The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (macaca mulatta): An autoradiographic study

Brain Research, 108 (1976) 1-24

1

© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

Research Reports

THE CORTICAL PROJECTIONS OF THE INFERIOR PULVINAR AND ADJACENT LATERAL PULVINAR IN THE RHESUS MONKEY (MACACA MULATTA): AN AUTORADIOGRAPHIC STUDY

L. A. BENEVENTO AND MICHAEL R E Z A K

College of Medicine, University of Illinois Medical Center, Chicago, Ill. 60680 (U.S.A.) (Accepted October 10th, 1975)

SUMMARY

An autoradiographic technique was used to determine superior colliculus (SC) and pulvinar projections in the rhesus monkey. SC projects bilaterally to the inferior pulvinar (PI) while occipital cortex projects to PI and the lateral pulvinar (PL). PI has sustaining, topographical projections to layers IV, III and I of areas 18 and 19 (and VI and I of 17) which agrees with the central representation of the visual hemifield and suggests that there is more than one hemifield representation in prestriate cortex. PL adjacent to PI also projects to the same cortical areas and layers, while the portion of PL extending into the caudal pole of the pulvinar projects to layers IV, III and I of areas 20 and 21. Thus, occipital cortices are associated by cortico-thalamocortical connections and also receive direct lemniscal input via SC-PI and the dorsal lateral geniculate nucleus (DLG), while inferotemporal areas 20 and 21 receive only cortico-thalamocortical connections. It is concluded that Stoffels' principle of lamellation holds and, that one pulvinar subdivision projects to several cortical areas, that adjacent pulvinar subdivisions have overlapping projections to these cortical areas and their layers and that the pulvinar also projects to the same cortical area as DLG but to different layers. These connections are similar to those in lower mammals but not to those in the squirrel monkey and bushbaby.

INTRODUCTION

Despite the fact that the pulvinar complex is a dramatic feature of the simian thalamus 60, anterograde studies of the cortical projections of the pulvinar complex, or

2 its homologue, have received the most attention in prosimians 29, cats 3°-32,47,53 and lower mammals 7,34-36,5°. To date the most detailed investigations of the cortical projections of the pulvinar in simians such as the rhesus monkey (Macaca mulatta) have made use of the retrograde cell degeneration technique 16,18,'al,26,39,4%6°. Ablations of identifiable subdivisionsr~,13, is of the preoccipital gyrus (prestriate cortex) and of the middle and inferior temporal gyri (inferotemporal cortex) defined a general topography of retrograde cell degeneration within the inferior pulvinar and adjacent portions of the lateral pulvinar18, 21,26,39. Such studies have also shown that ablations of the subdivisions of occipital and inferotemporal cortices are related to different visual deficits in behavioral experiments~6,19,')1, 24,26,39,61,62. It appears that the degree of complexity of visually guided behavior which is lost increases as the cortical ablation is moved from occipital to inferotemporal cortices, presumably due to the dependence of prestriate and inferotemporal cortices on convergent corticocortical inputs originating from the striate cortex (area 17)8,22,23,4°,41,58,65,66. The existence of identifiable, functionally distinct and interconnected subdivisions of prestriate and inferotemporal cortex which may be related to a topographical input from the pulvinar led to one aim of the present anterograde autoradiographic study in the rhesus monkey. This aim was to detail the cortical areas and layers of projection of the inferior pulvinar and adjacent lateral pulvinar and to compare the topography of these projections with the topography of the known projections from striate cortex to prestriate cortex and prestriate cortex to inferotemporal cortex. Other recent anterograde studies in the rhesus monkey have detailed ipsilateral tectal 1° and cortical 4,9A°,17 inputs to the pulvinar. These studies have shown that there are topographical projections to the inferior pulvinar from the striate cortex and superficial layers of the superior colliculus related to a representation of the visual hemifield which is similar to that demonstrated physiologically in the inferior pulvinar of New World monkeys 3. Moreover, one of these studies 11 has shown that the regions of the inferior and lateral pulvinar receiving projections from occipital cortex have sustaining projections 52 which associate area 17 with the prestriate cortex. Thus, another aim of the present autoradiographic study was to compare the topography of the projections of the inferior pulvinar with the topography of the representation of the visual hemifield in the thalamus and cortex2a, 5s and to determine which regions of prestriate and inferotemporal cortices receive projections from the areas of the pulvinar which receive separate and overlapping projections from the occipital cortex and the superior colliculus. Finally, since our previous anterograde degeneration z7,46 study ~0 reported only the ipsilateral projections of the superior colliculus, and one aim of the present study is to demonstrate the cortical projections of the areas of the pulvinar which receive separate and overlapping projections from the cortex and tectum, we have repeated the studies on the superior colliculus with the autoradiographic tracing method in order to determine the presence of bilateral projections to the pulvinar. The following results will show that there are bilateral projections from the superior colliculus to the inferior pulvinar and that the topography of the cortical projections of the inferior pulvinar is related to the representation of the visual hemi-

field. The results expand upon the topographical maps reported in the retrograde degeneration studies and indicate that there is more than one representation of the visual hemifield in prestriate cortex of the rhesus monkey. Further, it will be shown that the corticorecipient zone of the lateral pulvinar and the cortical and tectal recipient zones of the inferior pulvinar have overlapping projections to the same areas and layers of prestriate cortex, while only the corticorecipient zone of the caudal pole of the pulvinar projects to inferotemporal cortex. These various connections provide another basis, in addition to corticocortical connections, for explaining the different functions attributed to the various subdivisions of occipital and inferotemporal cortices. A preliminary report of these findings has been given elsewhere4S,49. MATERIALS AND METHODS

