimated loci of the streak axis using the expression: tan(Elevation) = A x sin(Azimuthl + B. The values of slope, A. obtained with this explicit expression were virtually identical to those calculated by assuming an approximately linear relationship between elevation and azimuth for points near the origin (Mcllwain, 1977). Combining response-field coordinates with the penetration grid yielded sets of curves for each animal which related collicular loci to visual field azimuths and elevations (Fig. 2). Selected isoazimuth and iso-
elevation lines derived from these curves were projected to a horizontal plane by normals to that plane. Thus, the maps are orthographic projections giving a dorsal view of the collicular visuotopic patterns. These maps were placed within profiles of the boundaries of the smmm yriseunl superjicialr determined by serial histological reconstruction. No shrinkage correction was applied to these profiles. An average map was also prepared after photographically normalizing the individual maps so that the anteroposterior diameters of the colliculi equalled 4.5 mm. The maps were then superimposed at azimuth 20’. elevation 0” and averaged by computer. A second series of five individual maps and their average was obtained following computer rotation of each set of map data by an angle equal to the tilt of the visual streak. All maps are presented as though they were obtained from the left superior colliculus. RESULTS
Figures 1 and 2 illustrate the nature of the data used to generate the present maps. The arrow in the histological section of Fig. I points to an electrolytic lesion made at one of the recording sites. Since the recordings were made with the microelectrode’s tip just beneath the collicular surface, it was usually impossible to see recording points at which lesions were not placed, although the tracks of the penetrations were evident in the overlying hemisphere (Fig. 1). Figure 2 shows a plot of the elevations of JZP response-fields recorded in this row of penetrations (curve marked “Caudal”) as well as those obtained in a more rostra1 row near the representation of the area centralis (curve marked “Rostral”). It may be seen that the region of highest vertical magnification (minimal slope) in the caudal curve lies above the horizontal meridian, suggesting that the nasal streak was tilted as predicted. Maps obtained from the five cats used in this study are presented in Fig. 3A. In each of these maps and in their average (Fig. 4A) it is evident that the upper visual field is disproportionately represented. This is most prominent posteriorly where there is marked asymmetry in the vertical magnification factors about the projection of the horizontal meridian (labelled HM) and crowding of the isoelevation lines in the posterolateral quadrant of the maps. If this asymmetry is due to tilt of the nasal streak. then rotation of the visual field’s coordinate system by an angle equal to the tilt should eliminate or greatly reduce the asymmetry. This follows from the assumption that magnification factors are proportional to retinal ganglion cell densities and from the fact that the nasal streak is an axis of symmetry for isodensity contours in topographic maps of ganglion cell distribution (Stone, 1965; Hughes, 1975, 1981; Stone and Keens, 1980). The results of rotation shown in Figs 3B and 4B are consistent with this prediction. The magnification factors become approximately equal at corre-
JAMES T. MCILWAIS
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A
medial
lmm Fig. 3. Topography of retinocollicular projection in five cats as determined from JZP recordings. Maps formed by connectmg selected coordinate points by line segments. Additional isoazimuth and isoelevation lines available for some maps deleted for clarity. Coordinate labels for all five pairs of maps correspond to those of the leftmost map of row A. Row A: The zero isoelevation line (HM in leftmost map) is the projection of the horizontal meridian of the visual field. Row B: Same dam as m A but rotated so that the zero isoelevation line corresponds to the projection of the itxis of tho nasal visual streak (VS in leftmost map).
sponding loci medial and lateral to the zero isoelevation line. which now represents the projection of the visual streak (VS) and which inclines medially as it runs from anterior to posterior across the colliculus and intercepts the isoazimuth lines at right angles. The projection of the streak axis can be seen to divide
the projected surface of the colliculus about equally between upper and lower visual tields. The isoazimuth projections are changed little by the rotation procedure. since near the horizontal meridian they are essentially parallel to the direction of rotation. Despite differences in the shape of the colliculnr
medtal A
1 mm
Fig. 4. Average maps of retmocollicular projection as determined from JZP recordmgs. (A) Normalized average of maps in Fig. IA, in which zero isoelevation line corresponds to horrzontal meridtan (HMI. (B) Normalized average of maps in Fig. IB, in which zero isoelevation line corresponds to projection of nasal visual streak (VS). Format as in Fig. 1. See Methods for normalization procedure. Ipsilateral field coordinates are not illustrated in these average maps.
