Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca.

THE JOURNAL OF COMPARATIVE NEUROLOGY 310~475606(1991)

Architectonics of the Parietal and Temporal Association Cortex in the Strepsirhine Primate Galago Compared to the Anthropoid Primate Macaca TODD M. PREUSS AND PATRICIA S. GOLDMAN-RAKIC Section of Neurobiology, Yale University School of Medicine, New Haven 06510 (T.M.P., P.S.G.-R.) and Department of Anthropology, Yale University, New Haven 06520 (T.M.P.), Connecticut

ABSTRACT A number of higher order association areas have been described in the parietal and temporal cortex of large-brained anthropoid primates such as Macaca. However, little is known about the evolution of these areas, and the existence of homologous areas has not yet been clearly demonstrated in other mammalian groups. We addressed this issue by comparing the myelo- and cytoarchitecture of posterior association cortex in the anthropoid Macaca to that of the small-brained, strepsirhine ( "prosimian") primate Galago. Our results suggest that Galago possesses many, if not most, of the areas present in Macaca. We were able to identify regions in Galago which resemble Macaca posterior parietal area 7, superior temporal polysensory cortex (ST), inferotemporal visual cortex (IT), the temporoparietal auditory area (Tpt), and posterior parahippocampal cortex (areas TH and TF). Area 7, ST, and IT can each be subdivided further in Macaca, and for most of these subdivisions we were able to identify counterparts in Galago. However, we could not distinguish as many divisions of ST cortex in Galago as in Macaca, and it is possible that new areas arose in this region during anthropoid evolution. There also appear to be general differences in architectonic organization between these animals, with Macaca exhibiting greater development of pyramidal layer IIIc and of the internal granular layer (IV)across much of the parieto-temporal cortex. These findings suggest that many, although possibly not all, of the parietal and temporal association areas present in the modern anthropoid Macaca evolved early in primate history, prior to the divergence of the lineages leading to strepsirhines and anthropoids. Key words: higher cortical function, evolution, monkey, prosimian

In a previous study (Preuss and Goldman-Rakic, '91a), we compared the myelo- and cytoarchitectonic organization of granular frontal cortex (GFC) in the strepsirhine primate Galago and the anthropoid primate Macaca Here, we extend our comparative architectonic investigation of primate association areas to the parietal and temporal cortex. In anthropoids, much of the parietal and temporal cortex is occupied by higher order association areas, that is, regions which receive input from sensory areas and which mediate integrative aspects of perceptual, cognitive, and motor functions (Fig. 1).The parietal lobe contains higher order somatosensory and visuospatial areas (Andersen, '87, '88, '89; Friedman et al., '86; Mountcastle et al., '841, many of which lie within the region designated as area 7 by Brodmann ('05, '09). The temporal lobe contains auditory association areas (Galaburda and Pandya, '82, '83;Leinonen et al., '801, polysensory areas (Baylis et al., '87; Bruce et O

1991 WILEY-LISS, INC.

al., '811, visual areas including notably the inferotemporal (IT) cortex (Gross et al., ,811, and areas in the parahippocampal region, which has been implicated in memory processes (Van Hoesen, '82). These structures exert their influence on behavior in part through their strong connections with the frontal lobe, and in particular with the granular frontal cortex (Goldman-Rakic, '87a,b, '88). At present, there is little indication that homologous higher order association areas exist in strepsirhines. There is some limited evidence that they possess parietal area 7 and perhaps also IT visual cortex (Allman et al., '79; Brodmann, '08, '09; Glendenning et al., '75; Raczkowski and Diamond, '80; Wall et al., '821, although it is not known Accepted May 3,1991. Dr. Preuss is now a t the Dept. of Psychology, Vanderbilt University, 301 Wilson Hall, Nashville, TN 37240.

476

T.M. PREUSS AND P.S. GOLDMAN-RAKIC

whether these regions consist of multiple divisions as they do in anthropoids. There is almost no information available at present concerning other associational regions, such as the superior temporal polysensory cortex or the parahippocampal region. An important objective of the present study, therefore, was to determine whether Galago possesses homologues of the higher order parietal and temporal association areas of Macaca. To address this issue, we have analyzed the myeloand cytoarchitectonic organization of Galago cortex at a level of detail similar to that attained in recent studies of Macaca (e.g., Desimone and Ungerleider, '86; Pandya and Seltzer, '82; Seltzer and Pandya, '78, '80), and have evaluated homologies by direct comparison of cortical architecture in Galago and Macaca. This investigation also provides the architectonic foundation for our subsequent study of the connections between the parietal, temporal, and frontal association cortex in Galago (Preuss and GoldmanRakic, '91b).

METHODS We examined seven hemispheres from five greater or thick-tailed bushbabies (three Galago crassicaudatus and two G. garnetti), and six hemispheres from three macaque

monkeys (Macaca mulatta). Table 1provides a summary of the animals used and the manner in which tissue was sectioned and stained. The brains examined in this study were obtained from animals anesthetized and perfused with aldehyde fixatives, as described previously (Preuss and Goldman-Rakic, '91a). In most cases, brains were frozen sectioned at 35-40 pm and stained for Nissl substance with thionin and for myelin with a modification of the method of Gallyas ('79). Additional hemispheres were embedded in celloiden, sectioned at 25-35 pm and stained with cresyl violet and hematoxylin. The photomicrographs presented here are exclusively of frozen-sectioned tissue, however. All Galago and Macaca hemispheres but one were sectioned in the coronal plane. The exception was bushbaby G11, in which the left parietaltemporal block was sectioned horizontally. Architectonic analysis was carried out in a manner similar to that described in Preuss and Goldman-Rakic ('91a). Our surface drawing of posterior cortex in Macaca (see Fig. 4)is based primarily on published sources, supplemented by our own observations. Analysis of Galago was more comprehensive. Series of sections were drawn at low magnification (10x1 for five hemispheres (four sectioned coronally, one horizontally), showing the location of architectonic boundaries. Surface reconstructions were made for three of these cases, which served as the primary basis for our composite reconstruction of Galago cortex (see Fig. 5 ) .

Abbreviations AIP amyg AON

As ASd ASv CaS Cd CgS CgSa

CM CS FPO FSa FSP FST GFC HC HS Ia Ia-p Idg Ig IG Ins

10s IPL IPS IT L LCS LIP LMZ LOS LS LUS MF MFc MFr MIP MOS

anterior intraparietal area amygdala anterior olfactory nucleus arcuate sulcus arcuate sulcus, dorsal limb arcuate sulcus, ventral limb calcarine sulcus caudate nucleus cingulate sulcus cingulate sulcus, anterior part caudomedial auditory area central sulcus frontoparietal opercular area anterior frontal sulcus posterior frontal sulcus visual area in the fundus of the superior temporal sulcus granular frontal cortex hippocampus hippocampal sulcus agranular insular area periallocortical division of agranular insular cortex dysgranular insular area granular insular area induseum griseum insular cortex inferior occipital sulcus inferior parietal lobule intraparietal sulcus inferotemporal cortex lateral auditory area lateral calcarine sulcus lateral intraparietal area lightly myelinated zone of the temporal lobe lateral orbital sulcus lateral (Sylvian) sulcus lunate sulcus medial frontal areas caudal division of medial frontal cortex rostral division of medial frontal cortex medial intraparietal area medial orbital sulcus

MPD MPOS MST MT Oa-p

OB OF0 OLS

0s

OTS OTrS OTu Para PCS PIP Pir PL PM PO POS PrCO PS PSub R RcS RoS RS RSa RSP SP SPL SPS SSA ST STd STS TPt VA VIP VP

medial dorsal parietal cortex medial parieto-occipital sulcus medial superior temporal visual area middle temporal visual area periallocortical division of agranular orbital cortex olfactory bulb orbitofrontal opercular area olfactory sulcus orbital sulcus occipito-temporal sulcus transverse occipital sulcus olfactory tubercle paralimbic cortex paracalcarine sulcus posterior intraparietal area piriform cortex prelimbic area medial pulvinar parieto-occipital visual area parieto-occipital sulcus precentral opercular area principal sulcus presubiculum and parasubiculum rostral auditory area retrocalcarine sulcus rostral sulcus rhiual sulcus rhinal sulcus, anterior part rhinal sulcus, posterior part posterior somatosensory area superior parietal lobule splenial sulcus supplementary sensory area (part of Brodmann's area 5) superior temporal cortical region dorsal division of superior temporal cortex superior temporal sulcus temporo-parietal area ventral anterior visual area ventral intraparietal area ventral posterior visual area

477

GALAGO PARIETAL AND TEMPORAL CORTEX

Anterior Parietal (S1 complex & S2)

Posterior Parietal (5 8 L 7)

$$y _J .A.

.. ....

.......,..................

Posterior Parahippocampal - TF/TH (ventral surface)

1 cm Anterior Par (S1 corny'-

Galago Fig. 1. Organization of higher order association regions of parietal and temporal cortex in the anthropoid primate Macaca and the strepsirhine primate Galago, as currently understood. The regions discussed in this work include the posterior parietal cortex, with emphasis on area 7; auditory association area Tpt; the superior temporal region (ST), which is comprised of auditory association cortex and polymodal cortex; the inferotemporal visual region (IT); and the posterior parahippocampal cortex (areas TF and TH). Both the ST and IT cortex extend into the superior temporal sulcus (STS). The posterior

parahippocampal areas are located on the ventral surface of the temporal lobe, medial to IT. In Macaca, the organization of these regions has been worked out using architectonic, connectional, electrophysiological, and behavioral techniques. There have been relatively few investigations of these regions in Galago or related strepsirhines, and these have mainly employed architectonic techniques. There is general agreement among these studies regarding the location of area 7; there is also evidence suggesting that these animals possess IT cortex. However, Tpt, ST, and TF/TH have not yet been identified in Galago.

478

T.M. PREUSS AND P.S. GOLDMAN-RAKIC TABLE 1. Material Used for Study of Parietal and Temporal Lobe Architectonics Species and gender

Hemispheres

Plane

Sectioning Medium

G6 G11 G13

Galago garnetti adult M G. crassicaudatus adult F G. crassicaudatus adult M

L, R

G17

G. crassicaudatus adult M Garnetti adult M Macaca mulatta adult M Macaca mulatta adult M Macaca mulatta infant F

coronal coronal horizontal coronal coronal coronal coronal coronal coronal

celloiden freezing freezing freezing freezing freezing freezing freezing celloiden

Animal

G20

M1 M4 M5

(Brodmann, '09)

L

L R L

R L, R

L,R L, R

21

Thickness

Staining

25 pm 35 pm 40 pm

cresyl violet (1:41hematoxylin (1:4j thionin (1:8) Gallyas (1:s) thiomn (1:4) Gallyas (1:4) thionin (1:8j Gallyas (1%) thionin (1:81 Gallyas (1:8j thionin (1:5j Gallyas (15) thionin (1:5) Gdyas (1:lOI thionin (1:5) Gallyas ( 1 : l O j cresylviolet ( 1 : l O j

40 I*.m 35 pm 35 pm 40 hrn

35 ni 35 pm

Lemur (Brodmann, '09)

Fig. 2. Cytoarchitectonic maps of the anthropoid Cercopithecus and the strepsirhine Lemur from Brodmann ('09). In Brodmann's map of Cercopithecus, posterior parietal areas 5 and 7 occupy respectively the superior and inferior parietal lobules, which are separated by the intraparietal sulcus. In Lemur, area 7 covers both the inferior and superior parietal lobules.

RESULTS Parietal cortex Conventionally, the parietal cortex of primates is divided into anterior and posterior regions. The anterior region consists of somatosensory cortex, including the primary somatosensory complex, corresponding to areas 3, 1,and 2 of Brodmann ('091, the second somatosensory area, and related areas (for reviews, see Burton, '86; Kaas, '83).The posterior parietal cortex consists of Brodmann's areas 5 and 7 (Fig. 21, both of which can be subdivided further on physiological, connectional, and architectonic grounds (e.g., Murray and Coulter, '81a; Pandya and Seltzer, '82). Area 5 is part of the somatic sensorimotor domain, whereas most divisions of area 7 have visuospatial functions (Andersen, '87, '88, '89). Because the subdivisions of area 7 are strongly and differentially connected with the granular frontal cortex in Macaca (e.g., Cavada and Goldman-Rakic,

'89b), the organization of this region in Galago is a particular concern of the present study. However, portions of the anterior parietal cortex also have connections with GFC (Preuss and Goldman-Rakic, '89), and we therefore briefly consider the organization of this region. Anterior parietal cortex and posterior parietal area 5. The anterior parietal region has been intensively studied in both anthropoid and strepsirhine primates, and it is clear that these animals share a very similar plan of areal and architectonic organization (see the reviews of Carlson, '85; Kaas, '82b, '83). Here, we point out certain salient characteristics of this region that we have observed in Galago, emphasizing features which distinguish Galago from anthropoids. In Galago crassicaudatus, as in most other strepsirhines and unlike most anthropoids, the parietal and frontal lobes are not separated by a central sulcus (Figs. 3-5). However,


479

Macaca tnulatta

Galago crassicaudatus

Dorsal

Lateral

1 cm

Medial

4

OLS I

VentraI Fig. 3. External morphology of Macaca mulattu and Galago crassicaudatus. Galago is drawn at a slightly larger scale than Mucaca. Gulag0 is relatively lissencephalic compared to Mucaca. It has a deep intraparietal sulcus (IPS),but the superior temporal sulcus (STS)is usually a shallow dimple or depression rather than a deep fissure.


