The Ascending Projections of the Superior Colliculus in the Rhesus Monkey (Macaca mulatta) L. A. BENEVENTO

AND JAMES H. FALLON College of M e d i c i n e , U n i v e r s i t y of lllinois Medical C e n t e r , C h i c a g o , lllznois 60680

ABSTRACT We studied and compared the ipsilateral efferents of the superficial and deep layers of the superior colliculus of the rhesus monkey. Using a stereotaxic method, microelectrodes were inserted through the contralateral hemisphere in order to make electrolytic lesions of the superior colliculus. Large lesions involved all layers of the superior colliculus, while smaller lesions involved either the superficial or the deep layers of the superior colliculus. Following various survival times, the brains were prepared with the Fink-Heimer technique ('67). Following lesions of the superficial layers of the superior colliculus, definite degenerated axonal endings were found in the dorsal and ventral lateral geniculate nuclei, inferior pulvinar, centrointermediate nucleus, magnocellular dorsomedial nucleus, anterior pretectal nucleus and pretectal region. Sparse degenerated axonal endings were found in the limitans nucleus, lateral posterior nucleus and some intralaminar nuclei following lesions of the superficial layers in the rostral portion of the superior colliculus. Following lesions of the deep layers of the superior colliculus, degenerated axonal endings were found in the central gray, magnocellular medial geniculate nucleus, suprageniculate nucleus, limitans nucleus, lateral posterior nucleus, medial and oral pulvinar, nucleus of the accessory optic tract, zona incerta, subdivisions of the ventral lateral and ventral posterior lateral nuclei, ventral posterior inferior nucleus, densocellular and multiform dorsomedial nuclei, all intralaminar nuclei, inferior colliculus, parabigeminal nucleus, olivary nucleus, reunions nucleus, Forel's Field H and a n undefined midbrain nucleus. In general the projections were topographically organized in that the caudal portion of the superior colliculus projected to the rostral portions of thalamic nuclei and the rostral portion of the superior colliculus projected to the caudal portions of thalamic nuclei. All the degeneration patterns seen after lesions of the superficial and deep layers were accounted for by large lesions which involved all layers of the superior colliculus. It is concluded that the superficial and deep layers of the rhesus monkey superior colliculus have different ascending projections. The findings are related to the organization of visual and multimodal thalamocortical systems in primates and other mammals.

Some projections of the superior colliculus of the rhesus monkey were described in a brief account by Myers ('63) who made total ablations of the superior colliculus and used the Nauta technique. In that study Myers described projections to the intralaminar nuclei, dorsomedial nucleus, lateral and posterior nuclear groups, dorsal and ventral lateral geniculate nuclei, suprageniculate nucleus as well as some other thalamic and brainstem nuclei. Mathers ('71) provided a detailed account of the projections of the superior colliculus to the posterior thalamus of the squirrel monkey using both the Fink-Heimer technique and J. COMP. NEUR.,160. 339-362

electron microscope examinations. He found projections to the posterior nucleus and the ventral-medial two thirds of the inferior pulvinar, but no evidence of projections to other parts of the posterior thalamus, the dorsal lateral geniculate nucleus or other subdivisions of the pulvinar. It seems these reports indicate that a difference may exist between the rhesus monkey and the squirrel monkey in the number of ascending projections of the superior colliculus. The ascending projections of the superior colliculus have also been detailed in the tree shrew (Abplanalp, '72; Casagrande et 339

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al., '72; Harting et al., '72; Harting et al., '73; Harting et al., '73), cat (Altman and Carpenter, '61; Graybiel and Nauta, '71; Graybiel, '72), bushbaby (Harting et al., '72), hedgehog (Harting et al., '72; Harting et al., '73), and opossum (Martin, '69; Benevento and Ebner, '70; Rafols and Matzke, '70) with the use of Nauta stains. In the tree shrew and bushbaby, the superior colliculus was found to project to the intralaminar nuclei, pulvinar, posterior nuclear group, and the dorsal and ventral lateral geniculate nuclei. In the cat, while the existence of tectal projections to the intralaminar nuclei and the dorsal lateral geniculate nucleus remain uncertain (Altman and Carpenter, '61; Graybiel, '72a, 74), it has been demonstrated that there are tectal projections to the posterior nuclear group and perhaps the pulvinar. Thus, it appears that the projections of the superior colliculus to a number of thalamic nuclear areas is characteristic of the tree shrew, cat, bushbaby and rhesus monkey, but not the squirrel monkey. However, a closer comparison between the ascending tectal projections of the squirrel monkey, rhesus monkey and other mammals is hindered because a detailed analysis of tectal projections is not yet available in the rhesus monkey. Thus, one aim of this study is to attempt to detail the ascending projections of the superior colliculus of the rhesus monkey using results gathered with large tectal lesions and the Fink-Heimer technique ('67). Other recent anatomical studies in the tree shrew (Abplanalp, '71; Harting et al., '72), bushbaby (Harting et al., '72); and cat (Graybiel, '72) have shown that there are differences between the projection sites of the superficial layers and the deep layers of the superior colliculus. In the tree shrew the superficial layers project to the pulvinar, dorsal lateral geniculate nucleus (Harting et al., '72; Harting et al., '73) and suprageniculate nucleus (Abplanalp, '71), while the deep layers project to the intralaminar nuclei and posterior nuclear group (Harting et al., '72; Harting et al., '73). In the bushbaby, the superficial layers of the superior colliculus project primarily to the pulvinar while the deep layers project to the intralaminar nuclei and posterior nuclear group (Harting et al., '72). In the cat, yet another difference between the pro-

jection sites of the superficial and deep layers appears (Graybiel, '72). In this animal the superficial layers seem to project to the medial portion of the lateral posterior nucleus while the deep layers project to the ventral portion of the lateral posterior nucleus. It has been proposed that the efferents of the superficial layers, which receive projections from the retina and occipital cortex are related to the thalamic nuclei of the visual system, while ascending efferents of the deep layers are related to thalamocortical association systems which are not primarily visual (Harting et al., '72; Graybiel, '72). Physiological and anatomical studies in the rhesus monkey have indicated that connectional and functional differences also exist between the afferents to the superficial and deep layers of the superior colliculus. For example, anatomical studies have shown that while the superficial and deep layers receive projections from the occipital cortex, only the superficial layers receive projections from the retina (Hendrickson et al., '70; Campos-Ortega et al., '70; Kuypers and Lawrence, '67; Lund, '72; Wilson and Toyne, '70). In addition, the deep layers receive a variety of other afferents including projections from the inferior colliculus (Moore and Goldberg, '66) and the temporal, parietal and frontal lobes (Kuypers and Lawrence, '67). Physiological studies have shown that cells in the superficial layers may respond only to visual stimuli (e.g., Cynader and Berman, '72; Schiller and Koerner, '71). Cells in the deep layers, on the other hand, may respond to visual, somatic and auditory stimuli (Cynader and Berman, '72) and respond prior to saccades, and in relation to tracking eye movements (e.g., Cynader and Berman, '72; Schiller and Koerner, '71). Since anatomical and physiological studies indicate a different organization between the superficial and deep layers of the superior colliculus of the rhesus monkey, the ascending projections of the superficial and deep layers might also be expected to be different. I t is not known if a difference exists between the efferents of the superficial and deep layers of the superior colliculus in the rhesus monkey or how these efferents would compare to those reported for the tree shrew, cat, bushbaby and squirrel monkey. For these reasons, the present study is also