Eleven young adult rhesus monkeys (Macaca mulatta) weighing 3.0--4.0 kg were used in the present study. The animals were anesthetized with pentobarbital sodium (30 mg/kg) and placed in a stereotaxic instrument. Microinjections of 0.5-1.0 #1 of sterile normal saline solution containing L-[2,3-3H]proline (spec. act. 39.7 Ci/mmole) and L-[4,5-aH]leucine (spec. act. 5 Ci/mmole) at a concentration of 20 #Ci//~l were made stereotaxically in the two most superficial layers of the superior colliculus, the inferior pulvinar and the lateral pulvinar. The tritiated amino acid solution was injected with a 5-#1 Hamilton fixed-needle syringe held on a slightly modified version of a David-Kopf carrier. In order to prevent tissue damage a David-Kopf hydraulic microdrive was used to displace the plunger of the syringe at such a rate as to allow 1/~1 of the solution to be delivered over a 3-h period. The needle remained in place in the brain for at least 30 min before and after the injection and no label was seen along the needle tract. Survival times of 1-5 days were used in order to allow for the slow and fast components of axoplasmic flow to label the thalamocortical axons and axonal endings ~5. At the end of the survival times the animals were perfused transcardially with a solution of 0.9 % saline followed by 10 % formalin. The calvarium was then removed and the brains blocked transversally in a stereotaxic plane. The brains were subsequently transferred to a 30 % sucrose solution made with 10 % formalin until they sank. After the brains sank in the sugar solution, frozen sections were cut in the transverse plane at 20/zm and placed in compartmentalized trays containing 2% formalin. Every 10th or 20th section throughout the brain was washed and mounted on acid-clean glass slides. The mounted sections were processed in a manner similar to that detailed by Cowan et al. ~o. The mounted sections were defatted, dried at 40 °C overnight, and dipped in Kodak NTB-2 emulsion which was diluted 1:1 with a 0.25 Dreft detergent solution. The slides were hung and dried in a special light-tight box for several hours and then transferred to light-tight slide boxes containing Drierite dessicant for 6-8 weeks at 2 °C. Test slides were developed weekly in order to assess an appropriate development time for the series. The slides were developed in full strength Kodak Dektol at 15 °C, fixed with Kodak Rapid Fix and stained with cresyl violet or toluidine blue. Heavy densities of grains outlining projection pathways were quite

4 visible in the thalamus, internal capsule and cortex. Although the pattern and distribution of grains labeling thalamocortical axons and endings was obvious under the microscope, quantitative verification of each brain was made by performing grain counts on sampled sections at × 1000 using a grid method 2~. The grain counts revealed densities up to × 200 that of background in the cortical projection sites (see Fig. 9). The hippocampus and corpus callosum were used as a control for background counts since we know of no evidence for superior colliculus or pulvinar projections to these regions. The distribution and density of grains in each section was plotted using an electronic 'pantograph' as described elsewhere 6. The method consisted of projecting the image of each section at an optical magnification of × 8 in order to trace the outline and visible internal structures. The same slide was then placed on the stage of a Zeiss microscope and its drawing on the platen of an X-Y plotter. Linear motion transducers on the X and Y axes of the microscope stage were coupled to the X and Y amplifiers of the plotter. Thus, the point of the section viewed under the ocular hairline of the microscope could be matched to the comparable point on the tracing which was under the pen of the plotter. The sections were read at × 400. In order to correlate the information about thalamocortical connections with the various cytoarchitectonic subdivisions of the neocortex, both the information from the plots and Nissl stains were mapped onto surface photographs of the hemisphere. Cortical cytoarchitecture was identified with the aid of the definitions of Von Bonin and Bailey lz and Brodmann 15. Before presenting the results it is useful to briefly review the definitions of the cortical subdivisions*. Von Bonin and Bailey 1~ cytoarchitecturally divided prestriate cortex into areas OB and OA (corresponding generally to Brodmann's 15 areas 18 and 19) and inferotemporal cortex into an anterior area called TE which corresponds generally to Brodmann's areas 20 and 21. Another cortical subdivision located at the junction of the ventral prestriate cortex and posterior inferotemporal cortex and separated from area TE also seems probable in the macaque monkey based on behavioral, physiological and connectional studies 21,z6,2s,~3,39,57 and reconstructions o f V o n Bonin and Bailey's cytoarchitectural data 12 (see especially arguements of Iwai and Mishkin39). Moreover, in a later study ~3 Von Bonin and Bailey relabeled the junctional area in the macaque 'TEO' (corresponding to Brodmann's area 37), thus distinguishing ventrolateral OA, or the region of the prestriate cortex encompassing central vision3Z, zg, from the remainder of OA and TE (see Fig. 2). In this paper we have designated area TEO as the cortex located between the superior temporal and occipitotemporal sulci and extending from the cortex near the tip of the lunate sulcus and about the inferior occipital sulcus to the cortex about the posterior middle temporal sulcus. RESULTS

Superior colliculus projections to the pulvinar. Fig. 1 illustrates our largest injec* For all abbreviations see p. 21.

tion into the superficial layers of the superior colliculus (stratum griseum superficiale and stratum zonale) and a plot of the grains seen in the ipsilateral and contralateral inferior pulvinar nuclei (see also Fig. 9). The projections of occipital cortex to the pulvinar as determined in our previous studies4,9,10 are also shown for comparison. The rostral-caudal extent of the injection extended over the central one-third of the superior colliculus and thus overlapped the cortical and retinal inputs to the superior colliculus ~4 as well as central and peripheral representations of the visual field about the horizontal meridian 54. The ipsilateral distribution of grains within the inferior pulvinar agreed with the projection pattern seen in our previous degeneration study 10: the grains extended from about the level of the caudal pole of the medial geniculate nucleus (Fig. 1C and D) to the level of the caudal pole of the dorsal lateral geniculate nucleus (Fig. IA). At the level of the junction of the superior colliculus and pretectum (Fig. 1D) and at the level of the caudal pole of the medial geniculate nucleus (Fig. 1C) two separate foci of grains were seen, one situated lateral to the other, apparently within the medial portion of the inferior pulvinar (Fig. 1D). The grains did not extend into the region of the pulvinar which receives projections from occipital cortex. This medial location of both foci in the caudal inferior pulvinar is only apparent since the lateral pulvinar, at these levels, tends to cup the inferior pulvinar laterally and somewhat ventrally. Thus, at these levels the two foci extend across the entire inferior pulvinar. At rostral levels (Fig. 1A and B), the ipsilateral distribution of grains was found across the middle of the inferior pulvinar, extending into the zone which receives occipital projections. Most rostrally grains were also found in the dorsolateral portion of the inferior pulvinar and in the adjacent magnocellular layers of the dorsal lateral geniculate nucleus (Fig. 1A). At this level there is complete overlap of the tectal and occipital projections to the inferior pulvinar. In contrast to the ipsilateral distribution of grains in the inferior pulvinar, the contralateral distribution of grains in the inferior pulvinar, resulting from the same injection in the superficial layers of the superior colliculus, was found only in the portion of the inferior pulvinar which receives little input from occipital cortex (Fig. 1D). That is, in the contralateral inferior pulvinar the grains were found confined to the dorsal and medial portion at about the level of the junction of the superior colliculus and pretectum. The light density of grains in the contralateral tectorecipient zone of the inferior pulvinar and the short survival times for these cases (about 1 day) precluded an accurate determination of the route taken by the decussating fibers, although it appeared to involve the commissure of the superior colliculus. These corticorecipient and tectorecipient zones of the pulvinar will be related to the regions of prestriate and inferotemporal cortices which receive projections from the pulvinar. Cortical projections of the pulvinar. Before presenting the results in detail it is helpful to introduce some findings which were consistent for all the cases. First, the location of grains in the cortex is related to the location of the injection site in the pulvinar. In this study injections were placed dorsally and ventrally along a rostralcaudal axis extending from the portion of the pulvinar adjacent to the caudal pole of the dorsal lateral geniculate nucleus to the region of the pulvinar forming the caudal