Visual streak and coificular retinotopy borders. variations in ~ollicular surface curvature and a host of other inherent and experimental sources of v~~riability. the maps of Fig. 3B are rem~~rk~~blysimilar from animal to animal. For instance. the central 20 by 20’ region. bounded by isoazimuths 0 and 20. and isoelevations f lo’, occupies 30 + 2”, (mean f SD) of the total projection area of the superficial gray, even though the latter varies from 17.8 to 25.5 mm2 (mean 20.3. SD 2.9 mm2). The internal scaling of the maps also differs little from animal to animal. Other general features of the maps of Figs 3 and 4 are consistent with earlier reports and need not be treated in detail here. Requiring mention is the represent~~tion of the ipsilateral hemifield at the anterior margin of the colliculus. first noted by Straschill and Ho~rn~~nn (1969) and subsequently documented in detail by others (Berman and Cynader. 1972: Feldon et ul., 1972: Lane et ul.. 1974). The present maps agree with previous reports in allotting approximately the anterior I mm of the superficial gray to the ipsilateral visual field. but a caveat is warranted here. The zero isoazimuth lines in the present maps are arbitrarily defined with respect to tangent screen axes perpendicular either to the horizontal meridian or to the projection of the axis of the nasal visual streak. Therefore, the zero isoazimuth lines need not correspond to retinal features such as the nasotemporal raphe, which may not be per~ndicul~tr to the nasal streak (Cooper and Pettigrew. 1979b) or to the “zero meridian” of Cooper and Pettigrew ( f979a.b), which is defined by functional connections to binocular cortical units (see also Nikara er u/.. 1968: Joshua and Bishop, 1970; Sanderson. 1972).
DISCUSSlOX
When the cat‘s eye is in the “position of paralysis”. the nasal limb of the visual streak is not horizontal but is tilted downward on the retina. This tilt is apparent in maps of the retinocollicular projection based on recordings of synaptic activity generated by the crossed W-cell input. This result is not due to distortion of the data sample by one exceptional animal. since the phenomenon is present in each of the maps of Fig. 3A. It is also unlikely that a fortuitous selection of animals with marked ocular intorsion was studied, since the range of pupil angles observed in these cats was comparable to that reported by others. Tangent screen distortions were eliminated by calculating the spherical coordinates of the response-fields and possible effects of eye movements were reduced by periodic monitoring of eye position and by appropriate tr~lnsformation of the dnta. Finally. since the representation of the area centralis was estimated from the internal structure of the map. errors stemming from ophthalmoscopic estimates were avoided. Thus. the asymmetries of the map of Fig, 4A are probably not attributable to the more common sources of manning errors and mav_ be oresumed to .. _ .
513
reflect the tilt of the visual streak in the “position of paralysis”.
Earlier maps agree that the representation of the horizontal meridian begins anteriorly about midway between medial and lateral borders of the colliculus and drifts medially as it proceeds posteriorly. In the present maps. this trajectory corresponds to the projection of the visual streak, whereas that of the horizontal meridian drifts laterally. giving a disproportionate representation to the upper visual field. This is the most striking discrepancy between the present map and those published previously. Small errors in estimating the tangent screen projection of the area centralis can produce relatively large errors in visuotopic maps because of the large magnification factors at central representations of this retinal zone. It is unlikely, though. that this is the major source of the differences between Fig. JA and earlier maps, because such errors should not have been in the same direction in all previous studies and because the resulting discrepancies should have been more conspicuous in anterior than in posterior regions of the map, while just the converse was found. Earlier work was also carried out in paralyzed cats and, with the exception of one study. the animal’s eyes were presumably in the ‘position of paralysis”. Feldon er al. (1972) state that in their study “The contralateral (right) eye was aligned by attaching sutures to the conjunctiva, [and ] orienting the vertical slit pupil in the proper axis. . . ” (p. 135).The map resulting from this study exhibits an exceptionally steep medial drift of the projection of the horizontal meridian and an exaggerated representation of the irlfrrior visual field. This coordinate pattern would result were the nasal streak rotated so that its tangent screen projection lay in the lower visual field. a situation which may possibly have occurred during attempts to orient the slit pupil vertically. Under this condition, the projection of the horizontal meridi~tn would lie increasingly medial to the line marked VS in Fig. 4B for increasing values of eccentricity.
