The cortical representation of the retina in squirrel and rhesus monkeys and its relation to visual acuity

EXPERIMENTAL

The and

SE~ROLOG\’

Cortical Rhesus

24, 37k.385

( 1969)

Representation Monkeys A.

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and COWEY

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Retina

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ELLIS

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in Squirrel Visual

Acuity

1

lo,1969

Minimum separable visual acuity was measured by a modified method of limits in ten squirrel monkeys before and after removing various portions of the retinal projection area in striate cortex. The reduction in acuity was closely proportional to the number of degrees of the retinal projection area that were removed. The results were compared with those of a similar experiment on rhesus monkeys and it is shown that the acuity impairment following removal of a given angular extent of the retinal projection in striate cortex also depends on the amount of striate cortex devoted to each degree of the central retina, which is different in the two species. The results are related to the anatomical basis of the minimum angle of resolution in the cerebral cortex and in the lateral geniculate bodies of the thalamus. Introduction

The topographical representation of the retina in striate cortex of various monkeys can be determined by stimulating the retina with small spots of light and recording the position of maximum evoked response in striate cortex. The lateral striate cortex of rhesus monkeys, corresponding to central eight degrees of vision, was examined in this way by Talbot and Marshall (12). A map of the entire striate cortex of rhesus monkeys and baboons was determined by Daniel and Whitteridge (7)) who presented their results in terms of magnification factor; i.e., the number of millimeters of striate cortex corresponding to each degree of visual field along various meridia of the retina. They fomld that the magnification factor, which was about 6-mm degree at the fovea, decreased monotonically with increasing eccentricity from the fovea. This reduction in magnification factor clearly resembled the fall in visual acuity in man with increasing eccentricity of the test stimulus from the visual axis. If the cortical magnification factor for any given region of retina is an important anatomical determinant of visual acuity it follows that two species of monkey with very similar magnification factors would be expected to * This work was supported by Medical Research Council G.967/2/B. We thank Mr. H. Ali Khan and Mrs. L. Bowerman tological material, and Mr. J. Broad for making the photographs. 374

Grants for

G.965/96/B and preparing the his-

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have similar visual acuity. The projection of the retina on to striate cortex has also been mapped for the squirrel monkey (4) where it was again found that the central degree of retina projects to about 6 mm of cortex. When the visual acuity of 12 rhesus and 12 squirrel monkeys was compared the two species were very similar, havin, c mean a&ties of 0.65 and 0.74 min of arc, respectively (5). However, the cortical representation of the extra fovea1 retina is far from identical in the two species; in the squirrel monkey the representation is n~~~l~ more compressed. For example, although both species devote the same absolute amount of cortex to fovea1 vision, the entire extent of the striate cortex of one hemisphere is only about 700 mm’ in squirrel monkeys Sai~ivi scil~~s compared with about 1400 mm’ in rhesus monkeys &fncncn ~~llrtlatta (4). It follows that if the striate cortex corresponding to fovea1 vision is removed in the two species acuity should be much more impaired in Sni~zir-i than in ~~lacaca. This hyy pothesis was tested by measuring visual acuity in ten squirrel monkeys and six rhesus monkeys before and after removing various portions of the striate cortex corresponding to the central retina. The acuity decrements in the squirrel monkey are also related to the extent of the degeneration in the lateral geniculate body (LGB) following damage to striate tortes, and hence to the geniculate representation of the fovea1 region. Methods

i~eas~lrti~rr)~ts of I,‘isllnl Ac~it~r. The procedure for measuring visual acuity has been described elsewhere in detail (5, 13, 14). Briefly, the animals learned to discriminate between a 64-mm circular transilluminated homogeneous field and another bearing vertical stripes, the number and width of which could be altered without changing the luminance of the stimulus, which was identical for both stimuli. The test fields were mounted in trolleys, 1 m from the animal’s cage, and the animal was rewarded with a preferred food for pulling in the trolley bearing the positive stimulus. The stripes were made finer if the animal scored eight or more correct in ten consecutive trials; they were made broader if it scored seven or fewer correct. Criterion threshold was reached when the animal showed no improvement over 800 trials, with 50 trials given daily. Each animal required from 2-3 months of daily testing to achieve criterion. Each animal was tested to criterion preoperatively and again postoperatively, after a gap of 2 months to allow complete recovery from surgery and during which time it performed various pattern discriminations in a different apparatus. Surgery. The operations on rhesus monkeys have already been described (13). Various extents of the retinal projection to striate cortex were removed bilaterally, using the map provided by Talbot and Marshall (12, see