480

3% 3b buried in CS

6M

Lateral 1 cm

B Figure 4A-B


481

1 cm

L-../

Figure 4C-E

482

Galago does possess a surface marking in this region, a short, longitudinally oriented groove, which we have termed the posterior frontal sulcus, or FSp (Preuss and GoldmanRakic, '91a). The FSp extends caudally from primary motor cortex through the lateral part of the primary somatosensory area (Sl). Within the anterior parietal cortex of strepsirhines (Figs. 5-7), homologues of several anthropoid somatosensory areas have been proposed on the basis of cytoarchitectonic, physiological, and connectional studies (Burton and Carlson, '86; Carlson and Fitzpatrick, '82; Carlson and Welt, '80, '81; Fitzpatrick et al., '82; Krishnamurti et al., '76; Sanides and Krishnamurti, '67; Sur et al., '80). In Galago, the S1 cutaneous representation corresponds to a region of koniocortex (Carlson and Welt, '80; Sur et al., '80); this territory is probably homologous to area 3b of anthropoid primates (Kaas, '83; Sur et al., '80). In Galago area S1(3b), layer IV is very thick and densely packed with granular cells, and the supragranular layers are dense and small celled as well (Fig. 7). We have noted, however, that cell density in Galago 3b appears to be somewhat lower than in anthropoids (see also Kaas, '82b; Sur et al., 'SO), which may explain why Brodmann ('08, '09) designated this zone as area 1rather than area 3 in strepsirhines (Fig. 2). One unusual characteristic of Galago crassicaudatus, which has not previously been reported, is the presence of a prominent caudal spur of apparently koniocortical tissue, which extends caudally from 3b along the dorsal rim of the lateral sulcus (Figs. 5, 6A). This spur, designated here as Slc, is in the expected location of the S1 external ear representation. An enlarged ear representation would be consistent with the great size and exquisite tactile sensitivity of the pinnae in Galago crassicaudatus. However, it is also possible that this strip of tissue is a specialized subdivision of some area other than Sl(3b). Galago S1 (3b) is surrounded by additional somatosensory areas. Cortex resembling anthropoid area 3a in its architectonic and physiological characteristics lies immediately rostral to 3b (Carlson and Welt, '80). Ventral to 3b, the second somatosensory area, S2, is found along the dorsal bank of the lateral sulcus, as demonstrated with physiological and anatomical techniques by Burton and Carlson ('86). Architectonically, S2 is one of the most readily identifiable areas of the Galago cerebrum. It is very thick, forming a prominent bulge along the parietal operculum (Fig. 6A) and has a rather poorly stratified appearance in Nissl (Fig. 71, particularly in the deep layers (see also Burton and Carlson, '86). In myelin-stained sections, we have observed that S2 stains densely in both Galago and Macaca, with a characteristic single, thick band of diffuse fibers (Fig. 8A,E). In Galago, we have noted an additional area in the frontoparietal operculum immediately anterior to S2, designated here as FPO (Fig. 5 ) ,which possesses numerous long,

Fig. 4 (pages 480-481). Schematic representation of the cortical areal organization of Macaca. This interpretation is based on published studies (cited in the text), supplemented by our observations of myeloand cytoarchitecture. A,B: Lateral and medial views. C : Lateral view with the intraparietal sulcus (IPS)represented as "opened" to show the lateral divisions of the area 7 complex. D: Lateral view depicting areas buried within the lateral sulcus (LS). Areas R, L, PL, and CM are auditory areas. E: Areas located within the superior temporal sulcus (STS). Areas TAa, TPO, PGa, and IPa are divisions of ST polysensory cortex. Areas TEa and TEm are divisions of the IT visual cortex.

T.M. PREUSS AND P.S. GOLDMAN-RAKIC fine, radial fibers. In macaques, there appears t o be a myeloarchitectonicallysimilar area just anterior to S2 (Fig. 4),within cortex usually regarded as part of areas 1and 2 (Mesulam and Mufson, '82; Preuss and Goldman-Rakic, '89; Roberts and Akert, '63).Area FPO may correspond to a somatosensory area, termed the parietal ventral area, which has been localized immediately anterior to S2 in New World monkeys and in rodents (Krubitzer and Kaas, '90; Krubitzer et al., '86). The cortex in Galago, which extends posteriorly from S1 (3b) to the area 7 complex, is homotypical in character, with isolated, very large, layer V pyramidal cells (Fig. 7). We refer to this as the posterior somatosensory area, or Sp. Brodmann recognized a single unit, his area 5, in the same region of the strepsirhine Lemur, but recognized three separate areas, 1, 2, and 5, in the corresponding region of Old World monkeys (Fig. 2). Subsequent workers have found it difficult to distinguish Brodmann's areas 1, 2, and 5 in anthropoids using architectonic methods alone, although physiological and connectional studies have confirmed that they are distinct areas (Jones et al., '78; Kaas, '83;Nelson et al., '80; Pons and Kaas, '85; Pons et al., '85). Area 1 corresponds to a second, complete cutaneous representation lying immediately posterior to the S1 cutaneous representation (Nelson et al., '80). However, strepsirhines lack a complete cutaneous representation posterior t o S1 (Carlson, '85; Sur et al., 'SO), and therefore Sp is probably not homologous to area 1. Rather, units in Sp are responsive to stimulation of deep somatosensory receptors, similar t o neurons in anthropoid area 2 (Carlson, '85; h a s , '82, '83; Sur et al., '80). Sp may also include the homologue of anthropoid area 5, which is very similar in architecture to area 2 (Jones et al., '78). The area 7 complex. Brodmann ('05, '08, '09) designated a large region of posterior parietal cortex in primates as area 7. Subsequent investigations, mainly in Macaca, have demonstrated that area 7 is not in fact a single area but rather a heterogeneous group of areas, differing in architectonics, connectivity, and function. Various published interpretations of the divisions comprising the area 7 "complex" are illustrated in Figure 9. The lateral part of area 7, covering the inferior parietal lobule (IPL), is generally divided into anterior and posterior zones, following Vogt and Vogt ('19) and Bonin and Bailey ('47). The cortex of the intraparietal sulcus (IPS) is architectonically distinct from the IPL cortex and includes several subdivisions (Maunsell and Newsome, '87; Maunsell and Van Essen, '83; Seltzer and Pandya, '80; Ungerleider and Desimone, '86b; Van Essen, '85). The medial surface of the parietal lobe, included by Brodmann in area 7, contains additional areas (Pandya and Seltzer, '82; Vogt et al., '87). Whereas there is considerable agreement on these general points, published studies differ regarding the location of individual areas and names applied to them. The parcellation of macaque area 7 followed in this study is shown in Figure 4. Our observations indicate that area 7 can also be extensively subdivided in Galago, and some of these divisions appear to have counterparts in Macaca (Fig. 5). There are, however, several general differences in the architectonic organization of macaque and bushbaby cortex, which complicate the task of identifying homologous areas. First, as noted for area 3b, the internal granular layer (IV) in area 7 cortex usually appears less densely packed in Galago than in Macaca. (This difference extends to temporal cortex as well; see below.) There are also differences in the organiza-


483

tion of pyramidal layers I11 and V. In macaques, the largest than 7a-1 (Figs. 10, 11B). In Mucucu, 7a-m can also be pyramidal cells of a given area are usually concentrated in distinstinguished by the presence of conspicuous, large the deep part of layer 111, forming a distinct, dark sublam- pyramidal cells in layer IIIc. Pandya and Seltzer ('82) ina IIIc. Moreover, there is considerable variation in layer previously noted large IIIc cells along the rim of the IPS in I11 pyramidal cell size within the area 7 complex, providing Macaca but did not designate this zone as a separate area. one basis for its parcellation. In Galago area 7, by contrast, The opercular division of the area 7 complex, 7op, was the largest pyramidal cells are generally found in layer V, originally identified by Pandya and Seltzer ('82) who reand in most areas there is no distinct IIIc. Moreover, the ferred to it as PGop. The most distinctive characteristic of most obvious variations in pyramidal cell size across areas 7op is a band of very prominent, dark cells in layer IIIc. This are in layer V. is true of Galago as well as Macaca; in fact, 7op is the only Galago and Macaca also differ in the location of area 7 division of the Galago area 7 complex in which IIIc stands with respect to the sulci and gyri of the parietal lobe. In out as a distinct cell stratum. In myelin, Top has a diffuse Macaca, the IPS marks the border between areas 7 and 5: appearance, similar to S2, although the band of myelinated area 7 is located on the IPL and lateral bank of the IPS, fibers is narrower in Top than in S2 (Fig. 8B). whereas area 5 is situated on the medial bank of IPS and IPS and medial areas. Macaques and galagos both the SPL (Fig. 4). In Galago, the cortex which resembles possess several divisions of the area 7 complex medial to the macaque area 5 (area Sp, in our terminology) occupies only IPL and LS areas. However, the homologies of these areas a small, anterior part of the SPL, whereas most of the SPL are more difficult to specify. For this reason, we have used and the adjacent, medial bank of the IPS are occupied by different terms to designate areas in macaques and galagos, divisions of the area 7 complex (Fig. 5). (The location of area and we describe the areas of each animal separately before 7 in Galago corresponds very closely to that depicted by addressing the issue of homologies. Brodmann, '08, '09, for the strepsirhine Lemur, as shown Macaques. In macaques, the medial division of area 7a in Fig. 2.) As a consequence, there are certain divisions of extends for a short distance into the IPS, covering approxiGalago area 7, specifically those located on the medial IPS mately the outer one-quarter of its lateral bank. At the level and SPL, which correspond in position to Macaca area 5. of 7a, the lateral bank contains at least two additional, Despite these general differences, there are a number of myeloarchitectonically distinct zones, which evidently corcommon features of area 7 in galagos and macaques, particularly in the pattern of myeloarchitectonic variation respond to areas previously designated as LIP and VIP, as across its subdivisions (although there are cytoarchitec- shown in Figure 9D (Maunsell and Newsome, '87; Maunsell tonic and, for some areas, positional similarities as well), and Van Essen, '83; Ungerleider and Desimone, '86b; Van which provide a basis for inferring homologies. Our interpre- Essen, '85). (LIP and VIP correspond to the posterior tation of homologies is summarized in Table 2. For pur- portions of areas designated as POa-e and POa-i by Seltzer poses of description and comparison, it is useful to divide and Pandya "801.) Area LIP, which is located externally the area 7 complex into two groups of areas: one comprised along the bank adjacent to area 7a-m, has a bistriate of the areas located along the IPL and adjacent dorsal bank appearance in myelin, with distinct external and internal of the lateral sulcus (LS), the other comprising the IPS, the horizontal bands (Fig. 8B). It also has a few very coarse vertical fibers. Area VIP, which covers the internal part of SPL (in Galago),and the medial parietal cortex. the ventral bank and fundus of IPS, is also bistriate, The organization of this part of the IPL and LS areas. area 7 complex appears to be quite similar in Macaca and although the density of myelinated fibers is somewhat Galago; we have been able to identify four areas in both higher than in LIP and the gap between two horizontal taxa which share common characteristics of myeloarchitec- bands is often less distinct, particularly within the fundus. ture, cytoarchitecture, and location. We divide the IPL In some sections through VIP, especially those which pass cortex into an anterior zone, area 7b, and a posterior zone, through the middle portion of the area, VIP is much thicker 7a, and further divided the latter zone into a lateral area than LIP and forms a prominent bulge (Fig. 8B). At other (7a-1), located along the convexity of the IPL, and a medial levels, however, VIP and LIP are more nearly equal in area (7a-m), located along the rim of the IPS. An additional thickness. LIP and VIP are very similar in Nissl architecture, area, 7op, occupies the dorsal bank of the LS (i.e., the allowing for variations in cortical thickness and the compresparietal operculum) immediately ventral to the IPL. Area 7b stains well for myelin, with broad, diffuse sion of laminae within the IPS. Both areas possess thick external and internal bands, and thick vertical fibers (Fig. supragranular layers and thin infragranular layers (Fig. 8A,E). This area is distinguished in Nissl by the presence of 12). Layer V is very light and sparse and contains mostly relatively large pyramidal cells (Fig. 10). Broad cell columns small pyramidal cells with a few, scattered larger cells (which may be slightly more common in VIP than in LIP). are apparent in some (but not all) parts of 7b. Area 7a-1, located on the convexity immediately posterior Layer VI is very narrow, although this is a common feature to 7b, has a more orderly appearance in myelin than 7b, of cortex located along the walls of sulci. Layer IIIc is very with rigidly arrayed vertical and horizontal fibers and a prominent in both areas, with numerous darkly stained narrower external band (8B,F). In Nissl, 7a-1 has smaller pyramidal cells. In some sections, layer IIIc pyramidal cells pyramidal cells than 7b and its cell columns are narrower are clearly larger than in VIP than in LIP, but in other sections a difference is not obvious. (Fig. 10). The foregoing description applies to middle and posterior The cortex located along the rim of the IPS, area 7a-m, is distinctly different in appearance from area 7a-1. Area parts of IPS cortex, that is, to cortex at the level of area 7a. 7a-m is thicker and more heavily myelinated, with a dense Anteriorly, at the level of 7b, the organization of sulcal array of coarse vertical fibers that nearly obscures the cortex is somewhat different. Area 7b extends into the IPS horizontal and vertical bands (Figs. 8B,F, 11A). In addition, to cover the outer one-third to one-half of the lateral bank. area 7a-m has a broader layer IV and larger pyramidal cells The deepest part of the bank and the fundus are covered by

