the naso-temporal division of the cat's retina re-examined in terms of y-, x- and w-cells

The Naso-Temporal Division of the Cat's Retina Re-examined in Terms of Y-, X- and W-Cells

JONATHAN STONE AND YUTAKA FUKUDA Department of Physiology, T h e J o h n Curtin School of Medical Research, T h e Australian National University, Canbena, A.C.T. 2601, Australia

ABSTRACT In the cat, as in all mammals, optic nerve fibres decussate only partially, so that some of the ganglion cells in one retina project to the contralateral side of the brain, and some to the ipsilateral side. The retinal distribution of ipsi- and contralaterally projecting ganglion cells, described in a previous study, has been re-examined in the context of the recent classification of cat retinal ganglion cells into three major types (W-, X- and Y-cells). Evidence is presented of significant differences between the three cell types in the retinal distribution of ipsi- and contralaterally projecting cells. The pattern of naso- temporal division of retina described previously thus appears to be a composite of the different patterns of the three cell types. Functional implications of these different patterns are considered.

In probably all mammals the fibres of the optic nerve decussate only partially (Walls, '42; Polyak, '57). Some fibres cross in the optic chiasm, enter the contralateral optic tract and terminate on the contralateral side of the brain; other fibres do not cross, but enter the ipsilateral tract and terminate ipsilaterally. In mammals therefore each retina contains both ipsi- and contralaterally projecting ganglion cells and these two cell populations are always to some degree spatially segregated within the retina. Ipsilaterally projecting cells are generally confined to a temporal area of retina while nasal retina contains contralaterally projecting cells. Moreover, in those mammals in which a small area of retina is specialised for acute vision (such as the foveal specialisation in the monkey and human and the area centralis in the cat), that area is located at the junction of nasal and temporal areas of retina, i.e., at the junction of those areas containing ipsi- and contralaterally projecting ganglion cells, It consequently has be- come important for the understanding of central vision to know, in some detail, the naso-temporal division of the retina, i.e., to know the distribution in the retina of ipsi- and contralaterally projecting ganglion cells.

The first experimental investigation of the naso-temporal division of the cat's retina is probably the study of Ganser (1882), who noted that ipsilaterally projecting ganglion cells are confined to temporal retina. A more complete description was provided by Stone ( '66) , from an analysis of the distribution of ganglion cells in the retina after section of one optic tract, Since this report, evidence has ac- cumulated that cat retinal ganglion cells can be grouped into three distinct types, termed W-, X- and Y-cells (Enroth-Cugell and Robson, '66; Stone and Hoffman, '72; Stone and Fukuda, '74), which presumably serve different functional roles. It seemed likely that these different roles would be reflected in the patterns of naso- temporal division of the three cell types and that knowledge of these patterns might contribute to the understanding both of the naso-temporal division of retina as a whole, and of the different functional roles of the three types. We have therefore looked again at the naso-temporal division of the cat's retina, with the aim of de- scribing separately and comparing the retinal distributions of ipsi- and contralaterally projecting W-, X- and Y-cells.

Evidence is presented that the patterns of projection found in the three ganglion cell types differ significantly, The pattern

377 J. COMP. NEUR., 155: 377-394.

378 JONATHAN STONE AND YUTAKA FUKUDA

of naso-temporal division appears to be most developed among X-cells. All X-cells nasal to the area centralis project contralaterally, and all temporal X-cells project ipsilaterally. Intermingling of ipsi- and contralaterally projecting Xcells is found only within a limited region (corresponding to the "median strip of overlap" described by Stone ('66)) at the junction of nasal and temporal areas of retina, This pattern resembles the pattern of naso- temporal division described for monkey retina (Stone, Leicester and Sherman, '73). By contrast, the segregation of ipsi- and contralaterally projecting cells is least developed among W-cells, over half the W- cells throughout temporal retina projecting contralaterally, and only a minority (about 40% ) projecting ipsilaterally. Stone ('66) noted that approximately 25% of the ganglion cells in temporal retina project contralaterally. The great majority of these cells are W-cells, a small minority being Y-cells. The segregation of ipsi- from contralaterally projecting Y-cells is less complete than among Xcells, about 5% of the Y-cells throughout temporal retina projecting con trala ter ally.

It thus appears that the pattern of naso- temporal division described previously for the cat's retina (Stone, '66) is a composite of the different patterns found among W-, X- and Y-cells. Implications of these different patterns for the understanding of the functional roles of Y-, X- and W-cells are considered in DISCUSSION.

METHODS

The experimental techniques employed here have all been described previously. The techniques used for anaesthesia, para- lysis and retinal recording are described in Stone and Freeman ('71) and Stone and Fukuda ('74), for electrical stimulation of the optic chiasm (OX), optic tract (DT) and superior colliculus (SC) in Stone and Freeman ('71) and Fukuda and Stone ('74a), and for the preparation of whole mounts of the retinas of tract-sectioned cats in Stone ('65, '66) and Stone, Lei- cester and Sherman ('73). The criteria used for the physiological identification of W-, X- and Y-cells have been described previously (Hoffmann, Stone and Sherman,

'72; Stone and Hoffmann, '72; Stone and Fukuda, '74).