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Fig. 1) as a guide. From 1 to 3” of the cortical representation were removed bilaterally in squirrel monkeys, using the map given by Cowey (4, see Fig. 1) as a guide. Since the striate cortex is clearly visible by virtue of its unusually rich capillary bed it was not difficult to make the lesions as intended. All removals were made by gentle subpial suction with a 21-gauge stainless steel sucker while the animal was under deep Nembutal anesthesia and mounted in a stereotaxic instrument. Particular care was taken not to remove or enter any of the underlying white matter. The visual radiation fibers supplying the ablated cortex and lying immediately beneath it degenerate as a result of removing their terminals and their blood supply, but the next fiber layer supplying striate cortex of the calcarine fissure escapes altogether if the procedure described is successfully carried out. In view of the small size of squirrel monkeys (0.6-1.0 kg) all but minor bleeding was immediately stopped by applying cotton paddies soaked in topical thrombin. When these had been removed the ablated region was covered with a thin layer of “gel-foam,” the dura closed as far as possible with sutures, and the facia then skin sewn together. Bone was not replaced. This operation was performed on seven animals. In three further squirrel monkeys the lesion was deliberately extended into the pre-striate representation of the fovea (4 ) . These animals are included in this study since the pattern of degeneration in the lateral geniculate bodies was indistinguishable from that seen after damage to striate cortex alone and because a small striate plus larger pre-striate removal provided a control for those animals with a larger lesion restricted to striate cortex. All animals were given 0.25 ml penicillin (Penidural) intramuscularly at the end of the operation. Recovery was uneventful, but misreaching for food occurred for several days afterwards. This transient phenomen was

FIG. 1. Posterior (A), medial (B), and ventral (C) views of the left occipital lobe of Saimiri sciureus. Border of striate cortex, representing the vertical meridian, and successive arcs of the projection shown by stippled lines. Numbers refer to degrees eccentricity from fovea. Redrawn from Cowey (4). Dorsal view of left occipital lobe of Maraca mulafta (D) is drawn to same scale from Talbot and Marshall (12).

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undistinguishable from that seen in rhesus monkeys after the same operation (6). I-listolog~~. Histological reconstructions of the brains of rhesus monkys have been published ( 13). The squirrel monkeys were killed at the end of the experiment and perfused through the heart with normal saline solution followed by lO70 formalin. The animal’s head was placed in a stereotasic instrument, the brain exposed, and cut transversely in the vertical plane about 5 mm behind the posterior limit of the lateral geniculate bodies as determined from the atlas of Gergen and MacLean (9 ) The posterior blocks, containing the lesions, were photographed from several angles. Both blocks were placed in 10% formalin for at least 2 weeks, then in a solution of SUCrose formalin (10% formalin, 30% sucrose) until they sank. They were then embedded in albumen to prevent loss of any small tags of tissue around the lesion during sectioning, frozen, and cut as follows. Each anterior block, containing the LGB, was cut coronally at 50 p. Every alternate section was saved. When the LGB had been identified on unstained sections, every other saved section throughout the extent of the LGB was stained with cresyl-violet. Stained sections were therefore 200 TVapart, giving about 20 sections for each geniculate and allowing an accurate reconstruction to be made. In addition, sections 100 ,J apart were stained at the posterior tip of the LGB to improve the accuracy even further. The posterior blocks of the seven animals with striate cortex lesions were cut parasagitally since this plane permits the best reconstruction of striate cortex representing the central 3” of the retina. This representation lies at the back of the brain, extending from lateral to medial as shown in Fig. 1. Sections were cut at SO p and every eighth section saved. Saved sections were stained alternately with cresyl-violet and by Weil’s method for fibers. The lesions were reconstructed by projectin g and drawing all Nissl-stained sections. Those stained by Weil’s method were examined for fiber damage. The occipital lobes of the three animals with some prestriate removal were similarly treated, except that they were sectioned coronally to permit the best reconstruction of cortex extending forwards on the lateral surface. The extent of the retrograde cell degeneration in the LGB was estimated as follows: Figure 5 shows a section through the posterior third of the left LGB of squirrel monkey no. 5. The borders of the degenerated region are sharp and this was typical. Only a few isolated and shrunken cells were present in the atrophied region. Each section was projected at a magnification of 40 diameters and drawn. The length of the dorsal surface, from A to D in Fig. 5, was taken with a map measure and represented as a straight line. The distances from A to B. and C to D were similarly measured and marked on the straight line. which therefore provided a plane and unclistorted representation of the dorsal surface of the small-celled lamina of the