484

a single zone of thin cortex, which we term the anterior intraparietal area, or AIP. This area resembles LIP or VIP in general aspects of Nissl and fiber architecture. In myelin, for example, horizontal fibers predominate, sometimes appearing as a single band, although in some sections a fiber-sparse gap is apparent (Fig. 8A). Despite the resemblances between AIP and the posterior IPS areas, the fact that there is but a single area at anterior levels of the sulcus and that the connections of this region are with sensorimotor cortex rather than visual cortex (Matelli et al., '87; Seltzer and Pandya, '80) suggest that this zone is an area distinct from LIP or VIP. Colby et al. ('88) have proposed that there are two additional areas within the IPS, based primarily on connectional evidence. These are located along the fundus and medial bank at very posterior levels of the IPS and were termed the medial intraparietal (MIP) and posterior intraparietal (PIP) areas (Fig. 9D). We have not been able to delineate MIP and PIP in our architectonic material. However, our observations indicate that the region in which they are located is quite similar in myeloarchitecure to LIP, having a lightly to moderately stained bistriate appearance. In Nissl, also, the MIPPIP region resembles LIPNIP, with a light, cell-sparse layer V and prominent layer IIIc pyramidal cells. The medial part of Brodmann's area 7 covers much of the medial wall of the hemisphere ventral to the cingulate sulcus, from about the level of the splenium to the parietooccipital sulcus (POS). We recognize two areas within this region (Fig. 4B).The larger, more posterior division, which we term area 7m, is located immediately anterior to the parietal-occipital sulcus, where the parietal cortex borders visual area PO (Cavada and Goldman-Rakic, '89a; Colby et al., '88). The smaller anterior division, area 31, is located just dorsal to the splenial sulcus (SpS),occupying the region between area 7m and posterior cingulate area 23 (Armstrong et al., '86; Vogt et al., '871.' Compared to adjacent areas 1,2, and 5, the medial parietal areas are more lightly myelinated and have smaller pyramidal cells. They also lack the large IIIc cells present in lateral parts of area 7. In Nissl, areas 7m and 31 can be distinguished by differences in layer Va, which is light and very cell sparse in 7m and darker and more densely packed in 31 (Fig. 12). Also, layer VI in area 31 is divided into a dark upper band and a lighter deep band. In myelin, area 31 is lightly stained, with faint horizontal bands (Fig. 8C). Area 7m is darker, with distinct, narrow external and internal bands (Fig. 8D). Galagos. Medial to the IPL cortex in Galago, we recognize four divisions of the area 7 complex which occupy the fundus and medial bank of the IPS, the SPL, and the medial parietal surface. These areas are designated as 7s, 7d1, 7dm, and 7vm. It is important to note that in Galago most of the lateral bank of the IPS is occupied by 7a-m. In Macaca, by contrast, 7a-m is restricted to the rim, and most of the lateral bank is comprised of LIP and VIP. In Galago, 7a-m extends nearly to the fundus of the IPS, where it is replaced by the sulcal area, 7s (Figs. 6, 8E,F). Area 7s has welldeveloped internal and external fiber bands (Fig. BF), although the bands sometimes appear fused owing to the 'Area 31 is treated by some authors as a division of the cingulate cortex (Armstronget al., '86;Vogt et al., '87), rather than as the parietal cortex,but since it appears to fall within area 7 of Brodmann ('091, we treat it as part of the posteriorparietal cortex.

T.M. PREUSS AND P.S. GOLDMAN-RAKIC compression of the cortex around the fundus; there are also a few coarse vertical fibers. Prominent dark-staining layer V pyramidal cells are evident in Nissl, although, on the whole, layer V is rather cell poor (Fig. 12). Layers IV, V, and VI are very compressed in area 7s, with cells clustered into thick, wavy, vertical stacks. Given its location immediately adjacent to areas 7b and 7a-m, the most likely homologue of Gulag0 area 7s in Macaca is area LIP or AIP, or both. Certainly, the preponderance of horizontal fibers in 7s and the cell-poor character of its layer V are consistent with LIP and AIP (Figs. 8A,E,F, 12). Adjacent to area 7s in Galago, most of the dorsal bank of the IPS and the neighboring part of the SPL are covered by the thick cortex of the dorsolateral area, 7dl. Area 7dl is more heavily myelinated than 7s, having broad, dark, horizontal bands, and long vertical fibers (Fig. 8F). In Nissl, it has coarse cell columns, a thick layer IV,rather large, prominent Va pyramidal cells, and a very broad and pale deep stratum (Fig. 12). The most likely homologue of galago area 7dl is macaque area VIP, based mainly on the overall thickness and dense myelination of these two areas (compare D and F in Fig. 8). In contrast, 7dl differs considerably from VIP in its Nissl appearance (Fig. 12): layer Va of area 7dl contains many large, dark-staining pyramidal cells, whereas this stratum is cell sparse in VIP. Moreover, area 7dl lacks the large layer IIIc cells which are seen in VIP, although, as we have noted, Galago parietal cortex in general lacks large layer I11 cells. Sulcal area 7dl passes onto the superior parietal lobule for a short distance, where it is replaced by the dorsomedial area, 7dm. Area 7dm is rather similar to 7dl in architecture, and the border between them is sometimes difficult to locate precisely. However, area 7dm is typically less heavily myelinated than 7dl and has a narrower external fiber band (Fig. 8F). Additional myeloarchitectonic features of 7dm include a broad internal band, and prominent, long vertical fibers, similar to 7dl. Area 7dm also resembles 7dl in Nissl, although the columnar striations are finer and layer Va pyramidal cells are smaller on average in 7dm (Fig. 12).The largest class of pyramidal cells evidently have a patchy or irregular distribution in this area. Area 7dm is replaced in turn on the medial wall of parietal lobe by area 7vm. This area is lightly myelinated, with a very thin and pale external band and a somewhat more prominent internal band (Fig. BE). A few coarse vertical fibers are found in the internal band, but only a very few fine fibers extend superficially into the external band. In Nissl, 7vm has a darker and more densely packed layer Va than 7dm, although the largest class of Va pyramids are similar or slightly smaller in size (Fig. 12). Layer VI is split into a dark upper band and a paler deep band. Galago areas 7dm and 7vm resemble Macaca medial parietal areas 7m and 31, respectively. There are particularly good grounds for inferring homology between galago

Fig. 5. Interpretation of cortical areal organization in Galago crassicaudatus, based primarily on architectonic results of the present study. One division of the area 7 complex, area 7s, lies completely buried within the intraparietal sulcus and is not shown in this figure. The localization of extrastriate visual areas D, V4, and VANP is based in part on the electrophysiological mapping studies of Allman and McGuiness ('83) and Allman et al. ('79).

Entorhinal (28)

Figure 5


486

5 mm

Fig. 6. Areal divisions of the Galago parietal and temporal cortex, represented in a series of coronal sections arranged from anterior (A j to posterior (Ej.Case G17L.


3b

487

SP

m 0 m 0

P

Galago S2

Macaca S2

7 Fig. 7. Cytoarchitecture of parietal somatosensory areas 3b, Sp, 5, and S2. Gulugo area Sp is probably homologous to Mucacu areas 2 and 5, areas which are very similar in cytoarchitecture. Scale bar = 500 pm.

7vm and macaque 31. Both are located immediately dorsal to cingulate area 23, are lightly myelinated (compare C and F in Fig. 8) and possess a rather densely packed layer Va and a split layer VI (Fig. 12).Homolo@ between galago 7dm and macaque 7m is supported by the moderately dense, bistriate myelin staining of both areas and lower packing density of layer Va, especially in comparison to 7vm/31 (Figs. 8D,F, 12). In contrast, Galago area 7dm has somewhat larger pyramidal cells in layer Va than area 7vm, whereas macaque areas 7m and 31 both have small cells. It

is possible that area 7dm contains within it the homologues of macaque areas MIP and PIP in addition to 7m, as these areas all share a lightly to moderately stained, bistriate, appearance in myelin. The cortex posterior and ventral to area 7 in Galago. The parietal cortex extends posteriorly to about the level of the posterior tip of the IPS in Galago (Fig. 5).At this point, the area 7 complex is replaced by the extrastriate visual cortex (Allman and McGuiness, '83;Allman et al., '79). The cortex immediately posterior to the SPL is well myelinated,


488

Macaca

Galago

Fig. 8. Myeloarchitecture of the area 7 complex in coronal sections, arranged anterior to posterior. A-D: Macaca. E-F: Galago. G is a section from Galago taken through the extrastriate visual cortex immediately posterior to area 7. Scale bars = 2 mm.

with a broad, dense internal band and a somewhat thinner external band, as well as numerous radial fibers (Fig. 8G). The dense internal band is associated with the broad, cell-sparse appearance of layers Vb and VI in Nissl. This area corresponds in location to the dorsal visual area (D) described in Galago senegalensis by Allman et al. ('79). Area D is reported have an unusually large representation of the visual periphery, a characteristic which, along with its relatively medial location, has led to the suggestion that it is homologous to an area known as the medial visual area (M) in New World monkeys (Allman, '88; Allman and Kaas, '76) and as the parieto-occipital visual area (PO) in Old World monkeys (Colby et al., '88). Consistent with our observations of galago area D, Colby et al. noted that area

PO exhibits "numerous thick fibers in the lower layers which run parallel to the cortical surface." In Galago, area D is replaced posteriorly and ventrally by V2, which can be recognized in myelin by its numerous coarse radial fibers, a feature noted in Macaca by Gattass et al. ('81)'.

'In GaEago, area D extends from its border with area V2, on the medial surface, across the dorsolateral surface as far as the MT-V4 region (Allman et al., '79). By contrast, the presumptive homologues of area D in Aotus (area M) and Mucaca (area PO) are restricted to the medial surface of the hemisphere and are separated from the MT-V4 region by several intervening visual areas (e.g,,Allman and Kaas, '75; Maunsell and Newsome, '87; Van Essen, '85), which are evidently absent in Galago (Allman and McGuiness, '83; Allman et al., "79).

GALAGO PARIETAL AND TEMPORAL CORTEX Unlike Macaca, there is no deep lunate sulcus in Galago to mark the border of area V2 on the lateral surface of the hemisphere. Rather, most Galago crassicaudatus individuals possess a short indentation or dimple within the dorsal extrastriate region, known as the transverse occipital sulcus (OTrS) (Figs. 3 , 5 ) . Ventrally, the area 7 complex of Galago is bordered by the posterior cingulate area 23 (Figs. 5, 6). Area 23 in Galago is a narrow, poorly myelinated zone (Fig. 8F). Our Nissl observations confirm previous reports by Zilles et al. ('86) and Armstrong et al. ('86)that, whereas area 23 in anthropoid primates is granular and can be divided into several smaller zones, area 23 in Galago and other strepsirhines has a very poorly developed layer IV and cannot readily be subdivided (see also Bonin, '45; Vogt et al., '87; and Zilles et al., '79a,b).

TEMPORAL CORTEX Overview The temporal cortex of anthropoid primates is very diverse in structure and function, consisting of at least five major functional regions, each comprised of multiple architectonic subdivisions. The auditory cortex, including primary and association areas, occupies the most superior temporal cortex along the rim of the lateral sulcus (reviewed by Brugge, '82). The auditory region includes a posterior association area, the temporoparietal area (Tpt), which has particularly strong frontal connections (Kawamura and Naito, '84; Petrides and Pandya, '88). Polysensory cortex is found along the upper bank and fundus of the superior temporal sulcus and may extend for some distance onto the superior temporal gyrus (Baylis et al., '87; Bruce et al., '81). We refer to this region as ST. Most of the inferior temporal lobe is occupied by the higher order visual cortex, known as IT, which lacks obvious retinotopic organization and is involved in visual object discrimination and recognition (Gross et al., '81; Mishkin, '82). The posterior part of the temporal lobe contains several retinotopically organized, extrastriate visual areas, including the well-known middle temporal area, MT (Maunsell and Newsome, '87; Van Essen, '85). Finally, the most inferior and medial part of the temporal lobe contains the parahippocampal cortex, located adjacent to the allocortex of the hippocampal complex. The parahippocampal cortex, consisting of separate anterior and posterior regions, is thought to serve as a connectional link between higher order association neocortex and the hippocampus, relevant to memory processing (Van Hoesen, '82). In strepsirhines, only extrastriate visual areas and unimodal auditory areas have been identified in modern studies (Allman et al., '73, '79; Allman and McGuiness, '83; Brugge, '82). Our results suggest that Galago also possesses homologues of anthropoid higher order temporal regions, including Tpt, ST, IT, and the posterior parahippocampal areas. Auditory cortex; area Tpt. The auditory region of anthropoids is comprised of a primary area, Al, which lies along the rim of the lateral sulcus, a belt of auditory areas that surrounds Al, and a posteriorly situated association area, Tpt. Our main concern here is area Tpt; we consider other areas only briefly. The organization of A1 and the belt areas is believed to be similar in strepsirhines and anthropoids, based on microelectrode mapping studies in Macaca