RESULTS

Three experimental approaches were used. First, we isolated the activity of many (277) retinal ganglion cells, plotted their receptive fields, classified the cells as W-, X- or Y-cells by their receptive field properties and axonal conduction velocity (Stone and Fukuda, '74) and noted whether the cell responded antidromically to stimulation of the ipsilateral or contralateral optic tract or superior colliculus. This work provided an indication of the distribution with respect to the area centralis of ipsi- and contralaterally projecting cells of the three types. Second, we analysed the antidromic field potentials generated in the retina by OT stimulation. Because these field potentials have two distinct (early and late) components (Stone and Freeman, '71 ), which are generated in Y-cells and X-cells (Stone and Hoffmann, '72), these observations could be used to confirm the patterns of X- and Y-cell projection suggested by the single unit study. Third, there is substantial evidence that Y-cells have the largest cell somas found among cat retinal ganglion cells, and that W-cells have the smallest somas, X-cells being intermediate in soma size (Stone, '73; Fukuda and Stone, '74a,b). We therefore examined in some detail the distribution of ganglion cell somas of different sizes in the retinas of tract-sectioned cats. This analysis has provided a detailed confirmation of the patterns of projection of the three cell types suggested by the analyses of single units and field potentials.

Each of these approaches has inherent weaknesses. With single unit work only a limited sample of cells can be studied. This is largely overcome for X- and Y-cells by studying field potentials, but, since little is known of the extent of the volume of tissue whose cells contribute to such a potential, there is uncertainty as to the degree of spatiaI resolution obtainable. There are no problems of limited sampling or spatial resolution with the histological analysis, but here the distinction between the three cell types is less certain, particularly between X- and W-cells, whose ranges of cell body size overlap to some degree

NASO-TEMPORAL DIVISION OF CAT RETINA 379

(Fukuda and Stone, ’74a and see below). We sought, by using all three techniques, to overcome the different problems of each.

1. T h e single unit analysis Single units (total 277) were recorded

in the right retina of cats, at the area centralis and at locations above, below, nasal to and temporal to this area. For each cell we checked whether it responded antidromically to stimulation of the contralateral or ipsilateral OT and/or SC. This established the laterality of the cell’s projection. The latencies of each cell’s antidromic responses to stimulation of the OX, OT and/or SC were noted; these latencies give a clear guide to the classification of a cell as a Y-, X- or W-cell (Stone and Fukuda, ’74). We then plotted the receptive field of each cell on the 1 metre tangent screen used and examined the cell’s responses to visual stimuli, to confirm its classification. The “horizontal eccentricity” of each receptive field was then measured, as follows. The latencies of the antidromic

responses of X-cells were used to locate the centre of the area centralis, following a previous analysis (Fukuda and Stone, ’74a). The optic disc was projected onto the tangent screen, using the technique suggested by Fernald and Chase, ’71; its outline is labelled “blind spot” in figure 1. Previous work (Vakkur, Bishop and Kozak, ’63; Stone, ’66) has shown that the line joining the centre of the blind spot to the area centralis is inclined to the vertical at an angle of approximately 68”, as drawn in figure 1. For each unit we measured the distance d, from the geometrical centre of its receptive field to the vertical, i.e., we measured the horizontal component of the eccentricity of each receptive field from the area centralis. The direction of the eccentricity (nasal or temporal to the area centralis) was also noted.

The results of this analysis are sum- marised in the frequency/position histograms in figure 2. Separate histograms are shown for Y-, X- and W-cells and for ipsi- and contralaterally projecting cells of each

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Fig. 1 Diagram showing the measurement of the horizontal eccentricity d of a receptive field. The blind spot was plotted on the tangent screen by the technique described by Fernald and Chase (’71). The area centralis was plotted using the antidromic latency criteria described previously (Fukuda and Stone, ’74a). The receptive fields were located and plotted with small flashing spots of light. The horizontal component d of the receptive field’s eccentricity from the area centralis was measured as shown. The dotted line represents the vertical axis of the retina, which runs at an angle of approximately 68” to the line joining the area centralis to the centre of the blind spot (Vakkur, Bishop and Kozak, ’63; Stone, ’66).


type. The abscissa in these histograms represents horizontal eccentricity, i.e., the distance d measured for each receptive field, as just described. The abscissae of the histograms are marked in centimetres, representing distances on the tangent screen. Scales showing angular distance and distance on the retina are also drawn at bottom. Zero on the abscissa marks the point of zero eccentricity as determined by the antidromic X-cell latency criteria set out previously (Fukuda and Stone, ’74a).

Figure 2A shows that all the X-cells encountered more than 1.5 cm (approximately 1 ’ ) temporal to the zero point projected ipsilaterally , Conversely, figure 2B shows that X-cells encountered more than 2.5 cm nasal projected contralaterally. Intermingling or “overlap” of ipsi- and contralaterally projecting X-cells was found over only a very limited region. Including all cells in the sample the region extends from 1.5 cm temporal to 2.5 cm nasal and is thus 4 cm (2.3’) wide. Excluding the two most nasal ipsilaterally projecting cells and the most temporal contralaterally projecting cell in the present sample the overlap is 2 cm (1.2”) wide. This region of X-cell overlap (marked by the broken lines in figure 2 ) seems, therefore, to correspond well with the 0.9’ wide “median strip of overlap” described in the previous study (Stone, ’66).’

The pattern of distribution of ipsi- and contralaterally projecting Y-cells differs from the pattern seen among X- cells in two ways. First, some Y-cells throughout temporal retina project contralaterally. In the present data (fig. 2D) one of the 35 Y-cells located more than 2 cm (approximately 1 ” ) temporal projected to the contralateral optic tract but histological data, presented below, indicates that about 5% of Y-cells throughout temporal retina project contralaterally. Second, it appears that at least a great majority of the Y-cells in the region of X-cell overlap project contralaterally. Thus figure 2C shows that ipsilaterally projecting Y-cells were found only temporal to the region of X-cell overlap. All Y-cells encountered nasal to and within this region, and most of the Y-cells encountered up to 2 cm temporal to the region, projected contralaterally (fig. 2D). As a consequence, a re-

X-cells.