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an attempt to detail the ascending projections of the superficial and deep layers of the superior colliculus in the rhesus monkey using results gathered following lesions of the superficial or deep layers. MATERIALS AND METHODS

Superior colliculus lesions. Seventeen young adult rhesus monkeys (Macaca m u Zatta) weighing 2 . 5 4 . 9 kg were used for these studies. The animals were anesthetized for surgery with pentobarbital sodium (30 mglkg, i.p.) and aseptic precautions were taken in all operations. Lesions of the superior colliculus were made stereotaxically with an insulated microelectrode (10 pm tip diameter) inserted through the contralateral hemisphere. Upon reaching the desired stereotaxic coordinates (Olszewski, '52; Snider and Lee, '62; Benevento, '75), 45 minutes were allowed for the hemisphere to retract along the electrode because dimpling of the hemisphere occurred as a result of the electrode penetration. A two milliamperes D.C. anodal current was subsequently applied for five seconds. In some cases, two penetrations and lesions were made at different stereotaxic coordinates. On the basis of three cases, the optimal stereotaxic coordinates for making lesions of the superficial layers were found to be P = 0.5, V = 6.3, L = 2.5 (mm). On the basis of three different cases, the optimal stereotaxic coordinates for making lesions of the deep layers were found to be P = 0.5, V = 5.0, L = 2.5 (mm). In the present study, we define the superficial layers of the superior colliculus of the rhesus monkey as including the stratum zonale, stratum griseum superficiale and the dorsal half of the stratum opticum. The deep layers are defined as including the ventral half of the stratum opticum, stratum griseum intermedium, stratum album intermedium, stratum griseum profundum and stratum album profundum. These definitions are based on evidence from physiological recordings in the superior colliculus of the rhesus monkey (Schiller et al., '74) which indicated that the transitional zone, which separated the superficial and deep layers, was in an area between the dorsal and ventral parts of the stratum opticum. (For example, it was found that the responses of single units dorsal to the middle part of

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the stratum opticum were not affected to any great degree by cooling or removal of the occipital cortex, while the responses of single units ventral to the middle of the stratum opticum were affected by removal or cooling of the occipital cortex.) Large superior colliculus lesions involving all layers were made in two monkeys by applying a 4 milliamperes D.C. anodal current for one minute through a larger electrode (over 300 pm tip diameter). Survival times ranging from 5 to 17 days were used in these cases. In this anterograde degeneration study, a stereotaxic approach through the opposite hemisphere was made with the microelectrode in order to avoid damage to any other structure on the side of the superior colliculus lesion. Because of this approach we will present only the degeneration data obtained in the brain on the side of the superior colliculus lesion. Control lesions. Four control lesions were made by microelectrodes guided into structures other than the superior colliculus. These lesions involved either the central gray, inferior colliculus, fornix, corpus callosum, internal capsule or pulvinar. in three other monkeys only subpial aspirations of occipital cortex (areas 17, 18, 19) were made in order to determine the route of occipital projections to the thalamus. We were interested in determining the course of cortico-thalamic fibers to see if their route(s) to the thalamus could be interrupted by lesions of the superior colliculus (fig. 4B and legend). Survival times of 10, 14 and 16 days were used for these cortical lesions. Optic enucleations were also made in two other animals to determine the course of retinal efferents to the thalamus and pretectum. Again we were interested in determining the course of this fiber system to see if retino-thalamic or retino-pretectal fibers could be interrupted by lesions of the superior colliculus. Survival times of 10 and 14 days were used for the optic enucleations. Histology and interpretation. A t the end of the survival period each animal was anesthetized with pentobarbital sodium and perfused intracardially with 0.9% saline, followed by 10% formalin. The calvarium was removed and the brains were blocked transversely in a stereotaxic plane. The brains were stored for at least

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two weeks in 10% formalin and subsequently transferred to a 30% sucrose solution made with 10% formalin. After the brains sank in the sugar solution, frozen sections were cut in the transverse plane at 30 pm and placed in compartmentalized trays containing 5% formalin. Two adjacent sections were stained at 300 pm intervals throughout the brain; one with cresyl violet and the other with Procedure 1 of the Fink-Heimer technique (‘67). Variations in parameters of the silver staining technique were used in order to obtain optimal staining of the degeneration (Benevento and Ebner, ’71). The distributions of degenerated axons and axonal endings were plotted onto tracings of the sections (Benevento and Ebner, ’71). The degenerated fibers were considered to demonstrate terminations in two ways as defined previously (Benevento and Ebner, ’71; ’71a). “Pericellular degeneration” was recorded when degenerated fibers showed frequent tortuous arrangements around, or in the vicinity of neuronal cell bodies. “Terminal degeneration” was recorded when degenerated fibers led to, but not beyond, what appeared to be degenerated end ramifications consisting of fields of small, irregular, spheroidal argyrophilic particles. Degenerated axons could be traced from the lesion to the fields of pericellular and terminal degeneration. In this paper, the term “degenerated endings” is used to mean both pericellular and terminal degeneration.

Sections adjacent to the Fink-Heimer stained sections were stained with cresyl violet and studied under the microscope. In this way the limits of nuclear areas as defined by Olszewski (’52) were identified. These nuclear outlines were then superimposed upon the drawings from the FinkHeimer sections. This was done by means of a photographic enlarger. In this way it was possible to relate the extent and position of degeneration to Nissl cytoarchitecture. Lesions and electrode tracts were reconstructed from the Nissl stained sections. Figure 1 (C) illustrates reconstructions of lesions of the superior colliculus (dorsal view). Figure 1 (A,B) illustrates how the microelectrodes were inserted into the hemisphere opposite to the superior colliculus lesions. RESULTS

Before presenting the results it is helpful to consider some problems that arose in interpreting the data. Superficial and deep lesions were made in order to try to answer the question of whether the superficial layers project to different thalamic nuclei than the deep layers. With different animals having the same survival times, the pericellular and terminal degeneration resulting from lesions of the deep layers was found in more thalamic nuclei than the pericellular and terminal degeneration resulting from lesions of the superficial layers. Thus, it can be said that there is a difference in the number of thalamic projection -

Abbrevicitio?zs BSC, brachium of the superior colliculus CG, central gray CI, centrointermediate nucleus CL, central lateral nucleus CL,, superior central lateral nucleus CM, centromedian nucleus CTT, central tegmental tract H, Forel’s field H IC, inferior colliculus Li, limitans nucleus LG, dorsal lateral geniculate nucleus LG ventral lateral geniculate nucleus LP, lateral posterior nucleus MD, dorsomedial nucleus MG,, magnocellular medial geniculate nucleus MRN, mesencephalic reticular nucleus NAOT, nucleus of the accessory optic tract NLL, nucleus of the lateral lemniscus NMA, medial annular nucleus of the aqueduct aqueduct ON, olivary nucleus ~

Pi, inferior pulvinar P, medial pulvinar Po, oral pulvinar PA, pretectal region PCN, paracentral nucleus PF, parafascicular nucleus PN, parabigeminal nucleus PNC, pontine nucleus PR, anterior pretectal nucleus R, reunions nucleus SC, superior colliculus (layers 1-7) SG, suprageniculate nucleus SO, superior olivary complex TB, nucleus of the trapezoid body VL, ventral lateral nucleus VPI, ventral posterior inferior nucleus VPL, ventral posterior lateral nucleus VPL,, caudal ventral posterior lateral nucleus X, thalamic area X Z, undefined mesencephalic nuclear region ZI, zona incerta

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C

w super icial

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tat.