489

and Aotus by Brugge and his colleagues (Brugge, '82; Imig et al., '77; Merzenich and Brugge, '73) and a brief report on Galago (Brugge, '82). Parcellation of this region with architectonic methods is difficult, although we have been able to identify several areas in Galago based on published descriptions of Aotus (Imig et al., '77) and Macaca (Galaburda and Pandya, '83; Pandya and Sanides, '73). These include A1 (the auditory koniocortex), as well as rostra1 (R), caudomedial (CM),and lateral (L) belt areas (Figs. 5,6, 13). In general, A1 and its surrounding belt areas can be distinguished from other temporal regions by their dense supragranular and granular layers and pale-staining, cellsparse layer V. However, the border of the auditory belt region with the ST cortex is often difficult to specify precisely on architectonic grounds. In macaques, auditory association area Tpt is located at the posterior end of the superior temporal gyms, at the junction of the auditory cortex, posterior parietal cortex, and extrastriate visual cortex (Fig. 4 A Galaburda and Pandya, '83; Leinonen et al., '80; Pandya and Sanides, '73). It covers the surface of the superior temporal gyrus and extends into adjacent parts of the superior temporal sulcus and lateral sulcus. As noted by the authors cited above and as can be seen in Figure 14A, macaque Tpt is characterized in cytoarchitecture by a columnar arrangement of the pyramidal laminae (111 and V); a thick layer IV, with an indistinct lower border owing to the intermingling of granule cells and pyramidal cells; a split layer V with a broad, light layer Vb; and a dense, dark-staining layer VI. The highly stratified ("eulaminate") appearance of Tpt is similar to that of the posterior parietal areas and permits one to distinguish Tpt from the auditory areas located more anteriorly (Galaburda and Pandya, '82). In Galago, the cortex located at the posterior tip of the superior temporal gyrus has cytoarchitectonic characteristics very similar to macaque Tpt (Fig. 14). The only clear difference that we can discern in the architecture of Tpt in these two primates is that the largest pyramidal cells are found in layer Va in Galago, whereas in Macaca pyramidal cells are nearly equal in size in layers I11 and V. As in macaques, Galago Tpt is located at the junction of the auditory, visual, and posterior parietal cortex (Figs. 5, 6C). In its posterior parts, Galago Tpt directly borders posterior parietal area 7a-1 on the hemispheric convexity; these areas can be distinguished by the thinner, darker layer VI of Tpt and its more markedly columnar appearance. Anteriorly, Tpt extends onto the dorsal bank of the posterior LS where it is separated from the parietal cortex by a very distinctive area with conspicuous dark, round pyramidal cells and a coarse, columnar appearance. This area is similar in architectonics and location to the retroinsular area (RI) of macaques (Pandya and Sanides, '73). ST and IT cortex: Overview. In the anthropoid Macaca, the ST and IT regions comprise an extensive region of temporal cortex. We include within the ST region the fundus and dorsal bank of the superior temporal sulcus (STS), at anterior and middle levels of the temporal lobe, as well as much of the superior temporal gyrus (STG) at the same levels. ST includes the so-called superior temporal polysensory cortex, which is found within the fundus and dorsal banks of the STS (Baylis et al., '87; Bruce et al., '81;

490


u A

after Brodmann, '09

(and von Bonin tk Bailey, '47)

A c

after Pandya & Seltzer, '82, Seltzer & Pandya, '80, '83

0

D

after Colby et al., '88, Ungerleider & Desimone, '82b, Van Essen, '85 Figure 9

GALAGO PARIETAL AND TEMPORAL CORTEX Desimone and Gross, '79), as well as the auditory association cortex, along the superior temporal gyrus (Galaburda and Pandya, '83; Seltzer and Pandya, '78). (The location of the border between polysensory and unimodal, auditory association cortex has not yet been established precisely.) The IT visual region occupies the ventral bank of STS and the inferior temporal convexity. Detailed cyto- and myeloarchitectonic studies by Seltzer and Pandya ('78) and correlative architectonic and microelectrode studies by Baylis et al. ('87)demonstrate that ST and IT each consist of multiple divisions (Fig. 4A,E). The following areas are located within the physiologically characterized ST polysensory region: area Ts, which covers the dorsal rim of STS as well as the STG (and which can be subdivided further); areas TAa and TPO, covering the dorsal bank of STS; and areas PGa and IPa, which occupy the broad, flat fundus of the STS and adjacent parts of its upper and lower banks. The IT visual region consists of areas TEa and TEm, occupying the ventral bank and rim of STS, with additional divisions of TE located on the inferior temporal convexity. Most individuals of Galago crassicaudatus do not possess a deep STS, having instead a dimple or broad depression in the corresponding part of the temporal lobe (Figs. 3,6B,C). It is evident nevertheless that this region shares distinctive architectonic characteristics with the macaque ST and IT cortex. It is not clear, however, that Galago possesses all the subdivisions of ST and IT which are present in anthropoids. Our interpretation of temporal cortex homologies is summarized in Table 3. ST and IT cortex: Macaca. We have been able to subdivide ST and IT cortex in macaques in a manner largely consistent with published accounts. In describing these areas, we begin at the border of the ST and IT domains, which is found where the ventral bank of the STS joins the fundus. The fundus of the STS serves as distinctive architectonic landmark, being occupied by thin, lightly myelinated cortex (Fig. 15A). This region is comprised of two areas, PGa and IPa, which belong to the ST domain. As described by Seltzer

491 TABLE 2. Proposed Homologies of Divisions of the Area 7 Complex in Macaca and Galago Mama

Galago

7b

7b la-1 la-m 7s 7dl ldm IVm

7a-1 la-m LIP, AIP VIP 7m 31

and Pandya ('78), IPa covers most of broad floor of the fundus, whereas PGa lies along the sulcus that marks the dorsal limit of the fundus. These areas are very similar architectonically, and we found it difficult to distinguish them consistently. Both areas stain lightly for myelin (in some cases extremely lightly), with mainly fine horizontal fibers and a few coarse radial fibers. In Nissl, layers IIIc, Va, and VI are dark in these areas and contain clusters of cells which are especially apparent at low magnification (Figs. 14,15B). PGa and IPa appear to differ chiefly in the size of deep layer I11 and layer Va pyramidal cells, which are larger in IPa, although the difference is not striking. Compared to the fundus, the cortex of the dorsal bank of STS, consisting of areas TPO and TAa, is thicker and more heavily myelinated, with a bistriate appearance (Fig. 15A). Area TPO, located deep in the sulcus where it sometimes occupies a small gyms, can be distinguished from TAa by its long radial fibers. Areas TPO and TAa do not differ strongly in Nissl, although they can be distinguished from PGa and IPa by the absence of cell clusters (Fig. 15B). Along the dorsal rim of the STS, area TAa is bordered by the Ts cortex, which is more heavily myelinated than TAa and has lighter, less cell dense, deep layers. We have not attempted to subdivide Ts in our macaque material; however, Pandya and Sanides ('73)have described three subdivisions. The ventral bank of the STS, which lies within the IT domain, includes areas TEa and TEm. TEa, situated internally, is nearly as lightly myelinated as the areas in the fundus (PGa and IPa), although diffuse external and internal bands, and long, fine vertical fibers, are visible (Fig. 15A). In Nissl, some large pyramidal cells are present in layer IIIc; cell clusters are absent (Fig. 15B). Area TEm is situated external to TEa, covering the ventral lip of the STS. TEm is more heavily myelinated than TEa, with a Fig. 9. Summary of published interpretations of area 7 and its subdivisions in Macaca and other Old World monkeys. A According to dense array of irregular vertical fibers (Fig. 15A).It also has Brodmann ('091, area 7 covers the inferior parietal lobule on the lateral a broad outer cell stratum with a prominent layer I11 surface and much of the medial surface of the parietal lobe. Subsequent packed with clusters of dark, rather small, pyramidal cells; authors have subdivided Brodmann's area 7. B: Vogt and Vogt ('14) layer N is thick, and layer V is broad and pale (Figs. 14, divided the IPL cortex into separate anterior and posterior areas, 15B). termed 7b and 7a, as did Bonin and Bailey ('471, who termed these areas Area TEm is replaced on the inferior temporal convexity P F and PG. In contrast to Brodmann, the medial parietal cortex was considered by Bonin and Bailey to be part of area 5 (or PE) rather than by additional divisions of TE. The border of TEm with the area 7. C: Pandya and Seltzer ('82; Seltzer and Pandya, '80, '83)divided convexity cortex is marked by a reduction in myelin density the area 7 complex extensively. They recognized the architectonic and a decrease in the prominence of layer I11 (Fig. 15A,B). distinctiveness of the cortex within the IPS (areas POa-e and POa-i) At middle and caudal levels of the temporal lobe, the TE and also affirmed the architectonic likeness of the medial parietal cortex convexity cortex is moderately well myelinated, with a thin (their area PGm) to the cortex of the inferior parietal lobule. (The IPS is depicted as open in this and the following figure.) D: Divisions of the external band, broad internal band, and long, fine, regularly area 7 complex which receive projections from extrastriate visual arrayed, radial fibers (Fig. 15A). This cortex has a laminate cortex. This schematic is based primarily on Colby et al. ('881, Ungerlei- appearance in Nissl, with a dense, well-demarcated layer der and Desimone ('82b),and Van Essen ('85). Colby et al. ('88) noted IV,and a split layer V with a particularly densely packed Va projections to zones in the fundus and medial bank of the intraparietal (Figs. 14, 15B). At rostral levels, however, the convexity sulcus (areas MIP and PIP), which were not previously known to be cortex becomes more lightly myelinated and has a thinner visual areas. They also noted connections between visual area PO and the medial dorsal parietal cortex (MPD), as did Cavada and Goldman- layer IV. This pattern of rostrocaudal variation has previRakic ('89a), consistent with the inclusion of medial parietal cortex ously been noted in Aotus by Weller and Kaas ('87) and in within the area 7 complex. Macaca by Seltzer and Pandya ('78) and Baylis et al. ('87).


492

Fig. 10. Cytoarchitecture of the area 7 complex: areas of the inferior parietal lobule (IPL) and parietal operculum. Scale bar = 500 pm.

The major difference among published studies is that in Macaca workers have formally recognized two areas rostromedially (TE, and TE,) and a single division caudally (TE,), whereas single rostral and caudal divisions were recognized in Aotus. In our Macaca material, we find it difficult to subdivide the rostromedial region, and therefore we recog-

nize single rostral and caudal divisions of the inferior temporal convexity, designated TEr and TEc (Fig. 4A). The poleward reduction in the myelination of IT cortex is paralleled by a reduction in myelin at rostral levels of the ST region (Seltzer and Pandya, '78). Moreover, the cortex which covers the temporal pole, area TG of Bonin and

493


Fig. 11. Myelo- and cytoarchitecture of areas 7a-m and 7a-1 in Macaca. In myelin (A), area 7a-m is distinguished by its coarse radial fiber bundles; 7a-1 has fine fibers and distinct external and internal bands. In Nissl (B),area 7a-m has a thicker layer IV than 7a-1, and larger pyramidal cells in the deep part of layer 111. Scale bar = 500 wm.

Bailey ('47),is very pale in myelin. TG is also distinguished by its thin layer IV and broad, poorly stratified deep layers. Our observations of TG are consistent with those published by Seltzer and Pandya ('78) and Weller and Kaas ('87). ST and IT cortex: Galago. We noted in Macaca that the cortex occupying the fundus of the STS is distinctive, owing to its light myelination. A similar lightly myelinated territory is present in the shallow central depression of the Galago temporal lobe, providing a point of reference for comparing the architectonic organization of these animals (Figs. 5, 6C-D). The lightly myelinated zone (LMZ)of Galago has a thin inner fiber plexus, an extremely faint external band, and a few coarse vertical fibers (Figs. 13, 16A). LMZ is, moreover, nearly as distinctive in Nissl as in myelin: layer V is split, and Va and VI are compact bands of dark, clustered neurons (Figs. 14, 16B). The cortex is thin overall, particularly at the middle and caudal levels of the temporal lobe. In some Galago sections we have examined, there is evidence of areal differentiation within LMZ. For example, the posteroventral part of LMZ appears to lack the dense clusters of cells present more anteriorly and dorsally (Fig. 16B). Subtle variations in myeloarchitecture can also be seen (Figs. 13B,C, 16A). However, we have not been able to consistently follow these variations through serial sections and therefore have not formally subdivided LMZ. Galago LMZ bears an obvious resemblance to the lightly myelinated STS areas of Macaca, specifically areas PGa and

IPa of the ST domain (compare Fig. 15 with Figs. 13 and 16). In Nissl, too, the clustering of cells in LMZ resembles that seen in PGa and IPa; this feature is absent in TEa and possibly in the ventral part of LMZ as well. These similarities suggest strongly that LMZ is homologous to area PGa andor IPa. LMZ may also contain the homologue of one of the inferotemporal divisions, TEa. One difference we have observed between the myelinpoor regions of Galago and Macaca is that the internal fiber band is better developed in Galago areas than in their presumptive Macaca homologues. This does not constitute a critical objection to homology, however, as bushbabies (compared to macaques) exhibit a relatively pronounced inner band over much of the temporal lobe (Figs. 13, 15, 16). A more significant difference is that we have not been able to clearly distinguish subdivisions of LMZ in Galago, which may indicate that Galago possesses fewer areas than Macaca. However, architectonic differentiation of this region in Macaca is subtle, and given that the LMZ is very narrow in Galago, it is possible that subdivisions exist which we have been unable to recognize. Galago LMZ is separated dorsally from the auditory belt by a narrow zone of thicker, more heavily myelinated cortex (Figs. 13A,B, 15), which presumably corresponds to the cortex of the dorsal bank of STS and STG in Macaca. This region is very difficult to subdivide architectonically in Galago. We therefore recognize only a single division of the


494

7s

7dl

7dm

7vm

Fig. 12. Cytoarchitecture of the area 7 complex: areas located within and near the intraparietal sulcus (IPS) and medial wall. Areas in Galago (above) are matched to their likely homologues in Macaca (below). Inferences about the homologies of sulcal areas (7s and LIP;

7dl and VIP) are based primarily upon myeloarchitectonic and positional similarities; these divisions do not hear a close resemblance in Nissl. Scale bar = 500 bm.

ST cortex dorsal to LMZ,termed area STd. In macaques, by comparison, the corresponding region of cortex consists of multiple areas: TPO, TAa, and several divisions of Ts. In contrast to the ST region, the cortex situated inferior to LMZ in Galago can be readily subdivided and the resulting divisions matched to specific areas of anthropoid IT cortex. Immediately inferior to LMZ,there is a narrow region of thick, relatively well myelinated cortex, with a dense array of irregular vertical fibers (Fig. 16A, see also Fig. 13B,C). In Nissl, this area has a dense, dark band of cells in deep layer I11 and broad, pale layers V and VI (Fig.