Y-cells.

gion of transition from contralateral to predominantly ipsilateral projecting cells can be specified for Y-cells. It appears to be located 2-3 cm (1-2”) temporal to the region of X-cell overlap.

The pattern of distribution of ipsi- and contralaterally projecting W-cells is distinct from the patterns described above for X: and Y-cells. As for X- and Y-cells, all W-cells encountered nasal to the region of X-cell overlap projected contralaterally. However, only one ipsilaterally projecting W-cell was encountered in the regon of X-cell overlap (fig, 2E), SO that (as with Y-cells) the majority of W-cells in this region (5/6 in the present data), appear to project contralaterally. Further temporal, over half of the present sample of W-cells (19/33) encountered temporal

W-cells.

1 It appears anomalous that the point of zero eccentricity determined in this way does not coincide with the centre of the region of X-cell overlap, but seems to fall 1 cm (0.57”) more temporal, at the temporal edge of this region. This appears anomalous because it is argued in this paper that the region of X-cell overlap corresponds to the “median strip of overlap” described previously (Stone, ’66) and it is argued previously (Stone, ’66) that the median strip is centred on the area centralis. Further consideration suggests that this anomaly results from a residual error in the localisa- tion of the point of zero eccentricity as the centre of the region of long X-cell latencies which can be localised at the area centralis (Fukuda and Stone, ’74a). It would be more precise to define the point of zero eccentricity as the centre of the localised region of relatively slow-conducting X-cells which can be defined at the area centralis. The slow conduction velocity of the axons of area centralis X-cells is, of course, reflected very directly in their antidromic latencies. But because these latencies are superimposed on a latency “baseline” which increases linearly with distance from the optic disc (fig. 2 in Stone and Free- man, ’71), the centre of the long-latency region is dis- placed slightly temporally from (i.e., further from the optic disc than) the centre of the region of slow- conducting X-cells.

Fig. 2A,B Frequency/horizontal eccentricity histograms for X-cells. Ipsi- and contralaterally projecting X-cells a re shown separately.

Fig. 2C,D Frequency/horizontal eccentricity histograms for ipsi- and contralaterally projecting Y-cells.

Fig. 2E,F Frequency/horizontal eccentricity histograms for ipsi- and contralaterally projecting W-cells.

The abscissae of the histograms are marked in centimetres, representing distance on the tangent screen. Scales showing distance on the retina and angular distances are drawn a t bottom. Distance on the retina was estimated assuming tha t 1 m m on the retina subtends 4.4” visual angle (Vakkur, Bishop and Kozak, ’63). The zero position o n the abscissa represents the point of zero eccentricity as determined by the antidromic latency criteria set out previously (fig. 1 in Fukuda and Stone, ’74a). The terms “nasal” and “temporal” at the top of the figure refer to direction in the retina.


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to the region of X-cell overlap projected contralaterally (fig. 2F), the remainder projecting ipsilaterally. As previously noted (fig. 14 in Fukuda and Stone, ’74a), the W-cells in temporal retina which project ipsilaterally differ consistently in receptive field properties from those which project contralaterally, most of the former being “tonic” in properties and most of the latter being “phasic.”

2. The field potential analysis The single unit analysis just presented

suggests specific differences between X- and Y-cells in the projection of ipsi- and contralaterally projecting cells of each type, and these differences should be evi- dent in the antidromic field potentials generated in the retina by optic tract stimulation. Results of an experiment done to test these patterns are illustrated in figure 3. The diagram at the top of figure 3 represents the positions of 12 electrode penetrations made into the retina at, nasal to and temporal to the area centralis. The positions were plotted onto the tangent screen which the cat faced by projecting on to the screen the tip positions of the electrode, as seen ophthalmoscopically. The technique of projection has been described elsewhere (Bishop, Henry and Smith, ’71). These projected positions are labelled 1- 12, in their nasal-to-temporal sequence. Positions 4-8 are within an area circum- scribed by a broken line. This line is the “5 msec isolatency line” defined in a previous analysis (Fukuda and Stone, ’74a) to localise the area centralis. The antidromic field potentiah recorded at the 12 recording positions following OT stimulation are shown in two columns in the lower part of figure 3. The rows are numbered 1-12, to indicate the positions at which particular potentials were recorded. Two traces are shown for each position, one (left column) showing the field potentials (if any) elicited by stimulation of the contralateral OT, the other (right column) showing the potentials (if any) elicited by ipsilateral OT stimulation. These antidromic potentials have been described and analysed previously (Stone and Freeman, ’71 ; Stone and Hoffmann, ’72; Fukuda and Stone, ’74a). Each potential typically comprises early and late components (indicated’ by

labelled arrows at the top of the left column in figure 3, and at the bottom of the right column). The early component is generated by the antidromic invasion of the cell bodies of Y-cells in the region of the electrode tip, and the later component is generated by the antidromic invasion of X-cell bodies.