@ deep

total t

Fig. 1 (A) Drawings of transverse sections illustrating how microelectrodes passed through the hemisphere opposite to the side of the lesions in the superior colliculus. Two small lesions (la,b) of the superficial layers of the superior colliculus in one rhesus monkey. Lesion l b is more rostral than lesion l a . CC, corpus callosum; Pul, pulvinar. (B)Drawings of transverse sections as in A. Small lesions (4a,b) of the deep layers of the superior colliculus in one rhesus monkey. Lesion 4b is more rostral than lesion 4a. IC, inferior colliculus; Sup. Cistern, superior cistern; I and 11, lateral ventricles. (C) Reconstruction of lesions onto dorsal view of right superior colliculus. Pulvinar would be located at upper right of each superior colliculus. Lesions were reconstructed from sections stained with cresyl violet. Tic marks in superficial, deep and total indicate transverse levels of the lesions shown in the photomicrographs of figs. 6-8. (Tic marks approximate drawings of l b and 4b above). Superficial: Three cases of small lesions (solid black) in the superficial layers of the superior colliculus. la,b account for a single case and transverse sections of these two lesions are illustrated in fig. 1A. Deep: Three cases of small lesions in the deep layers of the superior colliculus. 4a,b account for single case and transverse sections of these two lesions are illustrated in fig. 1B. Total: Two cases of large lesions (outlined) of all layers of the superior colliculus.

sites of the superficial and deep layers. It is more difficult, however, to answer the question of whether the projections of the superficial and deep layers overlap. There are two reasons which make this question difficult to answer. The first reason is that in the two cases having rostral, but not caudal lesions of the superficial layers of

the superior colliculus (fig. 1, lesions lb, 2) sparse degeneration was found in the limitans nucleus, lateral posterior nucleus and some of the intralaminar nuclei. The degeneration found in these nuclei was greater as a result of rostral or caudal lesions of the deep layers. Thus, we are not sure if these results from superficial lesions

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represent a difference in the projections of the caudal and rostral portions of the superficial layers or that ascending axons from the deep layers of the superior colliculus, en route to the thalamus, pass more superficially through rostral portions of the superior colliculus and hence were damaged by the rostrally placed superficial lesions. Secondly, while lesions of the deep layers produced degeneration in more thalamic nuclei than did a n y lesions of the superficial layers, lesions of the deep layers also produced degeneration in the same thalamic nuclei as did a n y of the lesions of the superficial layers (e.g., inferior pulvinar). Since the microelectrode had to puncture a small region in the medial portion of the superficial layers in order to make electrolytic lesions in the deep layers, this confounding of the degeneration results with deep lesions would be expected. Moreover, except for the degenerated endings seen in the intralaminar group, limitans nucleus and lateral posterior nucleus, the amount of degenerated endings found in the thalamic nuclei as a result of electrolytic lesions of the superficial layers was more dense than the amount of degenerated endings found in the same nuclei as a result of larger electrolytic lesions of the deep layers (e.g., inferior pulvinar, figs. 14, 15 and legends). Thus, it may be said that if there are projections from the deep layers to thalamic nuclei which also receive projections from the superficial layers, the projections of the deep layers are of a lesser extent. Lesions of the superficial layers. Figure 2 and plate 1 (fig. 6) demonstrate one case in which two superficial lesions were made. Both the caudal lesion (level 780) and the rostral lesion (level 740) involved the stratum zonale and stratum griseum superficiale and, in some areas, the most dorsal part of the stratum opticum. Ipsilaterally, the superior colliculus contained degenerated axons which coursed to the stratum opticum, and gave rise to pericellular degeneration within about 0.75 mm of the lesion. Degenerated axons destined for other areas followed two routes. In the first route, degenerated axons coursed via the brachium of the superior colliculus (fig. 2, levels 740420) and gave rise to moderately dense pericellular and sparse terminal degenera-

tion in the inferior pulvinar, especially in the medial sector (fig. 2, level 660). More rostrally, the degeneration in the inferior pulvinar was found in medial and dorsolateral sectors (fig. 2, level 620). Degenerated axons were also traced to the magnocellular layers of the dorsal lateral geniculate (fig. 11) and to the ventral lateral geniculate, where they gave rise to predominantly pericellular degeneration. In the second route, degenerated axons from the superficial lesion coursed in the medial pretectum (fig. 2, levels 700, 660) and gave rise to pericellular degeneration in the anterior pretectal nucleus, the pretectal region and limitans nucleus (fig. 10). En passage degenerated axons which coursed through the medial pretectum also gave rise to sparse pericellular and terminal degeneration in intralaminar nuclei, including the parafascicular, centromedian, centraolateral and paracentral nuclei. Degenerated axons not destined for intralaminar nuclei emerged from the internal medullary lamina of the thalamus to give rise to pericellular and occasional terminal degeneration in the magnocellular dorsomedial nucleus (fig. 9). These degenerated endings were seen to form a “rim” about the magnocellular dorsomedial nucleus (e.g., fig. 2B, level 559) at the midpoint of the nucleus, while at the caudal and rostral extents of the dorsomedial nucleus this “rimming” of degeneration was less evident. More rostrally, the degenerated endings were found in the centrointermediate nucleus (fig. 2, levels 510, 480). Degenerated axons also coursed dorsally and laterally out of the internal medullary lamina and gave rise to sparse pericellular and terminal degeneration in dorsal areas of the lateral posterior nucleus (fig. 2, levels 620, 559). Lesions of the deep layers. Figure 3A-C illustrates the degeneration seen following two lesions of the deep layers of one superior colliculus. The lesions were made beneath the stratum opticum in the caudal part of the superior colliculus. Figures 3 A and 7 (levels 809, 779) illustrate where the two lesions were made. The lesions extended ventrally to the stratum griseum profundum and dorsal portions of stratum album profundum. Both pericellular and terminal degeneration could be found in all layers of the superior colliculus, except

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831

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780

Fig. 2 (A) Plots of transverse sections through mesencephalon and thalamus illustrating degenerated fibers and endings after small lesions (la,b of fig. 1) of the superficial layers of the superior colliculus. Higher numbers designate more caudal levels. In this, and all other figures, abbreviations are listed above. Short black lines indicate degenerated axons, large black dots indicate pericellular degeneration and small black dots indicate terminal degeneration. Arrows ‘‘w” point to the areas of nuclei from which high power photomicrographs were taken. These photomicrographs are shown in flgs. 9-15. (B) More rostra1 levels of case shown in fig. 2 A . Higher numbers indicate more caudal levels.