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Fig. 1. Plots of transverse sections (A, most rostral; F, most caudal) through the superior colticulus and pulvinar illustrating the regions of the inferior pulvinar which receive ipsilateral (hatching) and contralateral (cross-hatching) projections from the superior colliculus as determined by the injection into the superficial layers of the superior colliculus shown in E and F and Fig. 9. The regions of the lateral and inferior pulvinar which receive projections from occipital cortex (areas 17, 18 and 19)are also represented (dots) (after refs. 4, 9 and 10). In caudal level D, the position of the abbreviation "PI" denotes the division between the medial and lateral loci found with ipsilateral projections. Appropriate levels of this figure are used for comparison with the location of the main focus of injection sites shown in Figs. 2-7. For this and all following figures refer to list of abbreviations.

pole of the thalamus, including the portions o f the putvinar which receive projections f r o m the occipital cortex and superior collicutus (Fig. 1A-F). The lateral pulvinar receives projections f r o m occipital cortex, but n o t the superficial layers o f the superior colliculus while the medial pulvinar receives little or no projections f r o m the occipital cortex and none f r o m the superficial layers o f the superior colliculus (Fig. 1). On the basis o f this connectional data we considered the portion o f the caudal pole o f the

pulvinar which receives input only from occipital cortex as a caudal extension of the lateral pulvinar and the portion of the caudal pole which receives neither cortical nor tectal input as a caudal extension of the medial pulvinar (Fig. 1E and F). The caudal pole of the dorsal lateral geniculate nucleus was used as a reference point in relating the positions of the various injection sites along the rostral-caudal axis throughout the pulvinar. Injections placed caudally in the pulvinar produced labeling of fibers which coursed laterally and rostrally to enter occipitotemporal cortex while injections placed rostrally in the pulvinar (i.e., near the dorsal lateral geniculate nucleus) produced labeling of fibers which coursed laterally and posteriorly to enter circumstriate cortex. In all cases the labeled fibers resulting from the injections were seen to course laterally through the pulvinar, external medullary lamina of the thalamus and reticular nucleus to enter the internal capsule en r o u t e to cortex. In addition, labeled fibers often coursed dorsal and lateral to the dorsal lateral geniculate nucleus, and sometimes through the dorsal lateral geniculate nucleus, en r o u t e to the internal capsule and cortex. In all cases the grains found in prestriate and inferotemporal cortices as a result of pulvinar injections were most dense in layer IV, and moderately dense in lower layer III and layer I (Fig. 9). It was difficult to say whether the light to moderate density of grains found below layer IV was due to a labeling of axons en r o u t e to layer IV or to a labeling of axon terminals. With the exception of those cases where the injection sites were confined to the posterior pole of the pulvinar or the caudal portion of the inferior pulvinar, grains were always found in layer I of striate cortex (area 17). This finding of extrageniculate projections to area 17 was the subject of a previous report 11 and will not be considered in any detail here. Finally, the distribution of grains within the various cortical areas was not of uniform density. That is the distribution of grains in layers IV-III and I of cortex formed moderate to dense 'patches' which were separated by areas containing a light density of grains (Fig. 2B). In this report the entire distribution and density of grains found in cortex will be presented and the discussion of patching will be the topic of a subsequent report. The following section presents selected cases which illustrate the topography of the total pattern of grains found in layers IV and III of the prestriate and inferotemporal cortices. The cortical projections are related to the 'main focus' of the injection site, i.e., the locus where the cellular uptake of tritiated amino acids was maximal (Fig. 9). C a s e 1. Fig. 2 illustrates an injection site located rostrally in the dorsal portion of the inferior pulvinar with the main focus at the level of the caudal pole of the dorsal lateral geniculate nucleus. This area of the inferior pulvinar receives overlapping projections from the cortex and tectum (compare with level A of Fig. 1). There was a slight spread of the amino acids into the ventral portion of the lateral pulvinar which receives only occipital projections. Grains were found in layer I of area 17zl. In addition, on the medial surface of the hemisphere, a moderate to dense distribution of grains was found in area 18 and in the cortex of the parieto-occipital sulcus. On the lateral surface of the hemisphere dense grains were found in area 18 which forms the dorsal portion of the lunate sulcus and the floor of the adjacent intraparietal sulcus.

Fig. 2. A: In this and subsequent figures the injection site in the pulvinar is illustrated in the bottom of the figure and the cortical distribution of grains as a result of the injection is illustrated in the top of the figure. Large circles denote a heavy density of grains of sulcal cortex; small circles represent a light to moderate density of grains in layer IV of sulcal cortex; and the large and small circles on cortical surfaces indicate the density of grains located in sulcal cortex which is buried beneath the cortical surface, e.g., in this case the lunate sulcus buried beneath dorsolateral area 17 shown on the right (see also cross-sections 1 and 2 illustrated in Fig. 2B). The density of dots reflects the density of grains in visible cortical areas on the surfaces of the hemisphere. Also in this and other cases the grains found in area 17 are not shown but are shown in the previous study”. Top: note that in this case grains were found dorsally (left) and medially (right) and extended to the border of area 17. Arrows indicate the levels of the cross-sections shown in Fig. 2B. Bottom: injection site located in the dorsal portion of PI and spilling into the ventral portion of the adjacent PL. The main focus was located at the level of the DLG (compare with level A of Fig. 1) and is within the corticorecipient and tectorecipient zones of PL and PI. B : illustrations ofcross-sections taken from cam ihustratecl in Pig. 2A. Arrows in Fig. 2A indicate levels at which cross-sections were taken. Sections illustrate further the distribution of grains in layer IV of cortex (dots). Note distribution of grains in cortex on medial surface of hemisphere as well as in buried sulcal cortex e.g., level 1 and 2. Grains presented a ‘patched’ appearance, e.g., in the posterior and anterior banks of the lunate sulcus and in the floor of the intraparietal sulcus in levels 2 and 3, and extended to the border of area 17 (dashed lines).