Because of the small size of W-cell somas (Stone, ’73; Fukuda and Stone, ’74a,b; and see below) and the scatter of their axonal conduction velocities (Stone and Fukuda, ’74) the antidromic invasion of these structures does not generate clear- cut field potentials, and the field potential analysis yields no information about W- cells. But making only the assumption that the field potential recorded at a particular location is generated by cells close to the electrode tip (i.e., close relative to the di- mensions being tested), these recordings should and do provide a test of the patterns of X- and Y-cell distribution deduced from single unit work. The single unit analysis predicts, for example, that over a narrow region centred at the area centralis (the region of “X-cell overlap”) an X-cell potential should be evoked by both ipsi- and contralateral OT stimuli. Correspond- ingly a n X-cell potential is apparent a t positions 5, 6 and 7 following both ipsi- and contralateral stimuli (i.e., in both left and right column traces). The single unit analysis also predicts that within this region the Ycell potential should be elicited predominantly from the contralateral optic tract, and this too is the case. At positions 5, 6 and 7 the ipsilaterally-elicited Y- potentials are almost indistinguishable,

Fig. 3 Analysis of field potentials recorded at, nasal to and temporal to the area centralis following electrical stimulation of the optic tract (OT). The diagram at top shows the pattern of electrode penetrations (labelled 1-12) used for this analysis. The position of the tip of the electrode, as observed ophthalmoscopically, was projected onto the tangent screen, using techniques described by Bishop, Henry and Smith (’71). The dotted line is a “5 msec isolatency line” plotted as described previously (Fukuda and Stone, ’74a) to localise the area centralis. The terms “nasal” and “temporal” refer to direction i n the retina.

In the lower part of the diagram are shown the field potentials recorded at these 12 locations following OT stimulation. Potentials recorded following stimulation of the contra- and ipsilateral OT are shown in the left and right columns, respectively.


whereas the contralaterally-elicited Y- potentials can be distinguished as far tem- potentials are substantial. The single unit poral as position 10. The same features analysis further predicts that substantial are apparent in a previous illustration of contralaterally elicited Y-potentials should these potentials, recorded in an earlier ex- be recorded for a small distance temporal periment (figs. 2B,C in Stone and Free- to the area centralis. Correspondingly, fig- man, '71). ure 3 shows that contralaterally elicited Y- Thus the field potential analysis seems

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to support three conclusions reached from the single unit analysis, ( a ) that ipsi- and contralaterally projecting X-cells intermingle over a narrow region at the area centralis, ( b ) that Y-cells in the region of X-cell overlap project predominantly contralaterally and ( c ) that for Y-cells the region of transition from contra- to predominantly ipsilateral projection lies temporal to the region of X-cell overlap and hence temporal to the area centralis.

3. T h e cell size analysis In the above analyses Y-, X- and W-cells

were distinguished by purely physiological criteria. Substantial evidence is available, however, that the somas of Y-, X- and W- cells differ markedly and consistently in size, Y-cells having the largest somas and W-cells the smallest (Stone, '73; Boycott and Wassle, '74; Fukuda and Stone, '74a,b; Stone and Fukuda, '74). The qfferent retinal distributions of ipsi- and contralaterally projecting cells of the three physiologically defined types should be reflected, therefore, in the retinal distributions of ipsi- and contralaterally projecting cells of different sizes. The retinal distributions of ipsi- and contralaterally projecting ganglion cells can be seen in the retinas of a cat in which one optic tract has been sectioned, causing the ganglion cells whose axons formed that tract to degenerate. Retinas from such animals formed the basis of a previous report (Stone, '66), and we have examined these three pairs of retinas, and the retinas of a recently sectioned animal, giving particular attention to the distributions of cells of different sizes,

Basic observations, If the correlation just discussed between cell type and soma size is valid, two main predictions can be made from the physiological analysis concerning the distribution of ganglion cells in the retinas of tract-sectioned cats. In- spection of whole mounts of these retinas (figs. 4, 5) suggests that both predictions are borne out.

First, in the course of the single unit analysis presented above (fig. 2 ) , a considerable number of contralaterally projecting ganglion cells was encountered temporal to the region of X-cell overlap. Considerable numbers of ganglion cells in

temporal retina should therefore survive section of the ipsilateral optic tract, correspondingly, Stone ('66) reported that approximately 25% of the ganglion cells throughout temporal retina survive section of the ipsilateral tract. Such cells are illustrated in figure 4B and in figure 1B of the earlier study (Stone, '66). Further, the single unit analysis indicates that a majority of these contralaterally projecting cells in temporal retina are W-cells, a minority being Y-cells. The majority of these cells should be small (4 15 pm) in soma diameter, a minority being large (> 22 in diameter). Cells intermediate in size (i.e., X-cells) should be absent. (For de- tails of the size ranges of the somas of Y-, X- and W-cells, see Fukuda and Stone ('74a) and below.) Accordingly the ganglion cell somas in figure 4B (which shows an area 2 mm temporal to the area centralis in the right retina of an animal in which the right optic tract had been sectioned) are almost all small (6 15 pm in diameter), one large (> 22 rm) soma being present, and the same range of cell sizes is found throughout temporal retina. For comparison, the corresponding region of a normal retina is shown in figure 4A; large, medium and small ganglion cells are present.

Second, the physiological analysis suggests that ipsi- and contralaterally projecting X-cells intermingle within a narrow (1" wide) region (the region of X-cell

Fig. 4A Area of methylene blue stained whole mount of a normal retina, approximately 2 mm temporal to the area centralis. Large, medium and small ganglion cell somas are present (c.f., fig. 5 in Fukuda and Stone ('74a)).

Fig. 4B Similarly located area of temporal retina, from the ipsilateral (Le., right) retina of a cat in which the right optic tract had been sectioned. Only large and small somas (i.e., the somas of Y- and W-cells) are present.

Fig. 4C Area of the median strip of overlap from the retina contralateral to the sectioned tract. The area shown is approximately 350 p m above the area centralis. The surviving cells project ipsilaterally. The great majority are X-cells (figs. 2 , 3 ) and their somas are of medium size (15-22 pm diameter).