stratum zonale. The degeneration seen in the thalamus was more extensive than that seen as a result of lesions confined to the superficial layers. As mentioned above, except for the intralaminar nuclei, lateral posterior nucleus and limitans nucleus, the density of degenerated axons and endings seen in the thalamic nuclei which contained degenerated endings as a result of

lesions of the superficial layers was less following lesions of the deep layers. However, the general location of the degeneration was the same after superficial and deep lesions, e.g., the magnocellular layers of the dorsal lateral geniculate nucleus (fig. 2 B , 3A-C). The degeneration seen after lesions of the deep layers of the superior colliculus

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could be traced in the brachium of the superior colliculus to an island of terminal and pericellular degeneration found in a dorsal area of the medial pulvinar that borders the lateral pulvinar. The exact position of this island of degeneration varied according to the placement of the lesion but was always situated in the dorsal aspect of the medial pulvinar at the border of the lateral pulvinar (fig. 3A, levels 718 to 658; fig. 12). Figure 3B (levels 609, 591) and figure 13 illustrate that sparse pericellular degeneration was also found in localized portions of a nuclear area which Olszewski (’52) called the oral pulvinar. This nuclear area is situated lateral to the centromedian nucleus and medial to the caudal subdivision of the ventral posterior lateral nucleus and is characterized by small cells and irregular cell density. Additional pericellular and,

to a lesser extent, terminal degeneration was found in the suprageniculate and magnocellular medial geniculate nuclei (fig. 3, levels 668-609). Degenerated endings were also seen in the olivary nucleus, nucleus of the accessory optic tract, parabigeminal nucleus, inferior colliculus, central gray and a nucleus which we were unable to define and labelled “ Z ’ (fig. 3A, level 699). Figure 3B illustrates pericellular and terminal degeneration in the oral and caudal subdivisions of the ventral lateral nucleus (figs. 3B, 3C, levels 591-453). Islands of pericellular and terminal degeneration were also seen in the ventral posterior inferior nucleus and subdivisions of the ventral posterior lateral nucleus. Pericellular and terminal degeneration was also found in the reunions nucleus, small portions of the multiform and denso-

G

Fig. 3 (A) Plots of transverse sections through mesencephalon and thalamus illustrating degenerated fibers and endings after small lesions (4a,b of fig. 1) of the deeper layers of the s u p e rior colliculus. In this figure, higher numbers designate more caudal levels. (B) More rostral levels of case shown in fig. 3A. (C) More rostral levels of case shown in figs. 3A,B.

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Figure 3

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L. A. BENEVENTO AND .JAMES H. FALLON

sc

A Fig. 4 (A) Large lesion ( 8 of fig. 1) of superior colliculus. In this figure lower numbers indicate more caudal levels. Level 291 illustrates pericellular and terminal degeneration in all cellular layers of the superior colliculus. Degenerated fibers passed ventrally from the superior colliculus to give rise to degenerated endings in the central gray, inferior colliculus and medial annular nucleus of the aqueduct. Not illustrated are all degenerated axons that coursed into the descending tectal tracts. Level 331 demonstrates the way in which some degenerated fibers passed from the lesion to the brainstem structures mentioned above. In addition, degenerated fibers passed lateral to the lateral lemniscus to give rise to degenerated endings in the parabigeminal nucleus. Level 371 illustrates additional degeneration in the undefined nucleus “Z’, nucleus of the lateral lemniscus, superior olivary complex (“to S.O.”), and a small “island’ of terminal and pericellular degeneration in the medial pulvinar. Level 411 illustrates that this “island” of degeneration in the medial pulvinar shifted dorsally and medially. This shift coincides with the cytoarchitectural boundary between the medial and lateral pulvinar as was seen in different sections. Level 411 illustrates degenerated z o n a l terminals that were seen in the nucleus of the accessory optic tract and in the dorsomedial division of the inferior pulvinar. Degenerated axons coursed into the trapezoid body (“to T.B.”). (B) Plot of further degeneration patterns following the lesion shown in fig. 4 A . Level 451 illustrates degenerated endings in the pretectum, posterior group nuclei, olivary nucleus and lateral posterior nucleus. Arrows labelled “Cortical Routes” indicate the course of occipito-thalamicfibers which entered laterally through the internal capsule. The route of these fibers was determined from separate cases of occipital lobectomies, one of which is illustrated in fig. 5A,B. These routes are indicated here for comparison with the routes of tecto-thalamic fibers. Level 491 demonstrates where degenerated endings were seen in the magnocellular dorsomedial nucleus, parfascicular nucleus, lateral portions of the oral pulvinar, magnocellular layers of the dorsal lateral geniculate nucleus and lateral pontine nucleus. Pericellular degeneration is illustrated in the ventral posterior inferior and caudal ventral posterior lateral nuclei. Level 511 illustrates the additional degeneration that was seen in the ventral lateral nucleus and in the dorsolateral and medial portions of inferior pulvinar. Level 551 indicates where degeneration was seen in some inealaminar nuclei and two separate areas of the lateral posterior nucleus. ( C ) Plot of further degeneration patterns following the lesion shown in fig. 4A. Level 591 illustrates degenerated endings in the reunions nucleus, centrointermediate nucleus, multiform dorsomedial nucleus, superior central lateral nucleus and ventral lateral geniculate nucleus. Level 611 illustrates degeneration in the lateral posterior nucleus as well as the ventral lateral nucleus. Level 631 iuuseates additional degenerated endings in the zona incerta. Level 671 illustrates degenerated endings in area X (medial portion of ventral lateral nucleus).

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349

Figure 4

cellular dorsomedial nuclei, zona incerta, Forel's fields H and HI and thalamic area X as defined by Olszewski ('52) (medial portion of ventral lateral nucleus, Akert, '64) (fig. 3 C ) . The intralaminar nuclei, the limitans nucleus and the lateral posterior nucleus, which contained degenerated endings as a result of rostral lesions of the superficial layers, also contained degenerated endings as a result of lesions of the deep layers. However, the degenerated endings found in these nuclei was somewhat more widespread in any given nucleus as a result of lesions of the deep layers. In addition, degenerated endings were found in the superior centrolateral nucleus after lesions of the deep layers (fig. 3, levels 560453). This intralaminar nucleus did not contain degeneration as a result of rostral lesions of the superficial layers. Topography. In general, lesions of the superficial or deep layers in the rostral portion of the superior colliculus produced degenerated endings in caudal areas of thalamic nuclei while lesions of the super-

ficial layers or deep layers of the caudal portion of the superior colliculus produced degeneration in rostral areas of the same thalamic nuclei. Large lesions. Large lesions of the superior colliculus were made to see if the degeneration patterns contained components not seen after lesions of the superficial or deep layers at the same survival time. One of the two lesions (fig. 8) and associated degeneration patterns are illustrated in figure 4A-C. These lesions included all layers of the superior colliculus and a large portion of the rostro-caudal extent of the superior colliculus. Neither lesion damaged the most lateral portions of the superior colliculus. The degeneration seen following large lesions was more dense than that seen after any lesions of the superficial or deep layers. However, the degeneration revealed no additional projections but simply reflected the projections that would be surmised as a result of combining the individual degeneration patterns resulting from the lesions of the superficial and deep layers (fig. 4A-C and legend).