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Fig. 3. Top- cortical distribution of grains as a result of injection illustrated in bottom of figure.

Note that the grains were found more laterally than in the previous case (Fig. 2A) but were also found on the medial surface of the hemisphere, and extended to the border of area 17. Bottom: crosssections illustrating injection site located slightly more caudally and more ventrally in PI than the one shown in the previous case (Fig. 2A.) The main focus is approximately 0.5 mm caudal to the caudal pole of DLG and is within the corticorecipient and tectorecipient zones of PI (compare with levels A and B of Fig. 1). Ventral to this region of dense grains a light to moderate density of grains was found in the floor and posterior bank of the superior temporal sulcus, across area 19, and in area 18 about and within the lunate sulcus. Furthermore, area 18 forming the portion of the lunate sulcus buried beneath the dorsal portion of area 17 was found to contain a moderate density of grains. The grains found in layers, III, IV and I of area 18 extended up to the border of area 17. Case 2. Fig. 3 illustrates an injection site also located in the rostral portion of the inferior pulvinar which receives occipital and tecta! projections (compare with levels A and B of Fig. 1). In contrast to case 1, the main focus extends more ventrally into the inferior pulvinar and is located approximately 0.5 mm caudal to the caudal pole of the dorsal lateral geniculate nucleus. There was no spread of amino acids into adjacent thalamic nuclei. The result of this injection was quite similar to that of the previous case but reveals that a slight difference in the loci of the injection sites effects the cortical distribution o f grains on the lateral surface of the hemisphere. While grains were found again in the cortex on the medial and dorsolateral surfaces of the hemisphere, grains were also found more ventrolaterally extending to upper TEO, i.e., in area 18 about and within the tip of the lunate sulcus, and in the adjacent area 19 and floor and posterior bank of the superior temporal sulcus. Again, the grains in layers, III, IV and I of area 18 extended to the border of area 17 and grains were found in layer I of area 17 (see ref. 11). It is important to point out at this time that the distribution of grains in cases 1 and 2 follows the vertical meridian of the lower visual quadrant along the border of areas 17 and 18, with the grains in case 2 extending to near the horizontal meridian,

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Fig. 4. Top: cortical distribution of grains as a result of injection illustrated in bottom of figure. Note that grains were found more ventrolaterally than in the previous two cases (Figs. 2 and 3), i.e., within the inferior occipital sulcus and extending to the middle temporal sulcus (which is often seen as a branch of the occipitotemporal sulcus) (right) and to near the occipitotemporal sulcus on the ventral surface of the hemisphere (left). Bottom: cross-sections illustrating injection site located more caudally and ventrally in PI than in the previous two cases (Figs. 2 and 3). The main focus (Fig. 9) of the injection site was located approximately 1.6 mm caudal to the caudal pole of the dorsal lateral geniculate nucleus in the caudal portion of PI which receives overlapping projections from the superior colliculus and occipital cortex (compare with levels B-D of Fig. l).

i.e., the junction of the ventral tip of the lunate sulcus and the inferior occipital sulCUSg3,SS.

Case 3. Fig. 4 illustrates a more caudal injection site located ventrally and medially within the inferior pulvinar and confined to the region where the tectal and occipital inputs do not completely overlap (compare with levels B-D of Fig. 1). The main focus in this case is located approximately 1.6 mm caudal to the caudal pole of the dorsal lateral geniculate nucleus, and is located more ventrally within the inferior pulvinar than the main foci of the previous two cases. Again, there was no spread of amino acids into adjacent thalamic nuclei. In contrast to the previous two cases, the grains in case 3 were found more rostrally in the cortex of the lateral and ventral surfaces of the hemisphere, The heaviest distribution of grains was found in area 18 of the inferior occipital sulcus starting at its dorsal tip, in the lower portion of area TEO and extending ventrally close to the occipitotemporal sulcus. A moderate amount of grains was also found in the floor and posterior bank of the mid-portion of the superior temporal sulcus and the floor and banks of the posterior middle temporal sulcus, A caudal portion of area 21 on the cortical surface contained only a light amount of grains. In contrast to this distribution of grains confined to the ventrolateral prestriate cortex (Fig. 4), more rostral injections in the corticorecipient and tectorecipient zones of the inferior pulvinar resulted in grains confined to dorsolateral prestriate cortex on the preoccipital gyrus (Figs. 2 and 3). The distribution of grains in layers III, IV andI of area 18 in this case (3) extended to near the striate border and follows the vertical meridian of the upper visual quadrant along the border of areas 17 and 18, with the

11

Fig. 5. Top: cortical distribution of grains as result of injection illustrated in bottom of figure. Note that the grains were found dorsolaterally and ventrolaterally in cortex and overlap the cortical projection field of the previous cases (Figs. 2-4). No grains were found in the cortex on the medial surface of the hemisphere. Bottom: cross-sections illustrating injection site located in dorsal PI and ventral PL at about same caudal level as the case illustrated in Fig. 4. The main focus is located in the corticorecipient zones of the PI and PL (compare with levels B-D of Fig. 1). grains in layer IV extending to just beneath the representation of the horizontal meridian at the dorsal tip of the inferior occipital sulcus23, 5s. Case 4. Fig. 5 illustrates an injection site located in the dorsolateral portion of the inferior pulvinar with the main focus at approximately the same rostral-caudal level as that of case 3. A small amount of the injected amino acids also spread into the brachium of the superior colliculus and the ventral portion of the lateral pulvinar. These regions of the inferior pulvinar and lateral pulvinar receive projections from occipital cortex (compare with levels of B-D, Fig. 1). As in case 3, but in contrast to cases 1 and 2, no grains were found in cortical areas on the medial surface of the hemisphere. In addition, grains were located in the same cortical region as in case 3, but in case 4 the grains were less dense. This light density of grains was found in the cortex forming the posterior middle temporal sulcus, rostral portion of the inferior occipital sulcus, caudal portion of the middle temporal sulcus and in area TEO, and caudal portions of areas 20 and 21. The cortical grains were also found more widely distributed than in case 3. The densest concentration of grains was found throughout area 18 of the entire lunate sulcus, the lower region of the preoccipital gyrus (area 19), and the floor and posterior bank of the upper portion of the superior temporal sulcus. The grains found in layers, III, IV and I of area 18 extended to the border of area 17 and grains were also found in layer I of striate cortex 11. The distribution of cortical