Fig. 4D Area from the median strip of the same retina as i n C, at the area centralis. The surviving cells are also predominantly X-cells, but their somas are smaller than those in C. This size difference is analysed further in the text related to figure 7.


overlap) which is centred on the area also indicates that ipsi- and contralaterally centralis and corresponds to the “median projecting ganglion cells found within the strip of overlap” described previously median strip differ markedly in their W/ (Stone, ’66). The physiological analysis X/Y composition, the ipsilaterally project-

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ing cells being predominantly X-cells, the contralaterally projecting cells including many X-cells but also including the great majority of the W-cells and Y-cells normally found within the median strip. Cor- respondingly the somas of the ipsilaterally projecting cells in the median strip should be predominantly intermediate in size, since they are predominantly X-cells; these cells are shown in figures 5A,B,C and, at higher power, in figures 4C,D. Conversely the contralaterally projecting cells in the median strip (shown in figs. 5D,E,F) should include many intermediate-sized somas, but should include more large somas and many more small somas than are found among the ipsilaterally projecting cells. Comparison of figures 5A,B,C with figures 5D,E,F confirms these predictions. The difference in soma size between the ipsilaterally projecting cells found at the area centralis (figs. 4D, 5C) and those found more peripherally (figs. 4C, 5A,B) is taken up below.

In summary, the above observations seem to give close support to the following conclusions reached from the physiological analysis. First, the region of X-cell overlap described above corresponds to the median strip of overlap described previously (Stone, '66) and therefore is centred on the area centralis. Second, most Y-cells located in this strip project contralaterally, while most Y-cells located more than 1-2" temporal to the strip project ipsilaterally. Among Y-cells, therefore, a region of transition from predominantly contralateral to predominantly ipsilateral projection can be specified. It is located slightly temporal to the analogous transition zone for X-cells. Third, most W-cells in the region of X- cell over1 ap project con tr alaterally . Fourth, many W-cells and a few Y-cells in tem- por a1 retina project contralater ally.

More detailed observations. Accepting that the retinal distributions of large, medium and small ganglion cell somas re- flect the retinal distributions of (respectively) Y-, X- and W-cells, several more quantitative questions can be answered concerning the retinal distributions of ipsi- and contralaterally projecting Y-, X- and W-cells.

First, it was noted above that small numbers of large cells (presumably Y-cells)

located throughout temporal retina project contralaterally, What percentage do these cells form of the total Y-cell population in temporal retina? To estimate this we measured the numbers of large (> 22 pm) somas present in corresponding areas of temporal retina in the two retinas of a tract-sectioned cat. Over areas of retina of 3.5 mm2 located more than 300 pm temporal to the region of X-cell overlap, 170 large cells were present in the retina contralateral to the sectioned tract, and 10 large cells were present in the ipsilateral retina, By this estimate 5.5% of Y-cells in temporal retina project contralaterally. In the single unit sample (fig. 2D), one of the 35 Y-cells encountered more than 2 cm ( 1 ) temporal to the region of X-cell overlap projected contralaterally, a comparable proportion,

Several further questions can be answered by reference to figure 6. This figure represents an attempt to express quantitatively the retinal distributions of ipsi- and contralaterally projecting cells of different sizes. The following analysis was done for each of the retinas of a cat in which the left optic tract had been previously sectioned. A montage of photomicro- graphs was made (magnification 500 X ) of the area of retina at and around the area centralis. In each retina a vertically oriented border, the "median edge" of nasal or temporal retina could be defined, as described previously (Stone, '66). A series of contiguous rectangles was marked off on each montage, extending horizontally across the retina, i.e., at right angles to the median edge. The rectangles each measured 100 pm (horizontal) by 200 pm (vertical), and were centred along a line

Fig. 5 Areas from the retinas of a cat contralateral and ipsilateral to a sectioned tract. In the contralateral retina the surviving cells project ipsilaterally (A,B,C). In the ipsilateral retina the surviving cells project contralaterally (D,E,F). The areas shown are from the median strip of overlap in each eye, at the area centralis (C,F) 350 pxn (1.5") above the area centralis (B,E) and 700 pm (3") above the area centralis (A,D). Areas at and away from the area centralis are shown to illustrate the increase i n cell size between the area centralis (C,F) and more peripheral retina (A,B,D,E). The increase is most clear cut among the ipsilaterally projecting cells (com- pare C with A and B). For further analysis see text relating to figure 7.

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SOMA DIAMETER prn Fig. 6 Frequency/soma size histograms obtained for ganglion cells in areas of retina

spaced 100 pm apart, spanning the median strip of overlap. Separate histograms are shown for ipsilaterally projecting ganglion cells (left column, as observed in a retina contralateral to a sectioned tract), and for contralaterally projecting cells (right column, as observed in a retina ipsilateral to a sectioned tract). The areas sampled extend horizontally across the median strip, approximately 700 pm (3") above the area centralis. Both series of histograms are arranged so that the histograms obtained from temporally located retinal areas are at top, from nasal areas at bottom. Indicated by the vertical broken lines are the estimated diameter ranges of W-, X- and Y-cells.


which passed 700 pm above the area centralis. (For reasons taken up below, the areas of retina studied were chosen to be out of the area centralis.) Each rectangle was thus 0.02 mm2 in area, and we measured the soma size of each ganglion cell in each rectangle, recording its diameter as the mean of its longest and shortest axes (as previously, Stone, ’65; Boycott and Wassle, ’74; Fukuda and Stone, ‘74a). Cell size spectra were thus obtained for regions of retina spaced 100 pm apart, and spanning the median strip of overlap. Eleven such rectangles were marked off in each retina and the frequency/cell size histograms obtained from them are shown in figure 6. The retina contralateral to the tract section contains ipsilaterally projecting ganglion cells and the histograms obtained from this retina are shown in the left column of figure 6, with more temporal areas of retina at the top. The other retina contains contralaterally projecting cells and the histograms obtained are shown in the right column of figure 6, also with the temporal areas a t top. The vertical “stacking” of the columns relative to each other was determined by reference to the previous study (Stone, ’66) where it was argued that in one retina the median edge of nasal retina lies 200 pm temporal to the median edge of nasal retina. Histograms in the same row in figure 6, therefore, were obtained from corresponding retinal areas. Also indicated on figure 6 are the diameter ranges of the somas of W-, X- and Y-cells, as determined previously (Fukuda and Stone, ’74a,b; see also below).