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LGB for a given coronal section. Successive sections were represented by straight lines 40 X 200 p apart. The entire LGB was therefore displayed as though its dorsal surface had been straightened and laid flat, with the degeneration shown in solid black. Its total area and that of the degeneration were then measured with a planimeter. Since anatomical evidence (3, 10, 11) indicates that the fovea projects to the posterior pole of the I,GB with more peripheral regions being represented anteriorally, the distance from the posterior pole to the nearest intact portion of the LGB was measured to see if this as well as the extent of removed striate tortes correlated with any acuity impairment. This distance is shown as a straight white line in the c!iagrams of the reconstructed geniculate bodies (Fig. 2 ) . The latter estimate needs an important qualification. In reconstructing the LGH, distances along the clorsnl surface of a coronal section are represented accurately. Hut there is no correction for the distortion introduced by the curvature of the LGB in measuring bct~er~ sections along the posterior-anterior axis of the geniculate. For example, two points represented in sections 200 p apart may actually be much further apart if the dorsal surface of the geniculate is not horizontal. which of course it is not. The reconstructed geniculate is therefore a true distance projection of the mediallateral axis but is a plane and foreshortened projection of the posterioranterior axis. The estimates of distance from the degenerated posterior pole to nearest intact portion of total area of degeneration are therefore rough approximations, although inaccuracies in the former measurement were minimized by measuring at a constant medial or lateral angle to the posterioranterior axis wherever there was more than one direction giving the same distance. Results

Postoperative acuity impairments occurred in all subjects. They are most conveniently expressed as relative acuity, which is the preoperative divided by the postoperative value. By comparing the histological reconstructions of the striate cortex with the map of the retinal projection on to striate cortex FIG. 2. Histological reconstructions of occipital lobes of S~i~liri sciztrrtrs subjects. Posterior and ventral views were prepared from sections 900 p apart. Medial view of animals with lesion restricted to striate cortex prepared from photographs of the medial surface of each hemisphere. Missing cortex is shown in black ; stippling indicates intact striate cortex. Smallest eccentricity of intact striate cortex is shown hy white arrow for each animal. Reconstructions of superior surface of LGB are shown at bottom, with posterior pole below. Area of retrograde cell degeneration is shown in black. Horizontal lines indicate plane of sections used in reconstruction. Sections 100 p apart were used at the posterior pole where deg-eneration is most prominent. White arrow indicates shortest distance from posterior pole to intact portion. The cross section of each hemisphere was selected to show a region where the lesion was largest.