12

Fig. 6. Top: cortical distribution of grains as a result of injection illustrated in bottom right of figure. Note that the distribution of grains is more rostral in this case than in any of the previous cases (Figs. 2-5) and extends to the occipitotemporal sulcus and the caudal tip of the anterior middle temporal sulcus in areas 20 and 21 (area TE). Bottom: cross-sections illustrating injection site located more caudally than the previous 4 cases. The main focus is located 2.8 mm caudal to the caudal pole of the dorsal lateral geniculate nucleus within the ventral cotticorecipient zone o f the caudal pole i,e., caudal PL (compare with levels D and E of Fig. 1). There was a slight spread of amino acids rostrally which overlapped the caudal extent of the injection shown in case 4 (Fig. 5). grains in case 4 extends along the vertical meridian of both the lower and upper quadrants at the 17-18 border 23,5s. These cases involving injections into the tectorecipient and corticorecipient zones of the pulvinar illustrate several points. First, in comparing cases 1 and 2, and cases 3 and 4 it appears that the dorsal portion o f the inferior pulvinar and the ventral portion of the lateral pulvinar have extensive overlapping cortical projections to the lunate sulcus, preoccipital gyrus, inferior occipital sulcus, and posterior bank and floor of the superior temporal sulcus. In fact, the density of grains in these regions was as great or greater in case 4 than in any other case in which an equal volume and concentration of amino acids was injected in the inferior pulvinar alone (compare case 2 with case 4). Secondly, grains are found ventrolaterally in cortex when the injection site is located caudally or ventrally in the inferior pulvinar and dorsolaterally and medially in cortex when the injection site is located rostratly or dorsally in the pulvinar. Such an organization in the topography of the projections of the inferior pulvinar would be in agreement with the topographical organization of the visual hemifield 8,1°,17,2~,5s and this topographical organization will be expanded upon in the Discussion. Case 5. Fig. 6 illustrates a case where the main focus of the injection site was located approximately 2.8 m m caudal to the caudal pole of the dorsal lateral geniculate nucleus. The main focus was found in the ventral and lateral portion of the caudal pole with some spread of amino acids rostrally into the ventral portion of the lateral pulvinar. This region of the caudal pulvinar recieves projections only from occipital cortex (compare with levels D and E in Fig. 1). At the rostral level of this injection site there was overlap with the caudal portion of the injection site in case 4 (compare Figs. 5 and 6). This rostral spread of the injection in case 5 may account for the light amount

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Fig. 7. Top: cortical distribution of grains as a result of injection illustrated in bottom of figure. Note that the distribution of grains is more rostral than any of the previous cases and is confined to area 20 about the occipitotemporal sulcus and extends to the rostral tip of the anterior middle temporal sulcus. Bottom: cross-sections (1 and 2) illustrating the most caudal injection site of this study. The main focus is located 3.0 mm caudal to the caudal pole of the DLG within the dorsal portion of the corticorecipient zone of the caudal pole, i.e., caudal PL (compare with level F of Fig. 1).

of grains found in the caudal part of the cortical projection field, i.e., area TEO and the cortex about the lower lunate sulcus. In case 5, grains were seen more rostrally in cortex than in any of the previous cases. The lightest density of grains was found in area 18 forming the anterior bank of the lower lunate sulcus, adjacent area 19 and the midportion of the posterior bank and floor of the superior temporal sulcus. A light to moderate density of grains was found in the inferior bank of the anterior portion of the inferior occipital sulcus, in the floor and banks of the caudal portion of the posterior middle temporal sulcus and caudal two-thirds of the occipitotemporal sulcus. On the lateral cortical surface, a moderate density of grains was found in area TE (areas 20 and 21). In case 5 the grains in layers, III, IV and I of area 18 did not extend to the border of area 17 and no grains were seen in any of the layers of area 17. Case 6. Fig. 7 illustrates our most posterior injection site in the pulvinar. The main focus is located in the dorsal and lateral portion of the caudal pole of the pulvinar approximately 3.0 m m posterior to the caudal pole of the dorsal lateral geniculate nucleus. This portion of the caudal pole receives only occipital input (compare with level F of Fig. 1). The cortical grains resulting from this injection were found most rostroventrally in the temporal lobe than with any of our other cases. A moderate to heavy density of grains was found in the floor and banks of the anterior portion of the occipitotemporal sulcus and medially and laterally within area 20 on the cortical surface. The grains in area 20 extended to the anterior limit of the anterior middle temporal sulcus, and no grains were seen in any other cortical area. Thus, cases 5 and 6 strongly suggest that the dorsolateral portion of the posterior pole of the pulvinar projects ventrorostrally while the ventrolateral portion of the caudal pole projects dorsocaudally to area TE.

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upper / " ~ C a u d a l quadrant Fig. 8. Schematic diagram of the topographical projections of the inferior pulvinar as related to the representation of the visual hemifield and of the topographical projections of lateral pulvinar proper and its extension into the posterior pole, based on the results of the present study. A: dashed line represents the cortical projection field in prestriate and inferotemporal cortices of these areas of the putvinar and an outfolding of the medial and ventrolateral surfaces of the cortex. The upper right portion of the dashed line represents the rostral inferior and lateral pulvinar adjacent to the DLG and an outfolding of the medial cortex extending to the parieto-occipital sulcus while the lower left portion of the dashed line represents the caudal pole of the pulvinar and an outfolding of the ventral cortex extending to the occipitotemporal sulcus. The heavy portion of the dashed line also represents the border between areas 17 and 18 and the vertical meridian (VM) which is shown again along the borders of the inferior pulvinar in B. The vertical meridian is intersected by the horizontal meridian (HM) at the center of the visual field (0 °) and divides the representation of the visual hemifield in the inferior pulvinar and cortex into upper and lower quadrants (after refs. 3, 10, 17, 23 and 58). In this scheme, prestriate cortex would contain a representation of the visual hemifield projected from the inferior pulvinar shown in B. The organization of the visual hemifield in the inferior pulvinar is taken after data reported previously3,10,17 (see text). Each number in the subdivisions of the pulvinar represents an injection site and the distribution of the numbers in the pulvinar indicates the spread of the injection. B : transverse sections passing through the pulvinar from the caudal pole of the DLG to the caudal pole of the pulvinar. The bottom of the figure (C) shows a horizontal section passing through the inferior pulvinar with tic marks to indicate the level from which the transverse sections in B were taken. By comparing the transverse and horizontal sections it is possible to see how the dorsal-ventral (as indicated generally by the arrow) and rostral-caudal projection axes interrelate (see text). For example, injection l is located dorsally and rostraUy near the more peripheral representation of the vertical meridian of the lower quadrant and the respective cortical projection zone is in dorsomedial prestriate cortex along this portion of the representation of the hemifield. Injection 2 is located in the lower quadrant near the horizontal meridian rostroventrally and also caudodorsally. The respective projection zone from

15 DISCUSSION The data of the present study show that there are topographical projections from subdivisions of the pulvinar to layer IV, lower layer III and layer I of prestriate and inferotemporal cortices. These topographical projections can be considered in two ways. First, the topography of the pulvinocortical projections can be related to the representation of the visual hemifield. Secondly, the topography of the pulvinocortical projections can be related to the separate and overlapping corticorecipient and tectorecipient zones of the pulvinar.