Figure 6 shows quantitatively all the features of cell distribution mentioned above as “basic observations.” For example, a region of X-cell overlap can be specified. In the histograms in rows 6 and 7, and only in these rows, substantial numbers of both ipsi- and contralaterally projecting cells fall in the X-cell range. The ipsilaterally projecting cells in this strip are mostly in the X-cell range, while the contralaterally projecting cells include many cells in the W-cell size range and several in the Y-cell range. Further, the contralaterally projecting cells in temporal retina (right column, rows 1-5) are predominantly in the W-cell range, with very few

cells in the X-cell range and an occasional cell in the Y-cell range.

Several specific estimates can also be made from figure 6. For example, of the 38 ipsilaterally projecting cells in the region of X-cell overlap (rows 6 and 7, left column) 33 are in the X-cell range, while of the 70 contralaterally projecting cells in this region (rows 6 and 7, right column) 31 had somas in the X-cell range. Thus, in agreement with the physiological analysis (figs. 2A,B), approximately half the X- cells in the region of overlap appear to project each tract. It is noticeable, however, that in the nasal half of the strip (row 7) the majority of X-cells (18/28) project contralaterally, while in the temporal half (row 6 ) most X-cells (20/34) project ipsilaterally. A similar analysis for W-cells shows that within the region of X-cell overlap a great majority (34/40) of the cells with somas in the W-cell range project contralaterally. In the physiological analysis (figs. 2E,F) five of the six W- cells encountered in the region of X-cell overlap projected contralaterally, a similar proportion. A similar analysis applied to figure 6 allows estimation of the proportions of W-cells in temporal retina which project to each tract. Thus, in retina temporal to the region of X-cell overlap (rows 1-5) 74 contralaterally projecting cells and 45 ipsilaterally projecting cells had somas in the W-cell range. These figures suggest that 60% of W-cells in temporal retina project contralaterally and 40% ipsilaterally. Correspondingly, in the physiological analysis (figs. 2E,F) 19 of the 33 W-cells encountered temporal to the region of X-cell overlap projected contralaterally and the other 14 projected ipsilaterally, very similar proportions.

Further analysis of the histograms of rows 1-5 of figure 6 suggests a consistent difference in soma size between ipsi- and contralaterally projecting W-cells in temporal retina. In histograms of contralaterally projecting cells (right column, rows 1-5) the mean diameter of cells 4 15pm in diameter is 10.2 pm. By contrast, the cells 4 15 pm in the histograms of ipsilaterally projecting cells (left column, rows 1-5) are consistently larger, with a mean diameter of 12.9 pm. It has already been noted above and elsewhere (Fukuda and


Stone, '74a) that ipsi- and contralaterally projecting W-cells in temporal retina differ in receptive field properties, most of the ipsilaterally projecting cells being tonic in properties (as defined previously by Stone and Fukuda, '74) while most of the contralaterally projecting cells are phasic in properties. The present observations therefore suggest that phasic W-cells are smaller in cell body size (about 10 pm in diameter) than tonic W-cells (about 13 pm diameter), It was previously noted also (Stone and Fukuda, '74) that phasic W- cells have on the average, slower conducting axons than tonic W-cells. Thus the relationship between cell body size and axonal conduction velocity which holds for W-, X- and Y-cells (i.e., larger cells have faster axons) may also hold for the two major sub-groups of W-cells.

Ganglion cell size as a func t ion of eccentricity. In the cat retina the mean size of ganglion cell somas increases between the area centralis and peripheral retina, the most frequently encountered size and maximum size both increasing as a function of distance from the area centralis (Stone, '65; Boycott and Wassle, '74; Fu- kuda and Stone, '74a). In retinal areas some distance from the area centralis the cell bodies of Y-, X- and W-cells ( a - , p- and wel ls in Boycott and Wassle's ('74) classification) have largely distinct ranges of soma size (fig. 14 in Boycott and Wassle, '74; Fukuda and Stone, '74a,b). Correspond- ingly, frequency/diameter histograms for ganglion cell somas in peripheral retina show three distinct modes, related to the three cell types (fig. 4 in Fukuda and Stone, '74a). More centrally, however, as mean cell size decreases, the modes of the frequency/diameter histograms coalesce and the size ranges of the different cell types, particularly of W- and X-cells, overlap extensively, the overlap being greatest at the area centralis. Because of the different patterns of projection of X-, Y- and W-cells from the median strip of overlap, the present material provides an oppor- tunity for estimating separately the size ranges of W-, X- and Y-cells at and near the area centralis. Knowledge of these size ranges is important for estimates, presented in a parallel study (Fukuda and Stone, '74a), of the relative frequencies

of W-, X- and Y-cells both at the area centralis and in more peripheral retina.