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CA

LATERAL

MEDIAL

Fig. 5 (A) Lateral and medial surfaces of one occipital lobe lesion. Nomenclature is according to Von Bonin and Bailey ('47) and Brodmann ('09) (area 19). (B) Plots of degeneration patterns seen in the superior colliculus, nucleus of the accessory optic tract, limitans nucleus, thalamic reticular nucleus, caudate nucleus, lateral pulvinar, medial pulvinar, inferior pulvinar and suprageniculate nucleus after lesion shown in fig. 5 A . In the superior colliculus, stratum album profundum is designated by the number 7.

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Controls One extensive lesion of visual cortex involving damage to areas OC, OB and OA of von Bonin and Bailey (’47), and corresponding generally to Brodmann’s (’09) areas 17, 18 and 19 is illustrated in figure 5A. The four drawings in figure 5B illustrate some of the degeneration patterns seen after this cortical lesion and demonstrate several points. The densest terminal degeneration was found in the lateral pulvinar. A moderate amount of pericellular and terminal degeneration was found in the inferior pulvinar. The portion of the medial puIvinar which borders the lateral pulvinar contained sparse pericellular degeneration. These areas of the pulvinar (inferior and medial pulvinar) that contained degeneration after the cortical lesion overlap areas that contained degeneration after lesions of the superior colliculus (Benevento and Fallon, ’75). This was also true of the oral pulvinar (not shown). Moderate amounts of pericellular and terminal degeneration were found in the superficial layers of the superior colliculus with some terminal and pericellular degeneration in deep layers, especially at the caudal two-thirds of the superior colliculus. Figure 5B further illustrates that pericellular and terminal degeneration was also found in the caudate nucleus, nucleus of the accessory optic tract, thalamic reticular nucleus, limitans nucleus, and suprageniculate nucleus. It is concluded that the degenerated axons following lesions of the superior colliculus in eight other monkeys were probably not due to interruption of occipito-thalamic fibers because the degenerated occipitothalamic fibers following lesions such as that illustrated in figure 5 A were not found to pass near the region of the lesions of the superior colliculus, unless they were destined for the superior colliculus itself. That is, the degenerated fibers seen following occipital lesions remained lateral to the brachium of the superior colliculus (fig. 5B), whereas lesions in the superior colliculus cases were made in the medial portion of the superior colliculus (fig. 1). In addition, other occipito-thalamic axons entered the pulvinar and other thalamic nuclei from the ipsilateral internal capsule (fig. 4B, “cortical routes”) which is removed from the superior colliculus. In the present

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study, the eight experimental lesions of the superior colliculus did not involve any other brains tem structures. Degeneration seen after lesions not in volving the superior colliculus but involving either the central gray, inferior colliculus, corpus callosum, fornix or contralateral hemisphere also indicated that the degeneration following damage to these structures could not be confounded with the degeneration seen following lesions in the superior colliculus. The possibility that lesions of the superior colliculus interrupted retinal fibers, especially to the pretectum, was excluded because degenerated retinal axons resulting from two separate cases of optic enucleations did not take the same course as the degenerated tectal axons. Similar findings of retina1 efferents in the rhesus monkey have been previously reported (Hendrickson et al., ’70; Wilson and Toyne, ’70). DISCUSSION

Projections of all layers of superior colliculus The only previous study describing the projections of the superior colliculus of the rhesus monkey was a brief report by Myers (‘63) who used the Nauta technique. Myers (’63) reported that following total removal of the superior colliculus definite degeneration was found in the inferior colliculus, pretectum, parafascicular nucleus, ventral lateral geniculate nucleus and “lateral and posterior nuclear groups.” Myers also reported evidence for projections to the dorsal lateral geniculate nucleus, suprageniculate nucleus, intralaminar nuclei, densocellular and multiform parts of the dorsomedial nucleus, zona incerta and Forel’s Field H. The degeneration results of the present study confirm the findings of Myers (‘63) and, in addition, show projections to the inferior, medial and oral pulvinar, magnocellular layers of the dorsal lateral geniculate nucleus, lateral posterior nucleus, the magnocellular subdivision of the dorsomedial nucleus, the centrointermediate nucleus, reunions nucleus, nucleus of the accessory optic tract, ventral posterior inferior and ventral posterior lateral nuclei, subdivisions of the ventral lateral nucleus, parabigeminal nucleus, olivary nucleus, limitans nucleus and a nuclear area which we could not define but called “Z” (fig. 3A). It should be mentioned here that our lesions of the

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superficial and deep layers which did not lateral posterior nucleus and to some intraapproach the central gray, produced degen- laminar nuclei. However, we cannot be sure erated endings in the dorsomedial nucleus. if these latter findings represent a differThus, previous studies in the rhesus mon- ence in the projections of the rostral and key and other animals with total ablations caudal portions of the superficial layers, of the superior colliculus which report a or that other ascending axons, en route to projection to the dorsomedial nucleus were the thalamus, pass superficially through not necessarily due to damage of the cen- rostral portions of the superior colliculus tral gray. and were damaged by the rostral lesions. All projections revealed by a large lesion On the other hand, the deep layers of the of all layers of the superior colliculus can superior colliculus project to the medial be accounted for by lesions restricted to and oral pulvinar, the limitans nucleus, the superficial and deep layers of the supe- lateral posterior nucleus and 21 other nurior colliculus. clear areas, part of which are the intraProjections of th e superficial versus deep laminar nuclei. The thalamus of the rhesus monkey is layers. The fact that the superficial layers and deep layers of the superior colliculus large and well developed with more cytoexhibit different projection patterns has architectonic parcellations of thalamic been reported in various mammals. In the nuclear groups (Olszewski, '52) than is cat, Graybiel ('72) first reported that the found with the species whose collicular efsuperficial layers project to the medial divi- ferents have been studied. The numerous sion of the lateral posterior nucleus while subdivisions of the thalamic nuclear groups the deep layers project to the ventral divi- in the rhesus monkey may partially form sion of the lateral posterior nucleus. In the the basis for the many projections of the tree shrew, the superficial layers of the superior colliculus which were found. Functional considerations and interspesuperior colliculus project to the pulvinar and dorsal lateral geniculate nucleus (Ab- cies differences. The present findings sugplanalp, '71; Harting et al., '72; Harting gest that the type of information relayed in et al., '73) as well as the suprageniculate the superficial and deep layers may be dinucleus, parabigeminal nucleus, pons and rected to different thalamocortical pathnucleus of the optic tract (Abplanalp, '71), ways. Because a variety of cortical areas while the deep layers project to the intra- may be indirectly influenced by the projeclaminar nuclei and posterior nuclear group tions of the superficial and deep layers of (Harting et al., '72; Harting et al., '73). In the superior colliculus in the rhesus monthe bushbaby (Harting et al., '72), the key, difficult questions arise as to the funcsuperficial layers project to the caudal part tions of such projections and how they of the pulvinar while the deep layers pro- compare to the projections of the superior ject to the intralaminar and posterior group colliculus in other species. On the basis of the findings in the tree nuclei. The present results in the rhesus monkey lend further support to the findings shrew and bushbaby, Harting et al. ('72) of different projections from the deep and argued that unimodal visual information superficial layers of the superior colliculus. from the superficial layers would be directThese results in the rhesus monkey also ed into the pulvinar and dorsal lateral geindicate that more nuclei receive projec- niculate nucleus while multimodal infortions from both superficial and deep layers mation from the deep layers would be of the superior colliculus than previously directed into the intralaminar and posterior group nuclei. One basis for their argument reported in other species. These results have led to the following was that the superficial layers receive proconclusions. The superficial layers of the jections from the retina and visual cortex. A superior colliculus in the rhesus monkey similar argument could be made for the rheproject to the dorsal and ventral lateral sus monkey. Physiological and anatomical geniculate nuclei, inferior pulvinar, mag- studies in the rhesus monkey have shown nocellular dorsomedial nucleus, centro- that the organization of the superficial and intermediate nucleus, anterior pretectal deep layers of the superior colliculus are to nucleus and pretectal region. In addition, a large extent different. Physiological studthe rostral portion of the superficial layers ies have shown that cells with only visual may also project to the limitans nucleus, properties are located in the superficial lay-