Yet another factor which may account for differences between the present and earlier visuotopic maps of the colliculus is related to the practice of using as mapping variable the centers of the receptive-fields of post-synaptic neurons. It is well established that microelectrode penetrations through the colliculus are likeiy to encounter cells with relatively large receptive-fields, ~rti~ularly in caudal regions representing the periphery of the visual field (McIlwain and Buser, 1968; Sterling and Wickelgren, 1969). These receptivefields can incorporate areas of visual space having disparate magnifications in the afferent map, with the result that collicular regions equidistant from the cell body do not have equal representation in the recep tive-field. Thus, the center of the receptive-field may
514
JAMES T. MC~LWAIS
AZIMUTH Fig. 5. Influence of receptive-field center measurements on estimated projection of horizontal meridian (A) Typical map from Fig. IA (second from left in that figure) based on horizontal meridian projection as determined from JZPs. Projection of axis of visual streak indicated by dashed line. Elliptical profiles are hypothetical RFIs of cells recorded at penetration sites indicated by large dots. (B) Receptive-fields of cells I-3 of part A. as mapped on the tangent screen. HM-horizontal meridran.
not provide an accurate estimate of the retinal origin of axons terminating near the recording site. The
potential effect of this phenomenon on a visuotopic map of the colliculus is illustrated in Fig. 5 with the aid of a graphical device which summarizes the relationship between a recording site and the boundaries of the receptive-fields of cells recorded there. It has been shown elsewhere (McIlwain. 1975: Capuano and McIlwain. 1982) that when collicular receptive-fields are plotted in a map based on JZPs, the resulting profiles are centered on the recording site and are generally oval and maximally 2 x 3 mm in size. with their long axes oriented mediolaterally. The interpretation of these profiles. called ReceptiveField Images or RFIs. does not concern us here, but we may take advantage of the empirical fact that their form and location with respect to a recording site are known. By drawing hypothetical RFls of the expected dimensions on :I JZP-based map. one can infer the shapes and locations of receptive-fields likely to be observed at ;I particular recording site. A typical map from Fig. 3A is reproduced in Fig. SA with the projection of the nasal streak indicated by a dashed Ime. lsoazimuth lines have been added at I5 ;md 50 Large dots mark the sites of three mapping penetrations. two of which fall on the projection of the horizontal meridian. Centered on these dots are k~porl~ricul RFls of moderate size, as might be observed for cells recorded in each mapping penetration. In Fig. 5B are shown the corresponding receptivefields 01 these cells. The receptive-field of cell I is centered near the horizontal meridian. but since the RFI of cell 2 encompasses more of the lower than the upper visual held. the center of its receptive-field lies below the horizontal meridian. Thus. a mapping ex-
periment based on locations of receptive-held centers would assign the locus of cell 2 to the lower quadrant of the visual field. The RF1 of cell 3 has been positioned so that the corresponding receptive-lield in Fig. SB is approximately centered on the horizontal meridian. The center of this receptive-held would indicate that the locus of ceil 3 receives the projection of the horizontal meridian. whereas it actually lies near the projection of the visual streak. Because of the marked asymmetry in vertical magnification about the projection of the horizontal meridian. only penetrations medial to it and near the projection of the vislral streak’s axis are likely to yield receptive-fields centered on the horizontal meridian. particularly in posterior regions of the map. As suggested in Fig. 5. if receptive-fields such as these were used to generate ;I visuotopic map, the apparent prqjection of the horizontal meridian would tend to “track” the projection of the visual streak ;IS it moves posteriorly and medially. Other consequences of this phenomenon may be appreciated by placing RF1 boundaries in different parts of the map of Fig. 5A. For instance. penetrations 0.5 mm medial and lateral to that containing cell 3 would yield receptive-fields centered about IO‘ above and below the horizontal meridian. respectively. This would have the effect of reducing the asymmetry in the vertical magnification factors for this while shifting the isoelevation contours region, toward the zero isoelevation line. Such exercises are useful for visualizing potential interactions between cell location. magnilication factors and the resulting map measurements. but it should be emphasized that the RFls in Fig. 5 were chosen to illustrate the point of this discussion. They