Evidence is presented above that the ipsilaterally projecting ganglion cells within the median strip of overlap are predominantly X-cells (comprising about 50% of the X-cells in the strip), but also include small numbers of Y- and W-cells. The frequency/size histogram for ipsilaterally projecting ganglion cells in the median strip, a t the area centralis, is shown in figure 7 h (top), The histogram is unimodal, with the mode at 11-12 pm and 95% of these cells fall within the range 9-18 pm. Conversely, evidence is presented above that the contralaterally projecting cells in the median strip comprise a majority of both the W- and Y-cells normally present in the strip, as well as 50% of the X-cells. Correspond- ingly, the frequency/size histogram obtained for contralaterally projecting ganglion cells in the median strip of overlap, at the area centralis (fig. 7A, second row) includes many cells similar in size to the ipsiIaterally projecting cells but also includes more large (> 18 pm diameter) and many more small (< 10 pm) diameter cells. This comparison indicates that at the area centralis, as elsewhere in the retina, the somas of Y-cells are larger than of X- cells, and the somas of W-cells are, on the average, smaller than of X-cells. The histogram in figure 7A, third row, is the sum of the upper two histograms and therefore represents the frequency/size distribution of all ganglion cells at the area centralis (cf . , fig. 4A in Fukuda and Stone, '74a). Sketched on this latter histogram are estimates of the W-, X- and Y-cell components of this distribution. The division between Y- and X-cells was determined by measuring the obviously large cells at the area centralis; all were greater than 18 pm in diameter. The extent of the overlap of the size ranges of X- and W-cells was determined by comparison of the histograms in the top and bottom rows of figure 7A. In the bottom row is shown the frequency/ size histogram obtained for contralaterally projecting cells located about 200 pm temporal to the area centralis. Evidence is presented above that these cells are almost all W-cells, but include small numbers of (in this region two) large (> 22pm) somas, presumably of Y-cells. By the esti-

NASO-TEMPORAL DIVISION OF CAT RETINA 39 1

CELLS SIZES IN MEDIAN STRIP

A Areo ren f ro i i i 6 350urn superior c 700um superior

I p s ' projecting cells

Ips1 I N u m b e r o f cells

cells confro projecting - in

L o

----.

Contro p r o l e c t i n q

SOMA DIAMETER urn

Fig. 7 Analysis of the sizes of ganglion cell somas in the median strip of overlap. In all cases the full width of the median strip was sampled.

Fig. 7A Upper his togram shows frequency/size histogram for ipsilaterally projecting ganglion cells in the median strip at the area centralis. These cells were observed in a retina contralateral to a sectioned optic tract. The second histogram from the top shows the frequency/size distribution obtained for contralaterally projecting ganglion cells in the strip at the area centralis, as observed i n the retina ipsilateral to a sectioned tract. The third histogram from the top is the sum of the upper two histograms. O n it are sketched the estimated W-, X- and Y-cell components of the cell population, (dotted, striped and filled respectively), estimated as described in the text. From this breakdown, mean W-cell size is 9.8 pm, mean X-cell size is 12.9 pm. The histogram at bottom shows the frequency size distribution for contralaterally projecting cells in temporal retina. Evidence is presented in the text that the 8-14 pm mode in this histogram represents the somas of W-cells.

Fig. 7B The same analysis as in A, for the median strip 350 p m (about 1.5") above the area centralis. Mean W-cell size is 10.1 pm, mean X-cells size is 15.1 pm.

Fig. 7C The same analysis as in A and B, for the median strip 700 p m (about 3") above the area centralis. Mean W-cell size is 10.6 pm, mean X-cell size is 17.3 pm. For conclusions drawn from this analysis see text.

mates in figure 7A, X-cells at the area centralis have a diameter range of 9-18 pm, while W-cells have a range of 7.5-14 pm; W-cells comprise approximately 40% of the population, X-cells 59% and Y-cells 1%.

Boycott and Wassle ('74) showed that within 1-1.5 mm of the area centralis mean soma sizes of a- and p-cells (i.e., presumably, of Y- and X-cells) decrease with distance from the area centralis. To measure these decreases, we applied the same analysis as used for the area centralis (fig. 7A) to areas of the median strip 350 pm (approximately 1.5") and 700 pm (3") above the area centralis. The results are shown in figure 7B and C. Confirming Boycott and Wassle ('74), mean X-cell size increases, from 12.9 pm at the area centralis to 15.1 pm at 350 pm eccentricity

and to 17.3 ,,XI at 700 pm eccentricity. This increase can be seen in figures 4C,D and 5A,B,C. Y-cells also increase in soma diameter, from 22 pm at the area centralis to 30 pm or more peripherally. The mean size of W-cells also appears to increase slightly, from 9.8 pm centrally to 10.1 pm at 350 pm and to 10.6 pm at 700 pm. In agreement with other work (Fukuda and Stone, '74a) the relative frequencies of W- and X-cells are relatively constant over this range (35-40% and 59-62% respectively), while the frequency of Y-cells increases steadily, from 1.3% centrally to 1.8% at 350 ,,XI and to 2.8% at 700 pm.

The values just presented for the mean sizes, size ranges and relative frequencies of W-, X- and Y-cells are estimates based


on several assumptions. It is probably fair to comment, however, that the assumptions fit the available data closely, and that this analysis provides a more complete description than previously available of the relative sizes of W- and X-cells a t and near the area centralis.