PRIMATE COLLICULUS PROJECTIONS

ers of the superior colliculus (Schiller and Koerner, '72; Cynader and Berman, '72; Goldberg and Wurtz, '72, '72a), while those in the deep layers have visual, auditory, somatic (Cynader and Berman, '72) and motor properties (Schiller and Koerner, '71 ; Wurtz and Goldberg, '71, '72; Robinson, '72; Schiller and Stryker, '72). Anatomical studies have shown that the afferent connections of the superficial and deep layers of the superior colliculus in the rhesus monkey are also different. Hendrickson et al. ('70) and Wilson and Toyne ('70) have reported that the retinotectal projection is restricted to the superficial layers of the caudal two-thirds of the superior colliculus. The rostra1 one-third of the superior colliculus may not receive retinal input but may receive topographical input from occipital cortex (Wilson and Toyne, '70). Wilson and Toyne ('70) and Lund ('72) have also shown that the occipital cortex projects to the entire rostro-caudal extent of the superficial layers of the superior colliculus, while the data in the present study and the data of Campos-Ortega et al. ('70) and Kuypers and Lawrence ('67) indicate that occipital cortex projects to the deeper layers as well. However, the visual cortex is not the only cortical area which projects to the deep layers of the superior colliculus. Cortical areas which include the parietal, temporal and frontal lobes also project to the deep layers of the superior colliculus (Kuypers and Lawrence, '67). These projections to the deep layers from cortices other than the visual cortex may provide a substrate by which non-visual modalities also influence the cells of the deep layers. In addition, the anatomical study of Moore and Goldberg ('66) showed that the inferior colliculus projects directly to the deep layers of the superior colliculus indicating that auditory information can be relayed directly to the cells of the deep layers. These anatomical and physiological results, when considered together, imply that in the rhesus monkey the cells of the superficial layers are basically concerned with visual input, and cells of the deep layers, although also concerned with visual input, are functionally different and may be multimodal as was argued before for other species. The argument that the superficial layers of the rhesus monkey superior colliculus

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are concerned with the visual system seems to be strengthened by a recent autoradiographic study of the cortical projections of the inferior pulvinar of the rhesus monkey (Rezak and Benevento, '75). The cortical projection zone of the portion of the inferior pulvinar that receives input from the superficial layers extends from area 17 to the posterior part of the temporal lobe and includes areas 18, 19, 20 and 21. These areas of projection include the lunate sulcus, the inferior occipital sulcus, and the floor and posterior bank of the superior temporal sulcus or area MT of other primates. All these cortical areas have been implicated in visual function in monkeys (e.g., Allman and Kaas, '71). Although the superficial and deep layers of the superior colliculus, contain cells with visual properties, one should not conclude that the many nuclei of thalamocortical systems receiving projections from the superior colliculus are primarily concerned with the processing of visual information, as are the dorsal lateral geniculate nucleus, inferior pulvinar and associated cortex. On the basis of the different afferent projections to the superior colliculus and efferent projections of the superior colliculus to a number of thalamic nuclei, it is more likely that the superior colliculus is involved, in part, with many sensory modalities. The superior colliculus may provide one route by which the visual modality enters multimodal thalamocortical systems. In the cat, tree shrew, and bushbaby, the recent data on the projections of the superior colliculus to certain thalamic nuclei and the cortical projections of these thalamic nuclei also suggest that the superior colliculus is involved with the transmission of information into thalamocortical systems other than the thalamo-occipital visual system. For example, in the cat, the superior colliculus projects to the pulvinar, lateral posterior nucleus and the nuclei of the posterior group which include the magnocellular medial geniculate nucleus and the suprageniculate nucleus (Rose and Woolsey, '49). The posterior nuclear group is a complex area which contains cells with multimodal properties including visual (Wespic, '66). The suprageniculate and magnocellular medial geniculate nuclear portions of the posterior nuclear group project, in turn, to distant cortical areas such as the orbital and insular cortices (Heath

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and Jones, ’70; Graybiel, ’72, ’72a). In addition, the lateral posterior nucleus, which may receive projections mainly from the superior colliculus projects to wide areas of neocortex beyond the occipital cortex (Graybiel, ’72). In the tree shrew and bushbaby, the superior colliculus has also been shown to project to the pulvinar, the posterior nuclear group and the intralaminar nuclei. In the tree shrew, Harting et al. (’72) and Harting et al. (’73) showed that the pulvinar, which receives projections throughout its extent from just the superficial layers of the superior colliculus, projects to the temporal cortex. In the bushbaby, both divisions of the caudal pulvinar project to the temporal lobe (Harting et al., ’72; Harting et al., ’73). It is difficult to view the many cortical areas of the cat, tree shrew and bushbaby which are not occipital cortex and receive projections from the thalamic target nuclei of the superior colliculus as strictly visual. Graybiel (’72) encountered this problem of interpreting the multiple ascending projections of the superior colliculus in the cat. This author pointed out that if many of the cortical areas which receive input from the thalamic target nuclei of the superior colliculus were viewed as “visual” or somehow associated with motor functions of the superior colliculus, then an “inversion of classic notions(s) about association cortex” would be encountered. In contrast to the projections of the superior colliculus of the cat, tree shrew, bushbaby and rhesus monkey, the projections of the superior colliculus of the squirrel monkey may be quite restricted and may be mainly involved with the visual system and occipital cortex. Mathers (’71) made large lesions of the superior colliculus and found degeneration only in the inferior pulvinar and posterior nucleus (suprageniculate nucleus). He found no evidence of projections to the magnocellular portion of the medial geniculate nucleus, the dorsal lateral geniculate nucleus or other subdivisions of the pulvinar. Such differences in the findings for the squirrel monkey and the rhesus monkey, upon both of which the same light-microscopic techniques were used, were not expected. However, Spatz and Tigges (’72) have shown that the connectional relationships between striate and prestriate cortices are different for the rhe-

