corticothalamic connections of the posterior parietal cortex in the rhesus monkey

THE JOURNAL OF COMPARATIVE NEUROLOGY 237:408-426 (1985)

Corticothalamic Connections of the Posterior Parietal Cortex in the Rhesus

Monkey

EDWARD H. YETEKIAN A") DEEPAK N. PANDYA Department of Psychology, Colby College, Waterville, Maine 04901 (E.H.Y.), Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Massachusetts 01730 (E.H.Y.,

D.N.P.), Departments of Anatomy and Neurology, Boston University School of Medicine, Boston, Massachusetts 02118, and Harvard Neurological Unit, Beth Israel Hospital,

Boston Massachusetts 02215 (D.N.P.)

ABSTRACT Corticothalamic connections of posterior parietal regions were studied

in the rhesus monkey by using the autoradiographic technique. Our observations indicate that the rostral superior parietal lobule (SPL) is connected with the ventroposterolateral (VPL) thalamic nucleus. In addition, whereas the rostral SPL is connected with the ventrolateral (VL) and lateral posterior (LP) thalamic nuclei, the rostral IPL has connections with the ventropostero- inferior (VPI), ventroposteromedial parvicellular (VPMpc), and suprageniculate (SG) nuclei as well as the VL nucleus. The caudal SPL and the midportion of IPL show projections mainly to the lateral posterior (LP) and oral pulvinar (PO) nuclei, respectively. These areas also have minor projections to the medial pulvinar (PM) nucleus. Finally, the medial SPL and the caudal IPL project heavily to the PM nucleus, dorsally and ventrally, respectively. In addition, the medial SPL has some connections with the LP nucleus, whereas the caudal IPL has projections to the lateral dorsal (LD) nucleus. Furthermore, the caudal and medial SPL and the caudal IPL regions have additional projections to the reticular and intralaminar nuclei-the caudal SPL predominantly to the reticular, and the caudal IPL mainly to the intralaminar nuclei.

These results indicate that the rostral-to-caudal flow of cortical connectivity within the superior and inferior parietal lobules is paralleled by a rostral-to-caudal progression of thalamic connectivity. That is, rostral parietal association cortices project primarily to modality-specific thalamic nuclei, whereas more caudal regions project most strongly to associative thalamic nuclei.

Key words: thalamus, cortical, parietal, connections

The specific and association nuclei of the thalamus tradi- tionally have been differentiated on the basis of their pe- ripheral input and their pattern of projections to the cortex. Whereas the specific thalamic nuclei have been shown to project mainly to the primary sensory and motor areas, the association nuclei project to parasensory and higher-order association areas (Walker, '36, '38; Clark and Powell, '53; Wilson and Cragg, '67; Jones and Powell, '70a; Hubel and Wiesel, '72; Mesulam and Pandya, '73; Bos and Benevento, '75; Trojanowski and Jacobson, '75, '77; Benevento and Rezak, '76; Burton and Jones, '76; DeVito and Simmons, '76; Baleydier and Mauguiere, '77; Kievit and Kuypers,

0 1985 ALAN R. LISS, INC.

'77; Kasdon and Jacobson, '78; Mauguiere and Baleydier, '78; Whitsel et al., '78; Jones et al., '79; Nelson and Kaas, '81). In recent years, it has been shown that the primary and association cortices have different patterns of cortical connectivity. Thus, the primary sensory and motor areas are shown to have relatively restricted projections to adjacent regions. In contrast, the association areas have more

Accepted March 15, 1985. A preliminary report of these findings was presented at the

meeting of the American Association of Anatomists, Indianapolis, Indiana, April 1982 (Yeterian and Pandya, '82).

CORTLCOTHALAMIC CONNECTIONS

widespread cortical connections. Moreover, increasingly di- verse cortical projections are seen as one progresses through the parasensory regions to higher-order association areas (Kuypers et al., '65; Pandya and Kuypers, '69; Jones and Powell, '70b; Chavis and Pandya, '76; Rockland and Pan- dya, '79; Ungerleider and Mishkin, '79). A general trend exists such that higher-order association areas show relatively more connectivity with multimodal and limbic areas than do parasensory regions (Jones and Powell, '70b; Van Hoesen et al., '72; Seltzer and Pandya, '76, '78; Mesulam et al., '77; Divac et al., '77; Pandya et al., '81).