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(Figs. 1 and 2) it was possible to determine how many degrees of the central projection had been removed. For example, in SM.1 the central so is missing whereas in SM.10 the nearest intact striate cortex lies on the 3” meridian. Relative acuity is plotted as a function of the smallest eccentricity of intact striate cortex in Fig. 3, where the points for the rhesus monkey have been taken from \\‘eiskrantz and Cowey ( 14 ). The graph confirms the principal prediction made in the introduction; namely, that the squirrel monkey is significantly more impaired than the rhesus monkey when both are deprived of striate cortex representing the first few degrees of the central retina. Figure 4 shows relative acuity, for squirrel monkey, as a function of the distance from the posterior poles of the LGB to the nearest intact region. Despite the reservations about the accurancy of this measurement there is a clear correlation between reduction in acuity and the extent of the LGB that is degenerated and this result suggests that the estimates of the smallest eccentricity of intact striate cortex are indeed correct. Furthermore, it can be seen from Fig. 2 and Table 1 that in every animal where the cortical lesions are unsymmetrical the shortest distance from the zero (foveal) projection to intact striate cortex and from the geniculate pole to nearest intact cells lies in the same hemisphere, as it should. Perhaps the most strikin g feature of the degeneration in the LGB is that the disproportionately large representation of the central few degrees of the retina exists at the geniculate as well as the cortical level. In order to determine how closely the geniculate and cortical magnifications of the fovea1 region correspond in the squirrel monkey the area of striate cortex representing the central 2” was measured on four freshly perfused hemispheres (see Ref. (1) for method) and espressed as a percentage of the entire striate cortex of one hemisphere, which is known to be about 722 mm? (4 j . This percentage was then compared with the percentage degeneration of the superior surface of the LGB. following removal of the striate representation of the central 2”. The first 2” were found to occupy about 98 mm?, or 14% of the striate cortex of one hemisphere. Animals in which approximately the central 2” of the projection have been removed in each hemisphere are SM.8 and SM.9, and the percentage of the LGB that has degenerated in the four hemispheres is from 13 to 16% (Fig. 2 and Table 1) indicating that the geniculate and cortical representations of the fovea1 region are indeed approximately equal and therefore similarly disproportionate with respect to the remainder of the projection. It was not possible with the relatively few sections available of the LGB of rhesus monkeys to perform a similar analysis in this species. However, Clark (2) determined that in lKucacn ~r~tlnffa a small circular lesion of striate cortex of that hemisphere led to retrograde degeneration of l/70 of

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the volume of the small-celled laminae in the ipsilateral LGB. It therefore seems likely that the large cortical magnification of the central retina is also present in the thalamus of this species. Discussion

The chief finding reported here is that removing the fovea1 projection area in striate cortex leads to greater impairment of visual acuity in squirrel monkeys than in rhesus monkeys. And the explanation given is that the projection of more peripheral retinal areas is much more compressed in S&&i. This finding, together with the fact that both species have approximately equal magnification factors for the fovea and also have very similar normal visual acuity (5) supports the suggestion that the cortical magnification factor is an important anatomical basis for minimum angle of resolution (7). Acuity and the cortical magnification factor should also be related to the density of cones across the retina, and it has been determined that Sahiri and Macaca have nearly equal cone densities per unit angle at the fovea whereas the density per unit angle declines more rapidly in Sai+~ziri with increasing eccentricity (Rolls and Cowey, in preparation). However, the density of ganglion cells is probably a more appropriate measure since this is likely to govern the size of receptive fields (and therefore acuity) than the density of receptors. Unfortunately, the absence of ganglion cells at the fovea itself-they are shifted laterally and away from the foveal pit-makes it impossible to relate ganglion cell density and eccentricity for the central few degrees on the retina since it is not clear which part of the central retina any particular ganglion cell is serving. The most likely artifact in the experiment reported here is that the cortical lesions in Saiwivi damaged underlying radiation fibers supplying striate cortex in the calcarine fissure. If so, the effect would be to produce larger field defects than intended, and the relatively severe acuity loss found in Saimiri would not be surprising. There are several reasons for discounting this possibility. First, the underlying striate cortex of the calcarine fissure and its fiber layer appeared to be intact. Second, accidental involvement of

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FIG. 5. Coronal section 50 b, through posterior third of left LGB of Sb1.5. Animal was killed 6 months after removal of part of posterolateral striate cortex. Note sharp boundary of degenerated area. Measurements were made along superior surface from .i to D, A to B, and C to D. Although lamination is diflicult to see in the small-celled mass, it can he demonstrated by uniateral enucleation (8). The measurements are therefore kno\vn to he made on lamina 6. which covers the dorsal surface of the LGB.

this region is just as likely in both species. Third, there was no evidence of islands of degeneration in the LGU in Sniwivi, except to a trivial extent in one animal (Fig. 2. SM.10 ) . Last. the fairly close correspondence between