sus and squirrel monkey. These authors stated that the squirrel monkey and rhesus monkey seem to represent “a remarkable species difference” with respect to the cortical organization of their visual systems. Furthermore, this difference may indicate that the associations of visual cortex in Old World and New World monkeys may have evolved independently. These species differences in visual cortical systems may also reflect differences in thalamo-cortical connections and, likewise differences in tecto-thalamic connections that are associated with thalamocortical systems. Thus, the differences between the tectal projettions of the squirrel monkey (Mathers, ’71) and rhesus monkey may be accounted for by differences in the development of visual systems in these two species. In contrast to the tectal projections of the squirrel monkey, the present findings are similar to those reported in an earlier Nauta study in the rhesus monkey (Myers, ’63) and, in many respects, similar to the findings reported in the recent degeneration studies in more distant species, i.e., the cat (Graybiel and Nauta, ’71; Graybiel, ’72), tree shrew (Abplanalp, ’71; Harting et al., ’72; Harting et al., ’73) and bushbaby (Harting et al., ’72). Pretectum. The axons of the neurons located in the superior colliculus were found to enter the pretectum. It is interesting that lesions of the pretectum (Carpenter and Pierson, ’73) gave rise to degenerated axonal endings in the medial pulvinar, inferior pulvinar, and dorsal and ventral lateral geniculate nuclei. These projections are similar to some of the projections of the superior colliculus in the present study. The efferents of the pretectum (Carpenter and Pierson, ’73) and the superior colliculus that project to the inferior pulvinar and dorsal and ventral lateral geniculate nuclei pass through the brachium of the superior colliculus. Therefore, it may be difficult to determine to what extent lesions of the superior colliculus might interrupt axons that originate in the pretectum and project to the inferior pulvinar and lateral geniculate nuclei. It is also possible that tectal efferents, which pass through the pretectum, are interrupted during lesions of the pretectum. Thus, whether the projections of the pretectum and superior colliculus constitute parallel visual system projections to thalamic nuclei, or whether the

PRIMATE COLLICULUS PROJECTIONS

interruption of fibers of passage with pretectal or tectal lesions accounts for these projections, remains to be resolved in the rhesus monkey. However, evidence has been presented in the opossum (Benevento and Ebner, '70, '71a) and cat (Graybiel, '74) for independent and parallel pretectal and tectal systems. ACKNOWLEDGMENTS

This study was supported by NSF grant GB 35366X. J . H. Fallon was supported by NIMH training grant 8396. The technical assistance of Nodee DuBose in the preparation of the histological materials is greatly acknowledged. LITERATURE CITED Abplanalp, P. 1971 The neuroanatomical organization of the visual system in the tree shrew. Folia. primat., 16: 1-34. Akert, K . 1964 Comparative anatomy of the frontal cortex and thalamo-frontal connections. In: The Frontal Granular Cortex and Behavior. J . M. Warren and K. Akert, eds. McGraw Hill, New York, pp. 372-396. Allman, J . M . , and J . Kaas 1971 A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey. Brain Res., 31: 8 S 1 0 5 . Altman, J., and M. B. Carpenter 1961 Fiber projection of the superior colliculus in the cat. J. Comp. Neur., 126: 157-177. Benevento, L. A. 1973 Synaptic mechanisms of orbital, insular, temporal tip cortex in the Rhesus monkey. Anat. Rec., 175: 498. 1975 New stereutaxic coordinates for the rhesus monkey thalamus referencing visual afferents with cytoarchitecture. J. Hirfosch. In press. Benevento, L. A,, and F. F. Ebner 1970 Pretectal, tectal, retinal and cortical projections to thalamic nuclei of the Virginia opossum in stereotaxic coordinates. Brain Res., 18: 171-175. 1971 The areas and layers of corticocortical terminations in the visual cortex of the Virginia opossum. J. Comp. Neur., 141: 157-190. 1971a The contribution of the dorsal lateral geniculate nucleus to the total pattern of thalamic terminations in striate cortex of the Virginia opossum. J. Comp. Neur 143: 243-260. Benevento, L. A., and J. Failon 1975 The projection of occipital cortex to the dorsal lateral geniculate nucleus in the rhesus monkey (Macaca mulatta). Exp. Neur., February: in press. Brodmann, K. 1909 Vergleich einer Lokalisationslehre der Grosshirnrinde in ihren prinzipien dargestellt auf Grund des Zellenbaues. J. A. Barth, Leipzig. Campos-Ortega, J. A,, W. R. Hayhow and P. F. De V. Cliiver 1970 The descending projections from the cortical visual fields of Macaca mulatta with particular reference to the question of a corticolateral geniculate pathway. Brain Behav. E d . , 3: 368414. Carpenter, M. B., and R. J. Pierson 1973 Pretectal region and the pupillary light reflex. An anatomical analysis in the monkey. J. Comp. Neur., 149: 271-300.

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Casgrande, V. A., J. K. Harting, W. C. Hall, I. T. Diamond and G. F. Martin 1972 Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science, 177, 444447. Cynader, M., and N. Berman 1972 Receptive field organization of monkey superior colliculus. J. Neurophysiol., 35: 187-201. Fink, R., and L. Heimer 1967 Two methods of selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res., 4 . 369-374. Goldberg, M. E., and R. H. Wurtz 1972 Activity of superior colliculus in behaving monkey. 11. Effect of attention on neuronal responses. J. Neurophysiol., 35: 560-574. 1972 Activity of superior colliculus in b e having monkey. I. Visual receptive fields of single neurons. J. Neurophysiol., 35 : 542559, Graybiel, A. M. 1972 Some fiber pathways related to the posterior thalamic region in the cat. Brain Behav. Evol., 6: 36S393. 1972a Some extra-geniculate visual pathways in the cat. Invest. Opthalmol., 1 1 : 322332. - 1973 The thalamo-cortical projection of the so-called posterior nuclear group: A study with anterograde degeneration methods in the cat. Brain Res., 49: 22S244. 1974 Studies on the anatomical organization of posterior association cortex. In: The Neurosciences. F. 0. Schmitt and F. G. Worden, eds. MIT Press, Massachusetts, pp. 205-214. Graybiel, A., and W. J. H. Nauta 1971 Some projections of superior colliculus and visual cortex upon the posterior thalamus in the cat. Anat. Rec., 169: 328. Harting, J. K., K. K. Glendenning, I. T. Diamond and W. C. Hall 1973 Evolution of the primate visual system: Anterograde degenerative studies of the tecto-pulvinar system. Am. J. Phys. Anthrop., 38: 383-392. Harting, J. K., W. C. Hall and I. T. Diamond 1972 Evolition of the pulvinar. Brain Behav. Evol., 6 424452. Harting, J. K . , W. C. Hall, I. T. Diamond and G. F. Martin 1973 Anterograde degeneration study of the superior colliculus in Tupaia g l i s : Evidence for a subdivision between superficial and deep layers. J. Comp. Neur., 148:361386, Heath, C. J., and E. G. Jones 1971 An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat. J . Comp. Neur., 141 : 397426. Hendrickson, A., M. E. Wilson and M. J. Toyne 1970 The distribution of optic fibers in Macaca mulatta. Brain Res., 23: 425427. Kuypers, H. G., and P. G. Lawrence 1967 Cortical projectionsto the red nucleus and the brain stem in the rhesus monkey. Brain Res., 4: 151-188. Lund, R. D. 1972 Synaptic patterns in the superficial layers of the superior colliculus of the monkey, Macaca mulatta. Exptl. Brain Res., 15: 194211. Martin, G. F. 1969 Efferent tectal pathways of the opossum. J. Comp. Neur., 135: 209-244. Mathers, L. H. 1971 Tectal projection to the posterior thalamus of the squirrel monkey. Brain Res., 35: 255298. Moore, R. Y., and J. M. Goldberg 1966 Projec-