DISCUSSION

The principal finding of the present study is that each of the three types of cat retinal ganglion cell described in recent studies (Y-, X- and W-cells) has a different pattern of naso-temporal division. These patterns are represented schemati- cally in figure 8. Within each type the cells which project to different sides of the brain are spatially segregated to some degree, the ipsilaterally projecting cells being confined to temporal retina, The degree of segregation differs, however, being most complete among X-cells and least complete among W-cells. Thus all X-cells in temporal retina project ipsilaterally, while 5% of temporally located Y-cells and 60% of temporal W-cells retain the phylogenetically older contralateral projection. Moreover, al- though a restricted region of the retina can be specified for each cell type, across which the laterality of the cells' projection changes from contralateral to more or less completely ipsilateral, the regions are not identical for the three types. For X-cells the region of transition (X-cell overlap) is centred on the area centralis. For both Y- and W-cells the zone of transition is located 1-2" (200-300 p on the retina) more temporal.

What is the significance of these different patterns of naso-temporal division? At this stage a full interpretation still does not seem possible, but several points of interest can be made.

X-cells. First, the pattern of naso-temporal divi-

sion observed among X-cells seems to be well developed in a phylogenetic sense. In that all nasal X-cells project contralaterally, all temporal X-cells project ipsilaterally, there being intermingling of ipsi- and contralaterally projecting X-cells only within a narrow strip centred on the area centralis, the X-cell pattern resembles the ,pattern of naso-temporal division which has

+Temporal ~ Nasal-

t o n t r a I a te r a I lps i la te ro l

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$ 0

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u 5 l U

i 0-1 : 100 F Contralatera l

4- ~ C : W - C E L L S

5 0 5 ANGULAR DISTANCE /degrees)

1 0 1 - 1 ?-

DISTANCE O N RETINA rnrn Fig. 8 Schematic plots of the percentage fre.

quencies of ipsi- and contralaterally projecting ganglion cells as a function of position with respect to the median strip of overlap.

Fig. 8 A X-cells. Fig. 8B Y-cells. Fig. 8C W-cells. The zero position on the abscissa represents the

centre of the median strip of overlap.

been described for the monkey retina (Stone, Leicester and Sherman, '73) and which is likely to be found in man. The point can also be made that X-cells project predominantly to the phylogenetically new visual centres of the forebrain rather than to the midbrain. Correspondingly, X- cells appear to subserve visual functions which, among mammals, may reasonably be considered to be phylogenetically recent developments, specifically high resolution vision and binocular stereoscopic vision. The point has already been made (Fukuda

NASO-TEMPORAL DIVIS :ION OF CAT RETINA 393

and Stone, '74a) that the small size of X- cell receptive fields, their concentration at the area centralis and their projection to the forebrain, make X-cells well suited for high resolution vision. The point is made here that their pattern of naso-temporal division makes X-cells well suited to subserve stereoscopic vision. Investigators of the neurophysiological basis of stereopsis have argued in recent years (Blakemore, '69; Bishop, '70) that among the ganglion cells subserving stereoscopic vision there must be an intermingling within the retina of ipsi- and contralaterally projecting ganglion cells and that, because stereoacuity is maximal a t the fixation point, this region of intermingling should be centred on the area centralis. The present results indicate that only among X-cells is a region of intermingling of ipsi- and contralaterally projecting cells centred on the area centralis.

This suggestion, that retinal X-cells subserve both high resolution vision and stereoscopic vision, is consistent with previous observations that, in area 17 of the cat's visual cortex, cells of one class, the so-called "simple" cells, have both the smallest receptive fields (Hubel and Wiesel, '62), and the most spatially sensitive patterns of binocular interaction, (Bishop, Henry and Smith, '71), and also appear to receive their afferent input from retinal X-cells (via a relay in the lateral geniculate nucleus) (Hoffman and Stone, '71; Stone and Dreher, '73).

W-cells In contrast with X-cells, the segregation

of ipsi- from contralaterally projecting cells seems least developed among W-cells. A majority of the W-cells at the area centralis and about 60% of W-cells in temporal retina retain the phylogenetically old contralateral central projection, Corre- spondingly W-cell receptive fields resemble the retinal receptive fields described in phylogenetically more primitive mammals, such as the rabbit (Barlow, Hill and Levick, '64; Levick, '67) and W-cells project to the phylogenetically old visual centres of the midbrain, and apparently not at all to the forebrain (Hoffmann, '73; Fukuda and Stone, '74a). It seems at least possible that W-cells comprise a phylogenetically

old group of ganglion cells, subserving ex- clusively midbrain functions. This suggestion is a development of an earlier suggestion (Stone, '66) that the contralaterally projecting cells in temporal retina project to the phylogenetically older visual centres of the midbrain.

The observation that subtypes of W-cells project differently from temporal retina, phasic W-cells projecting contralaterally and tonic W-cells ipsilaterally, confirms the suggestion (Fukuda and Stone, '74a) that these cells might subserve quite different visual functions and emphasises the het- erogeneity of W-cells described in the first reports of these cells (Stone and Hoff- mann, '72; Stone and Fukuda, '74). The different patterns of naso-temporal division of tonic and phasic W-cells may prove an important clue in the understanding of their functional roles.

Y-cells Among Y-cells, the segregation of ipsi-

from contralaterally projecting cells is less complete than among X-cells, but more complete than among W-cells. It has been commented elsewhere (Fukuda and Stone, '74a) that the retinal distribution, central terminations, and receptive field properties of Y-cells suggest that they subserve some function of peripheral vision, such as the detection of fast-moving images, which is important to both midbrain and forebrain visual processing. But until more is known of the specific functional role of Y-cells it seems difficult to interpret the pattern of naso-temporal division of Y-cells described here,

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the naso-temporal division of the cat's retina re-examined in terms of y-, x- and w-cells

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