515
Visual streak and collicular retinotopy
do not correspond to the smallest or the largest RFls observed for collicular cells. nor are they necessarily representative of cells encountered in earlier mapping experiments. It is clear, though, that the larger the receptive-field. the larger will be the effect of the phenomenon illustrated in Fig. 5. Moreover. the direction of the bias introduced by the large receptivefield will vary depending on where in the map the penetration occurs. This phenomenon may account in part for the considerable dissimilarities in coordinate structure apparent in earlier maps based on samples of coilicular receptive-fields. Differences are particularly striking between studies which included data from the deep collicular laminae (Straschill and Hoffmann, 1969; Hoffmann. 1970), where most cells have very large receptive-fields (Gordon, l973), and those in which recordings were limited to the superficial layers (Feldon et al., 1970; Berman and Cynader, 1972), where small-field cells may be encountered. The present map (Fig. 4B) closely resembles that of Berman and Cynader ( 1972). except that their map places the representation of the horizontal meridian where Fig. 4B shows that of the nasal visual streak. Since Berman and Cynader used receptive-fields up to 30” in diameter to develop the peripheral parts of their map, the phenomenon described above may account in large part for the differences between our results.
These results indicate that the choice of mapping variable can have a significant effect on the coordinate pattern of a visuotopic map of the superior colliculus. Analogous phenomena may occur in other visual structures where unit receptive-fields are very large, such as the lateral supr~lsyivian cortex (Spear and Baumann, 1975; Palmer er nl.. 1978), and the visual areas of the posterior thalamus (Suzuki and Kato, 1969; Godfraind er ul., 1972: Chalupd and Fish, 1978; Mason. 1978). The choice of mapping variable may make little difference if one is interested only in detecting an
orderly representation of the visual field or in the general form and boundaries of a projection. Its importance increases as quantitative information is needed about the spatial distribution of magnification factors. The present experiments offer an instance where such information permitted a more accurate assessment of the projection of the nasal streak than has hitherto been possible. Of greater interest is the possibility that visuotopic maps. and their constituent magnification factors, can be used to analyze the spatial distribution of neural activity produced by visual stimuli. For instance. inverse correlations between magnification factors and receptive-field Dimensions in striate cortex and superior collicuius have suggested that a relatively constant volume of tissue in each of these structures analyzes information from any visual point. regardless of its position in the visual field (Hubel and Wiesel, 1974: Albus, 1975; McIlwain, 1975. 1976: but cf. Dow et at., 1981). For the
superior colliculils, this neural “point image” has been shown to have a regular geometric relationship to the receptive-field images of the large-field cells, if these are plotted in a JZP-based map (McI~wain, 1975; Capuano and Mcilwain, 1981). Discovery of such relationships depends on having the appropriate map or spatial distribution of magnification factors and, since different mapping procedures can lead to different coordinate patterns, not all maps will be equivalent in this respect. Perhaps one useful index of the “validity” of a particular map might be its capacity, when combined with other information such as receptive-field size, to reveal invariance relationships such as those just mentioned. AcX-ilo~fpdyetttertrs-Ithank Drs David M. Eerson and Jonathan Stone for valuable comments. Dr Joseph Corless for help with computer chores and MS Anne Boyd for typing this paper. Drs W. C. Hall. C.-S. tin and Nell Cant also provided useful comments and generous hospitality during the phase of the work carried out at Duke University. This research was supported by PHS Grant EY 02505, by bequests from the Grass Foundation and by a Faculty Scholar Award from the Josiah Macy Jr Foundation.
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