Visual hemifield The topography of the cortical projections of the pulvinar based on the present results is summarized in Fig. 8. At the level of the dorsal lateral geniculate nucleus, the rostral portion of the inferior pulvinar projects to medial and dorsolateral prestriate cortex. The caudal portion of the inferior pulvinar, which extends to the levels of the caudal pole of the medial geniculate nucleus and the junction of the pretectum and rectum, projects to ventrolateral prestriate cortex. Moreover, the projections of the caudal portion of the inferior pulvinar extend as far rostrally as the posterior middle temporal sulcus. The dorsal portion of the inferior pulvinar also projects to dorsolateral prestriate cortex, while the central and ventral portions also project to ventrolateral prestriate cortex. This apparently complex projection pattern can best be understood when it is related to the topographical arrangement of the visual hemifield in the inferior pulvinar and cortex. To our knowledge no extensive physiological study exists in which the organization of the visual hemifield in the macaque inferior pulvinar has been detailed. However, anatomical evidence10,17 has been presented which provides an idea of the basic framework of the representation of the visual hemifield in macaque inferior pulvinar. This anatomical evidence is based on the projections of the superior colliculus 10 and striate cortex 17 to the macaque inferior pulvinar and suggests that the representation of the visual hemifield in the macaque inferior pulvinar is similar to that detailed by single unit studies in the owl monkey inferior pulvinar a. With the knowledge of the anatomical data in the macaque inferior pulvinar and assuming that the representation

injection 2 is found along the more central representation of the vertical meridian of the lower quadrant and reaches to the horizontal meridian. Injection 3 is located centrally and caudally in the upper quadrant just below the horizontal meridian and the respective cortical projection zone is found ventrally in prestriate cortex beneath the intersection of the vertical and horizontal meridians. Injection 4 is found most ventrally and caudally and the corresponding projection zone is found ventrolaterally away from the horizontal meridian and along the peripheral portion of the vertical meridian of the upperquadrant. Injections 5-7 indicate that the projection field of the ventral portion of the lateral pulvinar overlaps, at each level, with that of the inferior pulvinar. Injections 8 and 9 show that the corticorecipient zone of the posterior pole (PL) projects to inferotemporal cortex such that the dorsal portion projects to area 20 rostroventrally and the ventral portion to areas 21 and 20 dorsocaudally (indicated by arrow). Also indicated are the retinal and occipital projections to DLG, the tectal and occipital projections to PI and the occipital projections to PL and its extension into the caudal pole, i.e., lemniscal thalamocortical and cortico-thalamoeortical organizations.

16

Fig. 9. Photomicrographs of cases illustrated in Figs. 1 and 4. Shown are grains seen in PI (B, approximately ~ 160) as a result of injection into superficial layers of superior colliculus (A, approximately 14.8); and in layer IV of cortex within IO (D, darkfield, approximately • 300) as a result of large injection into PI (C, approximately 4.8).Toluidine blue stain. of the visual hemifield in the macaque monkey inferior pulvinar is similar to that of the owl monkey inferior pulvinar, then a plausible explanation of the results on the topographical organization of pulvinocortical projections in the present study is possible. In the owl monkey the horizontal meridian divides the inferior pulvinar into a rostromedial portion which contains the representation of the lower visual quadrant and a caudolateral portion which contains the representation of the upper visual quadrant 3 (Fig. 8). The representation is such that in the rostral transverse plane, at the level of the dorsal lateral geniculate nucleus, the lower visual quadrant is located dorsomedially and occupies the majority of the nucleus. At this level the horizontal meridian is found laterally and somewhat ventrally with the upper visual quadrant found below. More caudally the horizontal meridian is found dorsomedially in the nucleus and the reverse becomes true, i.e., the ventrolateral representation of the upper visual quadrant occupies the majority of the nucleus. Our previous (Fig. 2, ref. 10) and present results concerning the projections of the superior cotliculus to the inferior pulvinar as well as the results of others iv on the projections of striate cortex to the inferior pulvinar indicate the same position of the horizontal meridian in the macaque monkey. Also in the macaque monkey other physiological studies 2a,Sa have shown that the border of areas 17 and 18 which follows the curvature of the parieto-