14). These characteristics are shared with macaque area TEm, which likewise is located adjacent to the lightly myelinated areas of the STS. In Galago, the cortex situated between TEm and the parahippocampal cortex (on the ventral surface) resembles the inferior temporal convexity cortex of anthropoid primates (TE). In Nissl, this cortex exhibits a well-demarcated layer IV, a split layer V with a dense, dark Va, and a dark compact layer VI (Fig. 14). In myelin, most of TE is quite well myelinated, with a broad internal band, thin external band, and fine radial fibers (Figs. 13B,C, 16A). As in macaques and owl monkeys,


495

Galago

Fig. 13. A series of myelin-stained coronal sections through the temporal lobe of Galago case G17L,arranged from anterior to posterior (A-C). Like most galagos, this individual lacks a deep superior temporal sulcus, having instead a broad shallow depression occupied by the

lightly myelinated zone (LMZ). LMZ resembles the cortex lying in the fundus of the macaque superior temporal suleus (see text and Fig. 15). Staining of areas TF and TH in C is partly artifactual. Scale bar = 2 mm.

however, the most rostral part of TE is poorly myelinated (Fig. 13A).We therefore recognize rostral (TEr) and caudal (TEc) divisions of this region in Galago, as inMacaca. As in anthropoids, the most rostral part of the superior temporal region and the temporal pole, as well as the rostral IT region, are very lightly myelinated in Galago. The fairly uniform, sparse myelination of this region makes architectonic differentiation of this region quite difficult, although the temporopolar area (TG) can usually be distinguished from surrounding areas quite readily in Nissl. Temporal extrastriate cortex. In anthropoids, there are several visuotopically organized areas which are located posterior to ST and IT at the temporo-occipital junction (Fig. 4E). The best known of these is MT, an area noted for its distinctively heavy myelination, a characteristic originally observed in owl monkeys by Allman and Kaas ('71). In macaques, combined electrophysiological,connectional, and architectonic investigations have localized MT in the posterior part of STS, along the lower bank and adjacent part of the fundus (Desimone and Ungerleider, '86; Van Essen et al., '81). Additional temporal visual areas have subsequently been identified by physiological and connectional techniques, and some of these have been characterized architectonically. One such area, located on the floor of the STS anterior and ventral to MT, is called FST (for "fundus of' the superior temporal sulcus" ; Desimone and Ungerleider, '86; Ungerleider and Desimone, '86a'b). FST is reported to be heavily myelinated, like MT, and micrographs presented by Ungerleider and Desimone ('86a) suggest that FST and MT are similar in cytoarchitecture as well. Anterior and dorsal to MT, the STS cortex contains a more

lightly myelinated zone in which the visual periphery is represented; this is considered to be the peripheral portion of the MT representation (MTp; Ungerleider and Desimone, '86a). MTp is bordered in turn by the medial superior temporal area (MST;Desimone and Ungerleider, '86; Maunsell and Van Essen, '83).An area with connections similar to MST has also been identified in New World monkeys (Weller et al., '84). MST is particularly germane t o this study, as it has strong reciprocal connections with the granular frontal cortex (Maunsell and Van Essen, '83; Weller et al., '84). MST has not been fully characterized architectonically, however, although it is reported to have both densely myelinated and more lightly myelinated parts (Ungerleider and Desimone, '86a). Two additional areas, V4 and V4t, lie posterior and lateral to MT on the lower bank of the STS (Ungerleider and Desimone, '86a). V4 is a zone of moderately dense myelination. Area V4t lies between MT and V4, forming a narrow zone of thin, lightly myelinated cortex. At present, connectional and physiological studies have identified only two divisions of temporal extrastriate cortex in strepsirhines, the middle temporal (MT)and dorsolateral (DL) visual areas, based on studies carried out in Galago senegalensis (Allman and McGuiness, '83; Allman et al., '73; Raczkowski and Diamond, '81; Wall et al., '82). There is considerable evidence (reviewed by Weller and Kaas, '85) that DL is homologous to area V4 of macaques, at least in part. In Galago crassicaudatus, we have identified a zone of thick, heavily myelinated cortex in the posterodorsal temporal lobe (Fig. 17A). It seems clear that this region includes


496

Fig. 14. Cytoarchitecture of the temporal cortex: area Tpt, the ST cortex (LMZ, IPa), and IT cortex (area TEc). Galago area LMZ is probably homologous to macaque area IPa, at least in part. Scale bar = 500 wn.

area MT. However, there is subtle variation in the Nissl architecture within the heavily myelinated zone. Specifically, there is a small anterior and ventral extension of cortex in which the deep part of layer 111is darker and more densely packed than in the posterior portion (Fig. 17B). This variation may represent minor architectonic heterogeneity within MT. Alternatively, it may indicate that Galago

possesses one or more densely myelinated visual areas anterior to MT, possibly homologous to FST or the densely myelinated part of MST in Macaca. It is important to note that the MT region of Galago can sometimes be identified in Nissl-stained material as well as in myelin, owing to its thick layer IV and broad, pale layer V, similar characteristics can be observed in Macaca (Figs.

497


Macaca

Fig. 15. Coronal sections through the superior temporal sulcus of Macaca stained for myelin (A) and Nissl (B), showing areas originally described by Seltzer and Pandya ('78; see also Baylis et al., '87). Dorsal is toward the top. Areal borders are more easily distinguished in myelin than in Nissl at this low magnification. The areas of the fundus and upper bank of the sulcus (IPa, PGa, TPO, TAa, TS) constitute the ST

region; they are known t o have polymodal sensory properties (Baylis et al., '87; Bruce et al., '81). The lower bank areas (TEa, TEm) are part of the IT visual region (Baylis et al., '87). Compare the myelin-poor cortex in the fundus (areas IPa and PGa) to area LMZ of Galago (Figs. 13,161. Scale bar = 1mm.

17B, 18).Moreover, MT often stands out as a distinct bulge or small gyrus in Galago (Figs. 6E, 17).Identification of MT in Nissl-stained material has been reported in other strepsirhine studies (Raczkowski and Diamond, '81; Zilles et al., '79a,b). The cortex immediately anterior to the MT region is much thinner and stains more lightly for myelin; this region may correspond to macaque MTp or to the lightly myelinated portion of area MST (Figs. 13C, 17A,F). MT is surrounded dorsally, ventrally, and posteriorly by a narrow band of thin, lightly myelinated tissue, which is bordered in turn by somewhat more densely stained cortex (Figs. 6E, 17A). These myeloarchitectonic zones resemble macaque areas V4t and V4, respectively. Parahippocampal cortex. In anthropoid primates, the parahippocampal cortex has been divided into anterior and posterior regions (Van Hoesen, '82). The anterior region

TABLE 3. Proposed Homologies of ST and IT Areas in Macaca and GaEago Macaca

Galago

Tc

-I

TAa TPO PGa IPa

STd

LMZ

(TEa?) TEm TEc TEr

TEm TEc TEr

consists of the entorhinal and perirhinal areas (areas 28 and 35 of Brodmann, '09; see especially Amaral et al., '87; Van Hoesen and Pandya, '75). The posterior hippocampal region consists of areas TF and TH (Van Hoesen, '82).

T.M.PREUSS AND P.S. GOLDMAN-RAKIC

498

Galago

The existence of entorhinal and perirhinal areas in strepsirhine primates has generally been noted (Brodmann, '08, '09; Le Gros Clark, '31; Zilles et al., '79a,b). The entorhinal cortex is easily recognized in Nissl, due to the presence of a cell-sparse band (lamina dissecans) separating the superficial and deep layers (e.g., Amaral et al., '87; Van Hoesen and Pandya, '75). The entorhinal cortex is also very distinctive in myelin, with a narrow, dark band of horizontal fibers superficially, and in some parts of the region, long, thick radial fibers (Amaral et al., '87). These myeloarchitectonic characteristics can be seen in both Galago and Macaca (Fig. 19A,B; see also Fig. 13). In contrast, the posterior parahippocampal areas, TF and TH, have not previously been demonstrated in strepsirhines. In Galago, it appears possible to identify these areas in Nissl- and myelin-stained sections taken immediately posterior to the entorhinal cortex. TH and TF are pale in myelin compared to neighboring areas 28 and TE (Fig. 19C,D). Fine horizontal fibers are visible in some sections; in others (particularly in lightly stained material), TF-TH appear nearly devoid of myelinated fibers. Cytoarchitectonically, the presence of large, dark-staining cells in the deep strata is distinctive of posterior parahippocampal cortex (Fig. 18).The lateral (TF) and medial (TH) divisions can be differentiated in Nissl: TF is thicker overall, with better defined laminae, including a granular layer Iv. These characteristics accord well with previous architectonic descriptions of TF and TH in anthropoid primates (GoldmanRakic et al., '84;Weller and Kaas, '87).

DISCUSSION The purpose of this study was to directly compare the cyto- and myeloarchitectonic organization of the parietal and temporal association cortex in Galago and Macaca in order to identify areal subdivisions which are likely to be homologous. The macaque parieto-temporal cortex is currently known to consist of a large number of subdivisions (e.g., Maunsell and Newsome, '87; Pandya and Seltzer, '82; Seltzer and Pandya, '78, '80; Van Essen, '851, far more than were recognized by early architectonic investigators (e.g., Bonin and Bailey, '47; Brodmann, '091, although few of these divisions have as yet been demonstrated in Galago, or in related strepsirhine primates. Our results indicate that the Galago parieto-temporal cortex can be also divided into a large number of areas. Among these are divisions which resemble architectonically the higher order association areas and regions of Macaca, including multiple divisions of parietal area 7, auditory association area Tpt, ST polysensory cortex, IT visual Fig. 16. Horizontal sections through the broad, shallow superior cortex, and posterior parahippocampal areas TF and TH. temporal sulcus of Galago stained for myelin (A) and Nissl (B). The areal organization of the parietal-temporal cortex Anterior is toward the top. Because the temporal lobe has a rather may not be identical in Galago and Macaca, however. We vertical orientation in galagos (see Fig. 51, horizontal sections in these animals are nearly comparable to coronal sections in macaques. Galago have not identified as many areas in Galago as in Macaca, temporal cortex resembles that of Mucaca in several respects, although suggesting that additional cortical areas evolved in the we have not able to distinguish as many subdivisions. Galago possesses anthropoids; the disparity is especially notable for the ST a lightly myelinated zone (LMZ), similar to the myelin-poor region in region of temporal cortex. However, the difference may also the fundus of the macaque STS. LMZ also resembles macaque areas IPa and PGa in Nissl, with clusters of large, dark cells in the deep layers (see be explained to some extent by the greater difficulty of also Fig. 13). Area STd, the portion of the ST complex that separates distinguishing areas architectonically in Galago compared the LMZ from the auditory belt cortex (Aud), is very narrow and to Macaca. difficult to subdivide in Galago; the corresponding part of macaque Galago and Macaca differ in additional respects. For one, cortex consists of at least three areas (TPO, TAa, and Ts). LMZ is the location of areas with respect to sulci in the parietal lobe bordered posteriorly and inferiorly by IT cortex (area TE and its subdivisions).One part of IT stands out due to its denser myelination differs among these taxa. There also appear to be some general differences in cortical histology which span much of and dark-staining layer I11 cells; this is probably homologous to the parietal and temporal lobes. macaque area TEm. Scale bar = 1mm.


499

Fig. 17. Adjacent sections showing the (A) myelo- and (B)cytoarchitecture of the extrastriate visual region of Galago temporal cortex. (B is at higher magnification than A.) These are horizontal sections taken through the dorsal part of the temporal lobe; anterior is toward the top. This region contains a zone of thick, heavily myelinated cortex which corresponds at least in part to visual area MT; this cortex also has a thick layer IV (indicated in brackets in B). However, there is some cytoarchitectonic variation within the heavily myelinated region, specifically, the anterior part has larger deep 111 pyramidal cells. This

anterior zone may be part of MT or it may be a separate area, possibly FST or the densely myelinated part of area MST. Anteriorly, the heavily myelinated region is separated from auditory cortex auditory areas A1 and L by thin, relatively lightly myelinated cortex, which may correspond to the macaque territories designated as MST or MTp. Posteriorly, MT is bordered by an additional zone of thin, relatively lightly myelinated cortex, which probably corresponds to macaque area V4t. For descriptions of macaque visual areas surrounding MT, see Desimone and Ungerleider ('86) and Ungerleider and Desimone ('86a,b).