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tions of the inferior colliculus in the monkey. Exp. Neurol., 14: 4 2 9 4 3 8 . Myers, R. E. 1963 Projections of superior colliculus in monkey. Anat. Rec., 1 4 5 : 264. Olszewski, J. 1952 The thalamus of Macczccc mul a t t n . An atlas for use with the stereotaxic instrument. Karger, Basel. Rafols, J. A , , and H. A . Matzke 1970 Efferent projections of the superior colliculus in the opossum. J. Comp. Neur., 138: 147-160. Rezak, M . , and L. A. Benevento 1975 Some cortical projections of the inferior pulvinar in the rhesus monkey ( M a c a c a mulatta). American Association of Anatomists, L~~ ~~~~l~~ and Anat. Rec., March: in press. Robinson, D. A. 1972 E~~ mOvemenIS evoked by collicular stimulation in the alert monkey. Vision Res., 12: 1 7 9 5 1 8 0 8 . Rose, J. E., and C. N. Woolsey 1949 The relations of thalamic connections, cellular structure and evocable electrical activity in the auditory region of thecat. J. Comp. Neur., 91: 4 4 1 4 6 6 . Schiller, P. H. 1972 Some functional characteristics of the superior colliculus of the rhesus monkey. Bibl. Ophthal., 82: 122-129. Schiller, P. H., and F. Koerner 1971 Discharge characteristics of single units in suaerior colliculus of the alert rhesus monkey. J. Neurophysiol., 34 : 920-936. Schiller, P. H., and M. Stryker 1972 Single unit I

recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol., 35: 915-925. Schiller, P. H., M. S. Stryker, M. Cynader and N. Berman 1974 Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. J. Neurophysiol., 3 7 . 181-194. Snider, R. S., and J. C. Lee 1962 A stereotaxic atlas of the monkey brain (Macaccc mzrlattn). UnlvcrsitY of Chicago Press, Chicago. Spa% W. B., and J. Tigges 1972 Species difference between Old World and New World monkeys in the organization of the striate-prestriate association. Brain Res., 43: 591-594. Von Bonin, G . , and P. Bailey 1947 The neocortex of Mncncer mulntta. University of Illinois Press, Urbana. Wespic, J. G. 1966 Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. Exp. Neurol., 1 5 : 299-318. Wilson, M . E., and M. J. Toyne 1970 Retinotectal and cortico-tectal projections in Mocnccr mulnttci. Brain Res., 24: 3 9 5 4 0 6 . Wurtz, R. H., and M. E. Goldberg 1971 Superior colliculus cell responses related to eye movements in awake monkeys. Science, 171 : 82-84. 1972 Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements. J. Neurophysiol., 35: 587-596.

Note added in proof: Results from our recent autoradiographic studies (Benevento and Rezak, '75) with injection of tritiated Leucine and Proline into the superficial layers of the superior colliculus support the present findings and, i n addition, indicate that the superficial layers do project to the Zirnitans nucleus and lateral posterior nucleus. Trojanowski and Jacobsen (Brain Res., 80: 395-411, 1974) have recently reported that the medial pulvinar projects topographically to the frontal eye fields in the rhesus monkey. Thus the projection from the deep layers of the superior colliculus to the medial pulvinar a s reported in the present study may provide one means by which visuomotor and multimodal information reaches the prefrontal cortex.

PLATE 1 EXPLANATION

OF F I G U R E S

Low power photomicrographs of sections stained with cresyl violet showing examples of the lesions in the superior colliculus. Same cases as in figures 2-4. (Fig. 1, lesions l b , 4b, 8 ) .

6

Small lesion of superficial layers (stratum zonale, stratum griseum superficiale, dorsal part of stratum opticum) of a rostra1 portion of the superior colliculus. (Refer to fig. l A , lesion l b and tic marks in fig. ic, superficial.)

7

Small lesion of deep layers of a caudal portion of the superior colliculus (stained using the Fink-Heimer technique and counter-stained with cresyl violet). (Refer to fig. l B , lesion 4b and tic marks in fig. l C , deep.)

8

Large lesion of the superior colliculus. (Refer to tic marks in fig. l C , lesion 8, total.)

PRIMATE COLLICULUS PROJECTIONS L. A. Benevento and James H. Fallon

PLATE 1

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PLATE 2 E X P L A N A T I O N O F FIGURES

Photomicrographs of sections stained with the Fink-Heimer technique showing moderately dense pericellular a n d sparse terminal degeneration after small lesion of thc superficial layers of the superior colliculus. Same case a s in text ( l a , b f . 9

358

Degeneration in the magnocellular dorsomedial nucleus. X 320. (Fig. 2 A , level 660, arrow.)

x 320. (Fig. 2A, level 700,

10

Degeneration in t h e limitans nucleus. arrow.)

11

Degeneration in the dorsal lateral geniculate nucleus. level 620, arrow.)

X

640. (fig. 2B.

PRIMATE COLLICULUS PROJECTIONS L. A. Benevento and James H. Fallon

PLATE 2

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PLATE 3 E X P L A N A T I O N OF F I G U R E S

Photomicrographs of sections stained with the Fink-Heimer technique.

360

12

Sparse pericellular degeneration in the medial pulvinar after small lesions of the deep layers of the superior colliculus (fig. 3 A , level 6 5 8 , arrow and lesions 4a,b of fig. 1).

13

Sparse pericellular degeneration in the oral pulvinar after small lesions of the deep layers of the superior colliculus (fig. 3B, level 591, arrow and lesions 4a,b of fig. 1).

14

Moderately dense pericellular and terminal degeneration in the inferior pulvinar after small lesions of the superficial layers of the superior colliculus (fig. 2 B , level 620, arrow and lesions l a , b of fig. 1).

15

Sparse to moderately dense pericellular and terminal degeneration in the inferior pulvinar after small lesions of the deep layers of the superior colliculus (fig. 3B, level 6 3 8 , arrow and lesions 4a,b of fig. 1). A p prox. X 360.

PRIMATE COLLICULUS PROJECTIONS L. A. Benevento and J a m e s H. Fallon

PLATE 3

36 1