17 occipital, lunate and inferior occipital sulci represents the vertical meridian. Further, the horizontal meridian, which intersects the vertical meridian, extends posteriorly from near the junction of the lunate and inferior occipital sulci such that the lower visual quadrant is located dorsolaterally and medially in cortex and the upper visual quadrant is located laterally and ventrally in cortex (Fig. 8). The results of the present study can be related to these physiological and anatomical results in the owl and rhesus monkeys. For example, injections placed dorsally in the inferior pulvinar, at the level of the dorsal lateral geniculate nucleus, would be located in the representation of the lower visual quadrant (Fig. 8). As would be expected the cortical projection field is found about and within the parieto-occipital and dorsolateral lunate sulci and adjacent prestriate cortex on the medial and dorsolateral surfaces of the hemisphere (Figs. 2 and 8). More ventral injections at this rostral-caudal level extend the cortical projection field ventrolaterally towards the tip of the lunate sulcus, i.e., towards the horizontal meridian (Figs. 3 and 8). A more caudal and centrally located injection would cross the horizontal meridian in the inferior pulvinar and be located within the representation of the upper visual quadrant (Figs. 4 and 8). As would be expected the cortical projection field is found below the ventral tip of the lunate sulcus, i.e., beneath the representation of the horizontal meridian, and in the cortex about and within the inferior occipital sulcus and the adjacent prestriate cortices on the ventrolateral surfaces of the hemisphere (Figs. 4 and 8). These results would further be in agreement with physiological studies supporting the idea that ventral prestriate cortex (TEO) surrounding the intersection of the lunate sulcus and inferior occipital sulcus is primarily concerned with central vision33. It would also be valuable to have an idea of the organization of the visual hemifield in the ventral portion of the lateral pulvinar since our results show that at each rostral-caudal level the lateral pulvinar located above the inferior pulvinar has cortical projections which overlap those of the adjacent inferior pulvinar (Fig. 8). It could be suggested that since the vertical meridian is represented in the dorsal portion of the inferior pulvinara, it would also be represented along the adjacent border of the lateral pulvinar. In general these anterograde fndings on the rostral-caudal projections of the inferior pulvinar are in agreement with previous retrograde findingsla,21,2s,ag. However, our dorsal-ventral projection axis for the inferior pulvinar is more vertical than the one reported by Chow for the lateral and inferior pulvinaris. We attribute this discrepancy to Chow's consideration of the inferior pulvinar as only one point along a dorsal-ventral continuum for the entire pulvinar complex (Fig. 11, ref. 18). The present results support Chow's conclusion for the organization of pulvinar projections in simians. Specifically, our results are in agreement with Stoffels' principle of lamellation 56 which states that adjacent points or nuclei in the thalamus are projected to adjacent points or areas on the cortex. In addition, we would specify 3 correlates to this basic principle in regards to the organization of the projections of the pulvinar and adjacent dorsal lateral geniculate nucleus in the visual system of the macaque monkey. First, within a given nucleus of the pulvinar one locus projects to more than one adjacent cortical area. For example, small subdivisions within the inferior pulvinar project to cortical areas 17 (ref. ll), 18 and 19. Secondly, the pulvinar and adjacent

18 nuclei project to one cortical area but not necessarily the same layers. For example, the dorsal lateral geniculate nucleus projects to layer IV of area 17 (refs. 38 and 62) and our previous studies 1~ have shown that portions of the lateral and inferior pulvinar adjacent to the dorsal lateral geniculate nucleus project to layer I of area 17. Third, the present data also suggest that adjacent nuclei within the pulvinar complex project to the same cortical areas and layers. For example, the dorsal portion of the inferior pulvinar and the ventral portion of the lateral pulvinar project to layers, l l l, IV and I of cortical areas 18 and 19. A similar organization has already been described for the projections of the dorsal lateral geniculate nucleus and adjacent lateral group nuclei in the visual system of the opposumL These types of overlapping projections to several cortical areas would fit into the classic notions of intrinsic, association nuclei and sustaining projections 52 as will be discussed below. Finally, since different parts of the inferior pulvinar represent specific subdivisions of the visual hemifield and each of these parts has sustaining projections to more than one cytoarchitectural area, i.e., 17, 18 and 19, it can be suggested that there is more than one representation of the visual hemifield in the medial, dorsolateral and ventrolateral prestriate cortex of the macaque monkey. In fact, physiological studies1, 2 have demonstrated multiple representations of the visual hemifield in owl monkey prestriate cortex. Corticorecipient and tectorecipient zones The topography of the pulvinar projection to cortex can also be related to the portions which receive projection from the superior colliculus and occipital cortex. The portions of the inferior, pulvinar, lateral pulvinar and caudal pole of the pulvinar which receive projections from areas 17, 18 and 19 (including TEO) as well as the portion of the inferior pulvinar which receives tectal projections were shown in Fig. 1. All injections in the corticorecipient and tectorecipient portions of the inferior pulvinar and the corticorecipient portion of the ventral lateral pulvinar revealed projections to areas 17, 18 and 19 (including TEO) in a fashion in agreement with the topography reported above. In contrast to the inferior pulvinar and rostral lateral pulvinar the corticorecipient portion of the caudal pole (which can be considered as a caudal extension of the lateral pulvinar) projects to inferotemporal cortex beyond the posterior middle temporal suclus, i.e., area TE of Von Bonin and Bailey12 or areas 20 and 21 of Brodmann 15. The most caudal part of this portion of the caudal pole projects rostrally in TE, while the more rostral part of this portion of the pole projects caudally in TE (Fig. 8). In addition, the dorsal region of this portion of the caudal pole projects ventrally and the ventral region projects dorsally within area TE (Fig. 8). While our data on the rostral-caudal projections of this portion of the caudal pole are in agreement with previous retrograde studies 21,a9, to our knowledge no map on the dorsalventral projections of the caudal pole has yet been reported. The portion of the caudal pole which does not receive projections from occipital cortex may be a caudal extension of the rostral medial pulvinar and we have shown previously x4 that the rostral medial pulvinar and this portion of the caudal pole project to frontal cortex and to the cortex of the lateral fissure, but not to occipital and inferotemporal cortices. Thus, it seems clear that occipital and inferotemporal cortical areas 17, 18, 19, 20 and 21, in-

19 cluding area TEO, are associated by means of the portions of the pulvinar which receive projections from occipital cortex and these projections overlap with the corticocortical projections demonstrated in previous anterograde studiess,22,4°,41,65,66. That is, the pulvinar projections going to areas 18 and 19, including TEO, overlap with those from striate cortex and the pulvinar projections going to areas 20 and 21 overlap with those from prestriate cortex. Thus, occipital and inferotemporal cortices are connected by corticocortical and cortico-thalamocortical routes (Fig. 8). However, it is the posterior occipital areas, including TEO, which receive projections from the inferior pulvinar and thus are also influenced by direct input from the superior colliculus. On the other hand, cortical areas 20 and 21 or TE lying rostral to the posterior middle temporal sulcus do not receive projections from the inferior pulvinar and thus are not directly influenced by the superior colliculus. Thus, the present findings indicate that prestriate occipital cortex including area TEO is affected by lemniscal line input from the retina via the superior colliculus-inferior pulvinar route similar to the way in which striate cortex is influenced by the retinogeniculate routeST,as,6a. On the other hand area TE (areas 20 and 21) is not affected by any known lemniscal input, but only by the corticocortical and cortico-thalamocortical types of input which are also affecting the occipital cortex. These connectional differences between area TE and occipital cortex may be related to behavioral studies which have shown functional differences between area TE and the occipital cortex including area TEO21,26,ag,61. Area TE seems to be most concerned with the acquisition of different visual discrimination tasks presented 'concurrently'Z~,26,ag,6~ while prestriate area TEO seems to be important for the retention and acquisition of a single pattern discrimination task. Prestriate cortex proper may not play as crucial a role in visual discrimination but may be more important for visuospatial abilities while striate cortex has been reported to be important for visual identificationS4, 62. It appears, then, that more 'simple' visual abilities such as visual identification, visuomotor ability and single discrimination ability may be related to cortex dependent upon lemniscal line input from the dorsal lateral geniculate nucleus and the superior colliculus-inferior pulvinar route. Cortex involved with more complex visual abilities such as multiple or 'concurrent' discrimination may no longer rely on any direct lemniscal input but only on 'higher order' corticocortical and cortico-thalamocortical associations. In fact, a recent physiological study51 has shown that bilateral removal of occipital cortex (area 17) abolishes visual responses in area TE. Although the authors attributed these findings to interruption of corticocortical connections these findings could also be considered in relation to the interruption of cortico-thalamocorticai connections as well.