PARIETAL AREA 7 COMPLEX

comparative studies of the posterior cingulate region by Zilles et al. ('86) and Armstrong et al. ('86). The interpretation of homologies for the remaining, more medial divisions of the Galago area 7 complex (7s, 7dl,7dm) is less straightforward. These divisions probably include homologues of macaque areas which lie along the lateral bank of the intraparietal sulcus (AIP, LIP, VIP) and on the medial surface (7m), as other macaque areas have been accounted for. However, the Galago areas occupy the fundus and medial bank of the IPS and the adjacent SPL, territories which are occupied by area 5 , rather than area 7, in Macaca. As a result, these divisions cannot be matched to any parts of Macaca area 7 based solely on common location relative to the IPS. Moreover, the galago areas do not bear a particularly close cytoarchitectonic resemblance to the IPS and medial areas of macaques. In contrast, there are similarities in the pattern of myeloarchitectonic variation across the more medial parts of the area 7 complex in Galago and Macaca. This evidence suggests that galago area 7s is homologous to macaque area LIP (and possibly also AIP), area 7dl to VIP, and area 7dm to 7m. Comparison toprevious strepsirhine studies. Most prior investigations of the strepsirhine parietal cortex have dealt exclusively with Nissl architecture. In general, these ac-

Comparative architectonics and areal organization. In Old World anthropoid primates such as Macaca, the parietal area 7 of Brodmann ('05, '09) can be subdivided extensively based on differences in architectonics, connectivity, and functional properties (Andersen, '87, '88, '89; Cavada and Goldman-Rakic, '89a,b; Pandya and Seltzer, '82). We have been able to identify in Macaca most of the architectonic divisions described in the literature and have proposed two additional units: a medial division of area 7a (7a-m), located along the rim of the IPS, and an anterior intraparietal area (AIP). A major finding of the present study is that area 7 can also be subdivided in Galago. It is possible to suggest homologues for these subdivisions in Macaca. Similarities are most evident in the IPL region: Galago possesses four areas in this region, which can be matched to the IPL areas ofMacaca (7b, 7a-1,7a-m, Top) based on local variations in pyramidal cell size, in the thickness of layer IV, and in the arrangement of myelinated fibers. Also well matched are medial parietal area 7vm of Galago and area 31 of Macaca: both are lightly myelinated, have small pyramidal cells, and are located immediately dorsal to posterior cingulate cortex. The homology of 7vm and 31 is supported by recent


500

Fig. 18. Cytoarchitecture of the temporal cortex: visual area MT and posterior parahippocampal areas TF and TH. In area MT, note the much greater density of layer IV in Macaca compared to Galago; in this instance, both section were cut at 40 Km. Scale bar = 500 &m.

counts are in agreement with our localization of area 7 in Galago, covering both the IPL and SPL, with a division resembling area 5 (termed Sp, in our system) located more anteriorly. Such a parcellation was proposed by Brodmann ('08, '091, who examined the strepsirhines Lemur, Propith-

ecus, Perodicticus, and Loris, and by Diamond ('82) and Zilles et al. ('79a,b) for Galago and Microcebus. Only Le Gros Clark ('31), in Microcebus, suggested a macaque-like division of parietal cortex into a dorsal area 5 and a ventral area 7.

501


Macaca

Galago

Fig. 19. Myeloarchitecture of the anterior (A,B) and posterior (C,D) parahippocampal cortex. The anterior parahippocampal cortex is comprised of the entorhinal(28)and perirhinal(35) areas. Areas TF and TH constitute the posterior parahippocampal region. Scale bars = 2.5 mm.

None of the aforementioned studies distinguished subdivisions within area 7. In fact, Bonin ('45) concluded that virtually the entire parietal and temporal cortex of Galago is architectonically uniform. The electrophysiological and connectional information available for strepsirhines, although very limited, is consistent with our localization of area 7 in these animals. Allman et al. ('79) recorded units in the posterior parietal region of Galago senegalensis having large, ill-defined visual receptive fields, similar to units in the area 7 complex of anthropoids. Some of these units were found along the dorsal shoulder of the hemisphere, corresponding to the SPL. Also, lesion-degeneration studies by Atencio et al. ('75) and Glendenning et al. ('75) in Galago provide evidence for connections between the posterior parietal cortex and a thalamic region which appears to include the medial pulvinar (PM), a nucleus which has strong connections with the area 7 complex in anthropoids (e.g., Asanuma et al., '85; Weber andYin, '84; Yeterian and Pandya, '85). We have obtained similar results with injections of tritiated amino acids in the Galago area 7 complex (Preuss and Goldman-Rakic, unpublished observations). There is one published study which provides information about the subdivisions of area 7 in strepsirhines. Wall et al. ('82) injected tritiated amino acids into area MT in Galago senegalensis and found a discrete strip of labeling corresponding approximately in location to the IPS areas (7s and 7dl) of G. crassicaudatus. (The correspondence can at best be approximate, because the lissencephalic G. senegalensis lacks a deep IPS.) This result is of interest because in Macaca, area MT projects to intraparietal area VIP (Maunsell and Van Essen, '83; Ungerleider and Desimone, '86b),

the area which we have suggested is homologous to galago area 7dl. The pattern of parieto-frontal projections in Galago, described in a subsequent work (Preuss and GoldmanRakic, '91b), provides additional support for our interpretation of area 7 homologies. For example, we found that Galago area 7b has a particularly strong projection to premotor cortex and specifically to ventral premotor areas; this is consistent with the connections of area 7b in Macaca (Cavada and Goldman-Rakic, '89a,b). An injection of the Galago superior parietal lobule and medial parietal region, involving areas 7dm and 7vm (the suggested homologues of macaque areas 7m and 311, produced much less premotor labeling (which was concentrated dorsally) and dense labeling of granular frontal cortex. A similar distribution of label was obtained after injection of area 7m in Macaca by Cavada and Goldman-Rakic ('89b). In contrast, the SPL cortex of Macaca, area 5, projects densely to premotor cortex but does not project to the granular frontal cortex (Petrides and Pandya, '84). Our connectional results are therefore consistent with the view that Galago SPL is occupied by part of the area 7 complex rather than by area 5.

TEMPORAL CORTEX One of the most distinctive characteristics of the primate brain is its enormous temporal lobe, separated from frontal and parietal cortex by the deep lateral (Sylvian) fissure. This is an ancient characteristic: the earliest fossil endocasts of primate brains (approximately 50 million years old) possess remarkably large, bulbous temporal lobes

502 (Gurche, '82; Radinsky, '70). The expansion of the temporal lobe has generally been linked to the elaboration of visual areas (Allman, '77, '82; Diamond, '73; Glendenning et al., '75; Harting et al., '72). However, anthropoid temporal cortex possesses auditory, polysensory, and parahippocampal areas, in addition to strictly visual areas. Many of these areas, including auditory area Tpt, the superior temporal polysensory areas, and the posterior parahippocampal areas, (TFITH) have not previously been identified in strepsirhines. Moreover, one major component of visual cortex, the inferotemporal (IT) cortex, has not been clearly identified in strepsirhines. Our results suggest that each of these cortical regions is present in Galago, although galagos may not possess every areal subdivision of temporal cortex present in macaques. Auditor# association area Tpt. Electrophysiological studies of the Galago auditory region have localized the primary auditory cortex and a belt of surrounding auditory areas, similar to those identified in anthropoids (Brugge, '82). In anthropoids, however, an additional auditory area, Tpt, has been localized at the junction of the superior temporal gyrus with the parietal lobe (Leinonen et al., '80; Galaburda and Pandya, '83; Pandya and Sanides, '73). Tpt is easily identified in the same location in Galago, where it is distinguished from other auditory areas by its distinct cellular columns and clearly demarcated laminae, as in Macaca. In the literature on strepsirhine architectonics, only Zilles et al. ('79a,b) have delineated an area which corresponds approximately in location to Tpt (their area Te 2.11, although they did not suggest homology with Tpt. Among auditory areas, Tpt appears to have particularly strong connections with granular frontal cortex, as judged from the results of Kawamura and Naito ('84), and it is therefore of special interest from the standpoint of frontal lobe evolution and function. The microelectrode recording study of Leinonen et al. ('80) suggests that Tpt may be an important source of sound-localization and head-movement information for the frontal lobe. In macaques, Tpt projects specifically to the frontal eye field region of arcuate cortex (Petrides and Pandya, '88), where neurons with auditory receptive fields have been identified (Azuma and Suzuki, '84; Russo and Bruce, '89; Vaadia et al., '86). ST and IT. These regions are of considerable interest as higher order or integrative cortical domains. The several areas of the ST cortex, which receive inputs from the auditory, somatosensory, and visual cortex (Seltzer and Pandya, '781, have polymodal response properties and are thought to be involved in the analysis of the spatial location and movement of stimuli (Baylis et al., '87; Bruce et al., '81). The IT visual cortex, which also consists of multiple divisions (Sanides and Pandya, '78; Weller and Kaas, '87), is many synapses distal to the primary visual cortex (Desimone et al., '80; Weller and Kaas, '85, '871, and physiological and behavioral studies demonstrate that this region is involved in object discrimination and recognition (for reviews, see Gross et al., '81, and Mishkin, '82). Cells selective for faces are found in the IT region, although part of the ST region has face cells as well (Baylis et al., '87; Bruce et al., '81; Perret et al., '82). Our architectonic evidence suggests that at least some of the ST divisions of Macaca are present in Galago. In Macaca, the cortex in the fundus of the superior temporal sulcus is lightly myelinated compared to neighboring tissue. This territory includes areas PGa and IPa of the ST complex and area TEa of the IT complex. Galago crassicau-

T.M. PREUSS AND P.S. GOLDMAN-RAKIC datus possesses a similar lightly myelinated zone (LMZ) in the shallow depression that corresponds to the superior temporal sulcus in this species. Furthermore, the Nissl architecture of LMZ also resembles macaque areas PGa and IPa. In our material it is unclear whether Galago possesses all of the lightly myelinated areas present in Macaca, as we were not able to subdivide LMZ consistently across a series of sections. This region is also difficult to subdivide in Macaca, however. Differences between Galago and Macaca are more apparent in the cortex immediately dorsal to the LMZ, that is, the region of ST cortex which separates LMZ from the auditory cortex proper. This is a very narrow strip of tissue in Galago, which we were unable to subdivide. By contrast, the corresponding part of macaque ST cortex is extensive, covering the dorsal bank of the superior temporal sulcus and much of the superior temporal gyrus, and consists of at least three areas (TPO, TAa, and Ts). It is possible, therefore, that the dorsal ST region of Macaca possesses areas not found in Galago. Previous studies of strepsirhine cortex have distinguished areas which correspond approximately in location to the ST cortex delineated here, for example, area Te 2.2 in the Galago and Microcebus maps of Zilles et al. ('79a,b),and area Ta of Raczkowski and Diamond ('80) in Galago, although the specific architectonic resemblance of these areas to anthropoid superior temporal sulcal cortex was not noted. Raczkowski and Diamond ('80) also demonstrated connections between area Ta and the medial pulvinar nucleus, consistent with reports of connections between ST and pulvinar in Macaca (Burton and Jones, '76; Trojanowski and Jacobson, '76). Ventral to LMZ, the cortex of the Galago temporal lobe is architectonically similar to anthropoid inferotemporal cortex. The most dorsal of the IT divisions in Galago is a thick, well-myelinated zone, which is probably homologous to Macaca area TEm (Seltzer and Pandya, '78). Posteroventral to TEm, Galago temporal cortex has a well-developed granular layer, a densely packed layer Va, and a bistriate pattern of myelinated fibers; the density of myelin is reduced anteriorly, toward the temporal pole. These architectonic characteristics, and the anteroposterior differences in myelination, are consistent with anthropoid IT cortex (Seltzer and Pandya, '78; Weller and Kaas, '87). Again, it is not clear whether Galago possesses as many divisions of IT cortex as anthropoids, however, as we were not able to recognize all the divisions of IT cortex that have been distinguished in Macaca by Seltzer and Pandya ('78) and Baylis et al. ('87). Most previous architectonic studies in strepsirhines delineated areas similar in location to the IT areas of Galago. Brodmann ('08, '09) recognized areas 21 and 20 in the ventral temporal cortex of strepsirhines and anthropoids but was not certain that these areas are homologous across taxa. Le Gros Clark ('31) and Zilles et al. ('79a,b) divided the ventral temporal cortex of Microcebus and Galago in a manner similar to Brodmann. Also, area Tv of Raczkowski and Diamond ('80) in Galago corresponds approximately in location to IT cortex as reported here. Apart from architectonics, information bearing on the presence of IT cortex in strepsirhines is limited and ambiguous. The best evidence that IT is present in strepsirhines is the demonstration by Wall et al. ('82) of a projection from area V4 to the ventral temporal lobe in Galago; in anthropoids, there is a major projection from V4 to posterior IT cortex (Desimone et al., '80; Weller and Kaas, '85, '87). In