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the proportion of striate cortex devoted to the central 2” of the retina and the proportion of the LGB showing degeneration when the former is removed makes good sense. One feature of the pattern of degeneration in the LGB is puzzling. Almost without exception the degeneration is wide at the posterior pole and shows a long tail extending anteriorly along the mid-line of the geniculate. This tail is even more prominent than shown in Fig. 2, when the foreshortening of the anterior-posterior axis of the LGB is taken into account. The anterior-posterior mid-line axis of the LGB is probably the representation of the horizontal retinal meridian (as in rhesus monkeys (11, p. 334-389) and this supposition is supported by the observation that where the cortical lesion is more extensive either above or below the representation of the horizontal meridian the retrograde degeneration is more extensive in the lateral or medial half of the LGB (Fig. 2 ) . The long tail of degeneration in the representation of the horizontal meridian could indicate that the magnification factor along that meridian is disproportionately high. Chacko (1) in her careful examination of the LGB of various species of monkey drew attention to the conspicuous thinning of cells in the central region of the normal LGB of SaimX. Thus, any increase in the absolute amount of the geniculate devoted to the horizontal meridian may simply be a reflection of the increasing distance between cells. It is also possible that visual acuity diminishes least rapidly along the horizontal retinal meridian in the squirrel monkey and that this meridian therefore occupies a relatively large part of the LGB. There is no indication in either Saitpzivi or Maraca that the cortical magnification factor differs along the representations of different radii of the retina (4. 7) but the density of retinal ganglion cells is certainly greater along the horizontal meridan of the baboon eye (15). It would not be surprising if both the spacing of geniculate cells and the distribution of retinal elements along the different retinal meridia contributed to the prominent representation of the horizontal meridian in the LGB. References 1.

L. W. 1954. The lateral geniculate body in the new world monkeys. J. Sot. India 3 : 62-74. CLARK, W. E. LE GROS. 1941. The laminar organization and the cell content in the lateral geniculate body of the monkey. J. A~zut. ‘75 : 419-432. CLARK, W. E. LE GROS, and G. G. PENMAN. 1934. The projection of the retina in the lateral geniculate body. Proc. Roy. SoL-. London. Ser. B, 114: 291-313. COWEY. il. 1964. The projection of the retina on to striate and prestriate cortex in the squirrel monkey, Saimiri scizwcus. J. Nenropltysiol. 27 : 366-39.3. COWEY, .4., and C. M. ELLIS. 1967. Visual acuity of rhesus and squirrel monkeys. J. COW/J. Pkpiol. Psychol. 64 : 80-84. COWEY, A., and L. WEISRRANTZ. 1961. Role of experience in misreaching produced by visual cortex lesions. Natwr 192 : 1319. CHACKO,

drtat.

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P.M., and D. WHITTERIDGE. 1961. The representation of the visual field on the cerebral cortex in monkeys. J. PIrysiol. Lolldon 159 : 203-221. DOTY, R. W., M. GLICKSTEIN, and W. H. CALVIN. 1966. Lamination of the lateral geniculate nucleus in the squirrel monkey, Saigrziri sciurczts. J. c’ofrrp. Nenrol.

DANIEL,

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10.

J. A., and P. D. MACLEAN. 1962. “A Stereotaxic .4tlas of the Squirrel Monkey’s Brain.” Public Health Service Publication No. 933, U.S. Govt. Printing Office, Washington, D.C. NAEVE, H., P. GLEES, and W. HALLERMANN. 1967. Die Projektion zentraler und peripherer Netzhautanteile auf das Corpus Geniculatum laterale des Affen.

GERGEN,

.4rch. Ophtltdn~ol. 11.

POL~AK,

S. 1957.

173

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225-233.

Vertebrate

\‘isual

System.”

University

of Chicago

Press,

Chicago.

12.

S. A., and W. H. MARSHALL. 1941. Physiological studies on neural mechof visual localization and discrimination. .41n. J. Ophthal. 24: 1255-1264. 13. WEISKRANTZ, L., and A. CO\TEY. 1963. Striate cortex lesions and visual acuity of the rhesus monkey. J. Co+rtb. Physiol. Psychol. 56 : 225-231. 14. WEISKRANTZ, L., and A. COWEY. 1967. Comparison of the effects of striate cortex and retinal lesions on visual acuity in the monkey. Scicncc 155 : 104-106. 1.5. WHITTERIDGE, D. 1965. Geometrical relations between the retina and the visual cortex, pp. 269-276. III “Mathematics and Computer Science in Biology and Medicine.” Medical Research Council, London. TALBOT,

anisms