Comparison with other species Differences between the organization of Old World monkey and New World monkey visual systems have been noted before. Previous studies10,a5,55 in the macaque and squirrel monkey have shown that the projections from the superior colliculus to the thalamus and the connections between striate and prestriate cortices differ in extent and organization. It was postulated10 that these inter-species differences in

20 visual cortical and tectothalamic systems may also reflect differences in thalamocortical systems. The results of the present study indicate that this may indeed be the case since a recent retrograde study 59 using the enzyme horseradish peroxidase, has shown that the inferior and lateral pulvinar project to the superior temporal gyrus in the squirrel monkey. In contrast, the anterograde results of the present study in the macaque monkey never revealed any evidence for projections from the inferior and lateral pulvinar to any layers of the superior temporal gyrus (area 22). Regardless of survival time, grains were always seen within occipital and inferotemporal cortices and did not extend anteriorly beyond the floor of the superior temporal sulcus. Other studies using retrograde transport of horseradish peroxidase in the owl monkey 43 have shown that some of the cells of the inferior pulvinar project to the physiologically and anatomically defined visual area MT located in a small area of the cortex found posterior to and within the superior temporal sulcus. These results were related to the existence of a second lemniscal line system, in addition to the geniculostriate pathway, which projects to a cortical area located away from striate cortex. We were unable to demonstrate any such discrete cortical target of the inferior pulvinar in the macaque monkey. Rather, the present anterograde results in the macaque monkey indicate that each locus of the inferior pulvinar projects to more than one cytoarchitecturally defined cortical area and that if area MT does exist in the macaque monkey 67 it is not the sole target of the inferior pulvinar. An interesting variation in the organization of the cortical projections of the pulvinar amongst different species emerges when one compares the macaque monkey and a prosimian, the bushbaby. In the bushbaby z9 the caudal portion of the pulvinar receives tectal projections and projects, in turn, to temporal area MT, while the rostral portion of the pulvinar receives only cortical projections and projects, in turn, to area 18 adjacent to area 17. The present results show that the reverse is true for the macaque monkey. In the macaque monkey, the inferior pulvinar receives tectal projections and projects, in turn, to area 18 next to area 17 while the caudal pole receives only cortical projections and projects, in turn, to temporal cortex. Another distinguishing feature of the macaque pulvinar is that the lateral pulvinar receives cortical but not tectal projections and has projections which overlap with those of the inferior putvinar. These results would suggest that the functional organization of the pulvinocortical systems in simians and prosimians is different and that the basic parallel between the macaque monkey and the bushbaby is that the rostral portions of the pulvinar project caudally and the caudal portions of the pulvinar project rostrally regardless of which subdivision is receiving certain types of input. Moreover, in the macaque monkey the cortical projection field of the inferior pulvinar which includes area 18 adjacent to the cortical target(s) of the dorsal lateral geniculate nucleus is similar to that found in the tree shrew 36, squirrel 50, cat 30-32,47,53, and opossum 5,7. The present results on the ipsilateral projections of the superficial layers of the superior colliculus confirm the findings of our earlier degeneration study 1°. However, we are left with some results which are difficult to fit into the pattern of topographical projections of the pulvinar and the dorsal lateral geniculate nucleus to cortex. First, what is the underlying functional significance of the ipsilateral projections of the

21 superior colliculus to the m a g n o c e l l u l a r layers o f the dorsal lateral geniculate nucleus and, second, w h a t is the role o f the bilateral projections o f the superior colliculus to the c a u d a l p o r t i o n o f the inferior p u l v i n a r in the f u n c t i o n o f the t e c t o p u l v i n a r extrastriate visual system? It c o u ld be t h a t these pathways are related to the ex t r em e periph er y o f the visual field a n d even to the m o n o c u l a r crescents, since a recent physiological study 44 has s h o w n that a m a g n o c e l l u l a r layer o f the dorsal lateral geniculate nucleus is c o n c e r n e d with the m o n o c u l a r crescent an d since the c a u d a l pole o f the inferior p u l v i n a r contains only a r e p r e s e n t a t i o n o f the peripheral p o r t i o n o f the visual hemifieldL LIST OF ABBREVIATIONS

Cortex O = orbital cortex Cortical salci A = arcuate sulcus AMT = anterior middle temporal sulcus C - central sulcus Ca = calcarine sulcus EC = ectocalcarine sulcus IO = inferior occipital sulcus IP -- intraparietal sulcus L ~ lunate sulcus La = lateral fissure MT = middle temporal sulcus OT = occipitotemporal sulcus PMT = posterior middle temporal sulcus PO = parieto-occipital sulcus R = rhinal sulcus ST = superior temporal sulcus SP ~ subparietal sulcus

Subcortical nuclei and tracts B = brachium of the superior colliculus CC = corpus callosum CG = central gray DLG = dorsal lateral geniculate nucleus H = habenular nucleus IC = internal capsule Li = limitans nucleus LP = lateral posterior nucleus MD = dorsomedial nucleus MG medial geniculate nucleus P pretectum PI = inferior pulvinar PL = lateral pulvinar PM = medial pulvinar PO = oral pulvinar R reticular nucleus SC = superior colliculus Sg = suprageniculate nucleus SO = stratum opticum VPL = ventral posterior lateral nucleus

ACKNOWLEDGEMENTS This w o r k was s u p p o r t e d by N S F G r a n t B M S 75-07349. M. R e z a k was s u p p o r t ed by N I M H T r a i n i n g G r a n t 8396. T h e technical assistance o f N. D u B o s e in the p r e p a r a t i o n o f the histological m a t e r i a l is gratefully acknowledged.

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