503

contrast, macaque IT has very distinctive physiological sections were, in general, slightly thicker for macaques properties: neurons have large receptive fields that usually than galagos (40 km versus 35 Fm), it seems unlikely that include the fovea and often respond preferentially to com- this could account for the difference (see especially Fig. 18). plex visual stimuli; the region lacks obvious retinotopic h a s ('82) has previously noted the lower packing density of organization (Gross et al., '81). A comparable region has not area 3b in Galago, compared to anthropoids. These architecyet been demonstrated in physiological explorations of the tonic variations suggest that the laminar organization of GaEago cortex (Allman and McGuiness, '83). Additionally, connections may differ between strepsirhines and anthroNewsome and Allman ('80) found that the IT cortex of the poids, an expectation borne out in our study of Galago owl monkey (Aotus)has much denser callosal connections cortico-frontal connectivity (Preuss and Goldman-Rakic, than the ventral temporal region of Galago. Results such as '91b). these suggest that if IT is present in strepsirhines, its Evolution of primate parietal and temporal functional properties may differ from anthropoid IT. This would not be surprising, given that the strepsirhine visual cortex system has been adapted to nocturnal conditions, whereas This study provides evidence that many divisions of anthropoids (with the sole exception of the nocturnal Aotus, parietal and temporal cortex are common to the strepwhich is evidently derived from a diurnal ancestor) possess Galago and the anthropoid Macaca, and presumsirhine specialization of the fovea for fine discrimination and color ably were present in the common ancestor of these privision under diurnal conditions (Allman, '77; Casagrande mates. However, we were able to delineate more cortical and DeBruyn, '82; Martin, '90; Pariente, '79). divisions in Macaca than in Galago. This raises the possibilIn addition to IT, we have been able to tentatively ity that anthropoids evolved additional parietal-temporal identify several extrastriate visual areas in our Galago areas during their phylogenetic history. We reached very architectonic material, previously known from electrophyssimilar conclusions regarding the evolution of the granular iological studies (Allman and McGuiness, '83; Allman et al., frontal cortex: macaques appear to possess more areas than '79). These include V2, V4 (also known as DL), D, and MT. galagos (Preuss and Goldman-Rakic, '91a). MT is bordered along its posterior aspect by a zone of thin, The case for additional areas in the parietal-temporal relatively lightly myelinated cortex which may correspond cortex is less strong than for the granular frontal cortex, to Macaca area V4t (Ungerleider and Desimone, '86a). however. In the frontal cortex, we could be specific about Posterior parahippocampal cortex. I n anthropoids, which areas are unique to macaques, because at least some parahippocampal areas TH and TF are found posterior to of these areas are very distinctive architectonically, namely, entorhinal cortex and medial to IT cortex. Their Nissl the myelin-poor areas of the principal sulcus. In the parietal appearance is very distinctive, with large, densely packed and the temporal cortex, we were not able to identify any neurons predominating in the deep layers (e.g., Goldman- particular architectonically distinctive area that was clearly Rakic et al., '84; Weller and Kaas, '87). We have identified present in one primate and absent in the other, although areas with these architectonic characteristics in a compara- the total number of divisions in Galago was less than for ble location in Galago. These areas appear to occupy a very Macaca. We therefore cannot exclude the possibility that small region in Galago (Fig. 5 ) , both in absolute terms and this difference is more apparent than real: the architectonic relative to the size of entorhinal cortex, which may explain distinctions between adjacent areas of cortex (particularly why they have not been noted in previous strepsirhine the temporal cortex) are in some cases very minor, and as a studies. By contrast, TH and TF appear to be larger relative consequence it may be easier to delineate areas in the to the entorhinal region in Macaca (Fig. 5; see also Fig. 1of large-brained Macaca than in the small-brained Galago. Van Hoesen, '82). This suggests that the posterior parahip- Nevertheless we consider it likely that the dorsal part of the pocampal region, a region implicated in memory processes ST cortex underwent evolutionary elaboration In anthro(Goldman-Rakic, '87a; Goldman-Rakic et al., '84; Van poids: this region is narrow and apparently poorly differenHoesen, '82), may have expanded during anthropoid evolu- tiated in Galago but broad and well differentiated in tion. Macaca. Whereas our evidence suggests that the strepsirhine General differences in cytoarchitectonic primate Galago and the anthropoid Macaca share many organization divisions of the higher order parietal-temporal cortex, it is Whereas it is apparent that Galago and Macaca evince an open question whether homologous areas exist in nonmany similarities of cortical areal organization, we have primate mammals. As a rule, it has proven difficult to noted consistent differences in the laminar organization of identify homologous cortical divisions across mammalian cortex in these taxa, differences which transcend areal orders, excepting the primary sensory areas and immediboundaries and which extend over much of the posterior ately surrounding areas (&as, '87). Among the parietal cerebrum. One difference is in the size distribution of and temporal areas, homologues of the ST polysensory pyramidal cells. In most Macaca areas, there is a prominent cortex, IT visual cortex, and posterior parahippocampal band of pyramidal cells in the deepest part of layer 111, i.e., areas (TFITH) have not been clearly identified in nonsublayer IIIc; this stratum often contains the largest primates. Evidence reviewed by Olson and Lawler ('87) and pyramidal cells in a given area. In Galago, layer I11 exhibits Kolb and Walkey ('87) suggests that carnivores and rodents less obvious stratification by cell size, and the largest may possess a homologue of area 7, although there is little pyramidal cells are generally in layer V. Diamond et al. ('85) indication that area 7 in these animals is comprised of a have made similar observations regarding the primary large number of subdivisions, as it is in primates. Therefore, the possibility exists that the posterior cortivisual cortex of Galago and anthropoids. A second difference pertains to the density of granule cells in layer IV, cal areas described in this study are for the most part which appears to substantially higher in Macaca than in primate specializations. There is evidence that primates Galago. Whereas it is the case that our photographed possess unique areas of the granular frontal cortex as well


504

(Preuss and Goldman-Rakic, '91a). It is interesting that many of these higher order association areas share connections with a single thalamic nucleus, the medial division of the superior pulvinar, also known as the medial pulvinar (PM). In Macaca, the connections of PM (reviewed by Goldman-Rakic, '88) include the granular frontal cortex, parietal area 7, ST cortex, IT cortex, posterior parahippocampal areas, and posterior cingulate cortex; PM has at least some of these connections in Galago also (Preuss and Goldman-Rakic, '87; Raczkowski and Diamond, '80, '81). To our knowledge, there is no thalamic nucleus in nonprimates that has a comparable pattern of connections. This is noteworthy in view of suggestion that the pulvinar (and the superior pulvinar in particular) underwent great expansion in primate evolution, with concomitant addition of new divisions (Diamond, '73; Glendenning et al., '75; Harting et al., '72; Le Gros Clark, '32).

ACKNOWLEDGMENTS This is Publication #510 of the Duke University Primate Center. Our research was supported by NIMH grants 09146 and 38546 and by NSF grant BNS-8318167.

LITERATURE CITED Allman, J.M. (1977) Evolution of the visual system in the early primates. In J.M. Sprague and A.N. Epstein (eds): Progress in Psychology and Physiological Psychology, Vol. 7. New York Academic Press, pp. 1-53. Allman, J.M. (1982) Reconstructing the evolution of the brain in primates through the use of comparative neurophysiological and neuroanatomical data. In E. Armstrong and D. Falk (eds): Primate Brain Evolution. New York: Plenum Press, pp. 13-28. Allman, J.M. (1988)Variations in visual cortical organization in primates. In P. Rakic and W. Singer (eds): Neurobiology of Neocortex. Chichester: John Wiley & Sons, pp. 285-295. Allman, J.M., and J.H. Kaas (1971) A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus triuirgatus). Brain Res. 31.85-105. Allman, J.M., and J.H. Kaas (1976) Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. Science 191.572-575. Allman, J.M., and E. McGuiness (1983) The organization of cortical visual areas in a strepsirhine primate, Galago senegalensis. SOCNeurosci. Abstr. 9:957. Allman, J.M., C.B.G. Campbell, and E. McGuiness (1979) The dorsal third tier area in Galago senegalensis. Brain Res. 179:355-361. Allman, J.M., J.H. Kaas, and R.H. Lane (1973) The middle temporal visual area (MT) in the bushbahy, Galago senegalensis. Brain Res. 57:197-202. Amaral, D.G., R. Insausti, and W.M. Cowan (1987) The entorhinal cortex of the monkey: I. Cytoarchitectonic organization. J. Comp. Neurol. 264t326355. Andersen, R.A. (1987) Inferior parietal lobule function in spatial perception and visuomotor integration. In V.B. Mountcastle, F. Plum and S.R. Geiger (eds): Handbook of Physiology-The Nervous System, Vol. V. Bethesda: Am. Physiol. SOC.,pp. 483-518. Andersen, R.A. (1988) Visual and visual-motor functions of the posterior parietal cortex. In P . Rakic and W. Singer (eds): Neurobiology of Neocortex. Chichester: John Wiley & Sons, pp. 285-295. Andersen, R.A. (1989) Visual and eye movement functions of the posterior parietal cortex. Ann. Rev. Neurosci. 12377-403. Armstrong, E., K. Zilles, G. Schlaug, and A. Schleicher (1986) Comparative aspects of the primate posterior cingulate cortex. J. Comp. Neurol. 253.539-548. Asanuma, C., R.A. Andersen, and W.M. Cowan (1985) The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: Divergent cortical projections from cell clusters in the medial pulvinar nucleus. J. Comp. Neurol. 241r357-381. Atencio, F.W., I.T. Diamond, and J.P. Ward (1975) Behavioral study of the visual cortex of Galago senegalensis. J. Comp. Physiol. Psychol. 89:11091135.

Azuma, M., and H. Suzuki (1984) Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey. Brain Res. 298t343-346. Baylis, G.C., E.T. Rolls, and C.M. Leonard (1987) Functional subdivisions of the temporal lobe neocortex. J. Neurosci. 7:330-342. Bonin, G. von (1945) The Cortex of Galago. Urhana, IL: Univ. of Illinois. Bonin, G. von, and P. Bailey (1947) The Neocortex of Macaca mulatta. Urhana: Univ. of Illinois Press. Brodmann, K. (1905) Beitrage zur histologisichen Lokalisation der Grosshirnrinde. 111.Mitteilung: Die Rindenfelder der niederen M e n . J. f. Psych. u. Neurol. 4:177-226. Brodmann, K. (1908) Beitrage zur histologisichen Lokalisation der Grosshirnrinde. VII. Mitteilung: Die cytoarchitektonische Cortexgliederung der H a l b d e n (Lemuriden). J. f. Psych. u. Neurol. 10.287-363. Brodmann, K. (1909) Vergleichende Lokalisationslehre der Grosshirnrhinde. Leipzig: Barth. Bruce, C., R. Desimone, and C.G. Gross (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46t369-384. Brugge, J.F. (19821Auditory cortical areas in primates. In C.N. Woolsey (ed): Cortical Sensory Organization. Vol. 3. Multiple Auditory Areas. Clifton, NJ: Humana, pp. 59-70. Burton, H. Second somatosensory cortex and related areas. In E.G. Jones and A. Peters (eds): Cerebral Cortex. Vol. 5. Sensory-Motor Areas and Aspects of Cortical Connectivity. New York: Plenum Press, pp. 31-98. Burton, H., and M. Carlson (1986) Second somatic sensory cortical area (SII) in a prosimian primate, Galago crassicaudatus. J. Comp. Neurol. 247.200-220. Burton, H., and E.G. Jones (1976) The posterior thalamic region and its cortical projection in New World and Old World monkeys. J. Comp. Neurol. 168t249-302. Carlson, M. (1985) Significance of single or multiple cortical areas for tactile discrimination in primates. In: A.W. Goodwin and I. Darian-Smith (eds): Hand Function and Neocortex. (Exp. Brain Res., Suppl. 10.) Berlin: Springer, pp. 1-16. Carlson, M., and K.A. Fitzpatrick (1982) Organization of the hand area in the primary somatic sensory cortex (SmI) of the prosimian primate, Nycticebus coucang. J. Comp. Neurol. 254:280-295. Carlson, M., and C. Welt (1980) Somatic sensory cortex (SmI) of the prosimian primate Galago crassicaudatus: Organization of mechanoreceptive input from the hand in relation to cytoarchitecture. J. Comp. Neurol. 189:249-271. Carlson, M., and C!. Welt (1981) The somatosensory cortex SmI in prosimian primates. In C.N. Woolsey (ed): Cortical Sensory Organization. Vol. 1. Multiple Somatic Areas. Clifton, NJ: Humana Press, pp. 1-27. Casagrande, V.A., and E.J. DeBruyn (1982) The Galago visual system: Aspects of normal organization and developmental plasticity. In D.E. Haines (ed): The Lesser Bushbaby (Galago) as a n Animal Model: Selected Topics. Boca Raton, FL: CRC Press, pp. 137-168. Cavada, C., and P.S. Goldman-Fhkic (1989a) Posterior parietal cortex in rhesus monkey. I: Parcellation of areas based on distinctive limbic and sensory cortico-cortical connections. J. Comp. Neurol. 287:393421. Cavada, C., and P.S. Goldman-Rakic (1989b) Posterior parietal cortex in rhesus monkey. 11: Evidence for segregated cortico-cortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287:422445. Colhy, C.L., R. Gattass, C.R. Olson, and C.G. Gross (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J. Comp. Neurol. 2 6 9 3 9 2 4 1 3 . Desimone, R., and C.G. Gross (1979) Visual areas in the temporal cortex of the macaque. Brain Res. 178:363-380. Desimone, R., and L.G. Ungerleider (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J. Comp. Neurol. 248: 164-189. Desimone, R., J. Fleming, and C.G. Gross (1980) Prestriate afferents to inferior temporal cortex: An HRP study. Brain Res. 184t41-55. Diamond, I.T. (1973) The evolution of the tectal-pulvinar system in mammals: Strcutural and hehavioural studies of the visual system. Symp. Zool. SOC. Lond. 332205233. Diamond, I.T. (1982) The functional significance of architectonic subdivisions of the cortex: Lashley's criticism of the traditional view. In J. Orhach (ed): Neuropsychology After Lashley. Hillsdale, N J Lawrence Erlbaum, pp. 101-136. Diamond, I.T., M. Conley, K. Itoh, and D. Fitzpatrick (1985) Laminar organization of geniculocortical projections in Galago senegalensis and Aotus triuirgatus. J. Comp. Neurol. 242.584-610,

GALAGO PARIETAL AND TEMPORAL CORTEX Friedman, D.P., E.A. Murray, J.B. O'Neill, and M. Mishkin. (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch. J. Comp. Neurol. 252:323-347. Galaburda, A.M., and D.N. Pandya (1982) Role of architectonics and connections in the study ofprimate brain evolution. In E. Armstrong and D. Falk (eds): Primate Brain Evolution. New York: Plenum Press, pp. 203-2 16. Galaburda, A.M., and D.N. Pandya (1983) The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey. J. Comp. Neurol. 221:169-184. Gallyas, F. (1979) Silver staining for myelin by means of physical development. Neurol. Res. 1203-209. Gattas, R., C.G. Gross, and J.H. Sandell (1981) Visual topography of V2 in the macaque. J. Comp. Neurol. 201:519639. Glendenning, K.K., J.A. Hall, I.T. Diamond, and W.C. Hall (1975) The pulvinar nucleus of Galago senegalensis. J. Comp. Neurol. 161:419456. Goldman-Rakic, P.S. (1987a) Circuitry of primate prefrontal cortex and the regulation ofbehavior by representational memory. In V.B. Mountcastle, F. Plum, and S.R. Geiger (eds): Handbook of Physiology-The Nervous System, Vol. 5. Bethesda: Am. Physiol. SOC.,pp. 373-417. Goldman-Rakic, P.S. (1987b) Motor control function of the prefrontal cortex. In R. Porter (ed): Motor Areas of the Cerebral Cortex. CIBA Found. Symp. 132. London: CIBAFound., pp. 187-200. Goldman-Rakic, P.S. (1988) Topography of cognition: Parallel distributed networks in primate association cortex. Ann. Rev. Neurosci. 11:137-156. Goldman-Rakic, P.S., L.D. Selemon, and M.L. Schwartz (1984) Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12:719-743. Gross, C.G., C.J. Bruce, R. Desimone, J. Fleming, and R. Gattass (1981) Cortical visual areas of the temporal lobe: Three areas in the macaque. In C.N. Woolsey (ed): Cortical Sensory Organization, Vol. 2: Multiple Visual Areas. Clifton, NJ: Humana, pp. 187-216. Gurche, J.A. (1982) Early primate brain evolution. In E. Armstrong and D. Falk (eds): Primate Brain Evolution. New York: Plenum Press, pp. 227-246. Harting, J.K., W.C. Hall, and I.T. Diamond (1972)Evolution ofthe pulvinar. Brain, Behav. Evol. 6:424452. Imig, T.J., M.A. Ruggero, L.M. Kitzes, E. Javel, and J.F. Brugge (19771 Organization of auditory cortex in the owl monkey (Aotus triuirgatus).J. Comp. Neurol. 171:lll-128. Jones, E.G., J.D. Coulter, and S.H.C. Hendry (1978) Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortexof monkeys. J. Comp. Neurol. 181:291-348. Kaas, J.H. (1982) The somatosensory cortex and thalamus in Galago. I n D.E. Haines (ed): The Lesser Bushbaby (Gulugo) as an Animal Model: Selected Topics. Boca Raton, FL: CRC Press, pp. 169-181. Kaas, J.H. (1983) What, if anything, is SI? Organization of the first somatosensory area of cortex. Physiol. Revs. 63.206-231. Kaas, J.H. (1987) The organization of neocortex in mammals: Implications for theories of brain function. Ann. Rev. Psychol. 38t129-151. Kawamura, K., and J. Naito (1984) Corticocortical projections to the prefrontal cortex in the rhesus monkey investigated with horseradish peroxidase techniques. Neurosci. Res. 1239-103. Kolb, B., and J. Walkey (1987) Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behav. Brain Res. 23t127-145. Krishnamurti, A,, F. Sanides, and W.I. Welker (1976) Microelectrode mapping of modality-specific somatic sensory cerebral neocortex in slow loris. Brain Behav. Evol. 13267-283. Krubitzer, L.A., and J.H. Kaas (1990) The organization and connections of somatosensory cortex in marmosets. J. Neurosci. 10:952-974. Krubitzer, L.A., M.A. Sesma, and J.H. Kaas (1986) Microelectrode maps, myeloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels. J. Comp. Neurol250:403430. Le Gros Clark, W.E. (1931) The brain of Microcebus rnurinus. Proc. 2001. SOC.Lond. 101:463485. Le Gros Clark, W.E. (1932) The structure and connections of the thalamus. Brain 55:406-470. Leinonen, L., J. Hyvarinen, and A.R.A. Sovijiirvi (1980) Functional properties of neurons in the temporoparietal association cortex of awake monkey. Exp. Brain Res. 39203-215. Martin, R.D. (1990) Primate Origins and Evolution. London: Chapman and Hall.

505 Matelli, M., R. Camarda, M. Glickstein, and G. Rizzolatti (1987)Afferent and efferent projections of the inferior area 6 in the macaque monkey. J. Comp. Neurol. 251:281-298. Maunsell, J.H.R., and Newsome, W.T. (1987) Visual processing in monkey extrastriate cortex. Ann. Rev. Neurosci. 10:363401. Maunsell, J.H.R., and Van Essen, D.C. (1983)The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. 3. Neurosci. 3.9563-2586. Mesulam, M.-M., and E.J. Mufson (1982) Insula ofthe Old World monkey. I: Architectonics in the insulo-orbito-temporalcomponent of the paralimbic brain. J. Comp. Neurol. 212:l-22. Merzenich, M.M., and J.F. Brugge (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res. 50:275-296. Mishkin, M. (1982) A memory system in the monkey. Phil. Trans. R. SOC. Lond. B 298:85-95. Mountcastle, V.B., B.C. Motter, M.A. Steinmetz, and C.J. Duffy (1984) Looking and seeing: the visual functions of the parietal lobe. In G.M. Edelman, W.E. Gall, and W.M. Cowan (eds): Dynamic Aspects of Neocortical Function. New York: John Wiley & Sons, pp. 159-193. Murray, E.A., and J.D. Coulter (1981) Supplementary sensory area: The medial parietal cortex in the monkey. In C.N. Woolsey (ed): Cortical Sensory Organization, Vol. 1: Multiple Somatic Areas. Clifton, NJ: Humana, pp. 167-195. Nelson, R.J., M. Sur, D.J. Felleman, and J.H. Kaas (1980) Representations of the body surface in postcentral parietal cortex ofMacuea fascicularis. J. Comp. Nenrol. 192t611-643. Newsome, W.T., and J.M. Allman (1980) Interhemispheric connections of visual cortex in the owl monkey, Aotus triuirgutus, and the bushbaby, Galago senegalensis. J. Comp. Neurol. 194209-233. Olson, C.R., and K. Lawler (1987) Cortical and subcortical afferent connections of a posterior division of feline area 7 (area 7p). J. Comp. Neurol. 259: 13-30. Pandya, D.N., and F. Sanides (1973) Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern. Z. Anat. Entwick1.-Gesch.139:127-161. Pandya, D.N., and B. Seltzer (1982)Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J. Comp. Neurol. 204; 196-2 10. Pariente, G. (1979) The role of vision in prosimian behavior. I n G.A. Doyle and R.D. Martin (eds): The Study of Prosimian Behavior. New York Academic Press, pp 411459. Perret, E L , E.T. Rolls, and W. Caan (1982) Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47:329-342. Petrides, M., and D.N. Pandya (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J. Comp. Neurol. 228:105-116. Petrides, M., and D.N. Pandya (1988) Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J. Comp. Neurol. 273:5246. Pons, T.P., P.E. Garraghty, C.G. Cusick, and J.H. Kaas (1985) The somatotopic organization of area 2 in macaque monkeys. J. Comp. Neurol. 241:445-466. Pons, T.P., and J.H. Kaas (1985) Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys. J. Comp. Neurol. 240:16-36. Preuss, T.M., and P.S. Goldman-Rakic (1987) The anatomy of prefrontal cortex of a prosimian primate, Galago crassicaudatus: Characters shared with anthropoid primates. Am. J. Phys. Anthropol. 72244. Preuss, T.M., and P.S. Goldman-Rakic (1989) Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex. J. Comp. Neurol. 282293-316. Preuss, T.M., and P.S. Goldman-Rakic (1991a) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaea. J. Comp. Neurol. 310:429474. Preuss, T.M., and P.S. Goldman-Rakic (1991b) Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates. J. Comp. Neurol. 310: 507-549. Raczkowski, D., and I.T. Diamond (1980) Cortical connections of the pulvinar nucleus in Galago. J. Comp. Neurol. 193:140. Raczkowski, D., and I.T. Diamond (1981) Projections from the superior colliculus and the neocortex to the pulvinar nucleus in Galago. J. Comp. Neurol. 200:231-254.

506 Radinsky, L.B. (1970) The fossil evidence of prosimian brain evolution. In C.R. Nohack and W. Montagna (eds): The Primate Brain. New York: Appleton-Century-Crofts,pp. 209-224. Roberts, T.S., and K. Akert (1963) Insular and opercular cortex and its thalamic projection in Macaca mulatta. Schweitz. Arch. Neurol. Neurochir. Psychiatr. 9 2 - 4 3 . Russo, G.S., and C.J. Bruce (1989) Auditory receptive fields of neurons in frontal cortex of rhesus monkey shift with direction of gaze. Soc. Neurosci. Abstr. 151204. Sanides, F., and A. Krishnamurti (1967) Cytoarchitectonic subdivisions of sensorimotor and prefrontal regions and of bordering insular and limbic fields in slow loris (Nycticebus coucang coucang). J. Hirnforsch 9226252. Seltzer, B., and D.N. Pandya (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res. 149:l-24. Seltzer, B., and D.N. Pandya (1980) Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey. Brain Res. 192339-351. Seltzer, B., and D.N. Pandya (1983) The intraparietal sulcus of the rhesus Neurosci. Abstr. monkey: Intrinsic connections and architectonics. SOC. 9:352. Sur, M., R.J. Nelson, and J.H. Kaas (1980) Representation of the body surface in somatic koniocortex in the prosimian Galago. J. Comp. Neurol. 189:381402. Trojanowski, J.Q., and S. Jacobson (1976) Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. J. Comp. Neurol. 169:371-392. Ungerleider, L.G., and R. Desimone (1986a) Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2. J. Comp. Neurol. 248:147-163. Ungerleider, L.G., and R. Desimone (1986b) Cortical connections of visual areaMT in the macaque. J. Comp. Neurol. 248:190-222. Vaadia, E., D.A. Benson, R.D. Heinz, and M.H. Goldstein, Jr. (1986) Unit study of monkey frontal cortex: Active localization of auditory and of visual stimuli. J. Neurophysiol. 56:934-951. Van Essen, D.C. (1985) Functional organization of primate visual cortex. In A. Peters and E.G. Jones (eds): Cerebral Cortex. Vol. 3. Visual Cortex. New York: Plenum Press, pp. 259-329. Van Essen, D.C., J.H.R. Maunsell, and J.L. Bixby (1981) The middle temporal visual area in the macaque: Myeloarchitecture, connections,

T.M. PREUSS AND P.S. GOLDMAN-RAKIC functional properties and topographic organization. J. Comp. Neurol. 199t293-326. Van Hoesen, G.W. (1982) The parahippocampal gyms: New observations regarding its cortical connections in the monkey. Trends. Neurosci. 2:9-13. Van Hoesen, G.W., and D.N. Pandya (1975) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res. 95:l-24. Vogt, B.A., D.N. Pandya, and D.L. Rosene (1987) Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferent% J. Comp. Neurol. 262256-270. Vogt, C., and 0. Vogt (1919) Allgemeine Ergebnisse unserer Hirnforschung. J. f. Psychol. u. Neurol. 25:221-473. Wall, J.T., L.L. Symonds, and J.H. Kaas (1982) Cortical and subcortical projections of the middle temporal area (MT) and adjacent cortex in galagos. J. Comp. Neurol. 211:193-214. Weber, J.T., and T.C.T. Yin (1984) Subcortical projections of the inferior parietal cortex (area 7) in the stump-tailed monkey. J. Comp. Neurol. 224:206-230. Weller, R.E., and J.H. Kaas (1985) Cortical projections of the dorsolateral visual area in owl monkeys: The prestriate relay to inferior temporal cortex. J. Comp. Neurol. 234t35-59. Weller, R.E., and J.H. Kaas (1987) Subdivisions and connections of inferior temporal cortex in owl monkeys. J. Comp. Neurol. 256:137-172. Weller, R.E., J.T. Wall, and J.H. Kaas (1984) Cortical connections of the middle temporal visual area (MT) and the superior temporal cortex in owl monkeys. J. Comp. Neurol. 228:81-104. Yeterian, E.H., and D.N. Pandya (1985) Corticothalamic connections of the posterior parietal cortex in the rhesus monkey. J. Comp. Neurol. 237:408426. Zilles, K., G. Rehkamper, and A. Schleicher (1979a) A quantitative approach to cytoarchitectonics. V. The areal pattern of the cortex of Microcebus murinus (E. Geoffroy, 18281, (Lemuridae, Primates). Anat. Embryol. 157t269-289. Zilles, K., G . Armstrong, G. Schlaug, and A. Schleicher (1986) Quantitative cytoarchitectonics of the posterior cingulate cortex in primates. J. Comp. Neurol. 253514-524. Zilles, K., G. Rehkamper, H. Stephan, and A. Schleicher (1979b) A quantitative approach to cytoarchitectonics. IV. The area pattern of the cortex of Galago demidouii (E. Geoffroy, 1796, Lorisidae, Primates). Anat. Embryol. 157:81-103.

Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca.

Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates.

Parietal association cortex in the primate: sensory mechanisms and behavioral modulations.

Germinal cell ectopism in the strepsirhine prosimian Galago crassicaudatus crassicaudatus.

Hierarchical Encoding of Social Cues in Primate Inferior Temporal Cortex.

Multiple representation in the primate motor cortex.

Specialized vascularization of the primate visual cortex.

Regulation of the primate fetal adrenal cortex.

Responses of neurons in the primate taste cortex to glutamate.

Segregation of callosal and association pathways during development in the visual cortex of the primate.

First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy.

Local and Global Correlations between Neurons in the Middle Temporal Area of Primate Visual Cortex.

Thinning of capillary walls and declining numbers of endothelial mitochondria in the cerebral cortex of the aging primate, Macaca nemestrina.

Paecilomycosis in a nonhuman primate (Macaca mulatta).

Late Eocene of Burma yields earliest anthropoid primate, Pondaungia cotteri.

Cerebellar corticovestibular fibers of the posterior lobe in a prosimian primate, the lesser bushbaby (Galago senegalensis).

Specialized pathways from the primate amygdala to posterior orbitofrontal cortex.

Cerebellar corticonuclear and corticovestibular fibers of the flocculonodular lobe in a prosimian primate (Galago senegalensis).

Time course of functional connectivity in primate dorsolateral prefrontal and posterior parietal cortex during working memory.

The suprarenal glands of a prosimian primate, the lesser bushbaby (Galago senegalensis).

Oscillatory activity is not evident in the primate temporal visual cortex with static stimuli.

Dendro-dendritic and reciprocal synapses in the primate motor cortex.

Associative-memory representations emerge as shared spatial patterns of theta activity spanning the primate temporal cortex.

Hierarchy of hue maps in the primate visual cortex.