In particular, observations of parietal lobe connectivity have revealed two trends in intrinsic projections, which begin in area 2 of the postcentral gyrus. As these trends proceed caudally within the superior and the inferior parietal lobule, they show increasingly complex connections within the parietal lobe (Murray and Coulter, '81; Pandya and Seltzer, '82a). Furthermore, studies of long cortical association connections have revealed that whereas the rostral portions of the posterior parietal cortex have connections to the premotor, prefrontal, SI, SII, and MI1 areas, the caudal parietal regions project to the multimodal areas of the parietotemporal cortex and the frontal lobe as well as to the cingulate and parahippocampal gyri (Jones and Pow- ell, '70b; Chavis and Pandya, '76; Pandya and Seltzer, '82b). Likewise, physiological and behavioral studies suggest that the rostral portion of the parietal lobe has functional properties relating directly to somatosensory function, whereas the caudal portion is involved in more integrative and non- modality-specific functions (Moffett et al., '67; Heilman et al., '70; Duffy and Burchfiel, '71; Petrides and Iversen, '78; Robinson and Goldberg, '78; Yin and Mountcastle, '78; Lynch, '80; Hyvarinen, '82a,b). It is known that the posterior parietal cortex is related to associative thalamic nuclei, such as the lateral posterior and pulvinar nuclei (Clark and Boggon, '35; Petras, '71; Trojanowski and Jacobson, '77; DeVito, '78; Jones et al., '79). In view of the connectional and functional differences within the posterior parietal region as outlined above, it would be of great interest to know whether the corticothalamic connectivity of posterior parietal areas reflects this differential cortical organization.

In the present study, therefore, we have investigated the corticothalamic connections of the posterior parietal cortex, including both the lateral and medial areas as well as adjacent regions in the intraparietal sulcus, using the autoradiographic method.

409

MATERIALS AND METHODS Corticothalamic connections were traced in the brains of

19 rhesus monkeys by using radioactively labeled amino acids. Each animal received a unilateral cortical injection (3H-leucine and proline in equal amounts; volume range 0.4-1.0 pL; specific activity range 40-80 pCi) in a different part of the posterior parietal region. After a survival period of 4-7 days, the animals were killed, and their brains were removed and processed for autoradiography with the technique of Cowan et al. ('72). Exposure times ranged from 3- 6 months.

Each hemisphere was divided coronally into two blocks in the stereotaxic plane (Fig. 4A). Each block was embedded in paraffin and cut into 10 pm-thick sections in the coronal plane. Every tenth section was processed for autoradiography and stained with thionin. This stain allowed for the analysis of cortical architecture, localization of the injection

clei. The precise locations of the injections were determined by observing the cortical architecture around the labeled area in the cortex, and comparing this with the architecture of the corresponding nonlabeled area of the opposite hemisphere. Figure 4 (B-F) shows representative injection sites in five different cases described below.

The distribution of terminal label as revealed in each section under darkfield illumination was charted onto coronal tracings of the thalamus. The boundaries of the various thalamic nuclei were determined from the thionin- stained sections under brightfield illumination. Addition- ally, the atlas of Olszewski ('52) was used as a reference for delineating thalamic boundaries. Figures 1 and 2 depict the thalamic nuclei in the coronal plane in two representative rhesus monkey brains prepared with cresyl violet and acetylcholinesterase (AChE) stains, respectively. We realize that the nomenclature of the subdivisions of different thalamic nuclei is complex, as pointed out by Jones et al. ('79). Nevertheless, we have adhered to the nomenclature of 01-

AhbreviatLons

AM anteromedial nucleus AS arcuate sulcus AV anteroventral nucleus CC corpus callosum Cd caudate nucleus Cdc nucleus centralis densocellularis CF calcarine fissure CING S cingulate sulcus CL nucleus centralis lateralis CM centromedian nucleus CS central sulcus CSL nucleus centralis lateralis superior GLd dorsal lateral geniculate nucleus GM medial geniculate nucleus H hahenula 10s inferior occipital sulcus IPL inferior parietal lobule IPS intraparietal sulcus LD laterodorsal nucleus LF lateral fissure Li nucleus limitans LP lateral posterior nucleus LS lunate sulcus MD dorsomedial nucleus Pcn nucleus paracentralis pf parafascicular nucleus PI inferior pulvinar nucleus PL lateral pulvinar nucleus PM medial pulvinar nucleus PO oral pulvinar nucleus POMS medial parieto-occipital sulcus PS principal sulcus Re nucleus reuniens Ret reticular nucleus SG suprageniculate nucleus SN suhstantia nigra SPL superior parietal lobule Sth suhthalamic nucleus STS superior temporal sulcus ThB thalamic bundle VL ventrolateral nucleus VLc ventrolateral nucleus, caudal portion VLm ventrolateral nucleus, medial portion VLo ventrolateral nucleus, oral portion VLps ventrolateral nucleus, posteriormost portion VPI ventropostero-inferior nucleus VPL ventroposterolateral nucleus VPLc ventroposterolateral nucleus, caudal portion VPLo ventroposterolateral nucleus, oral portion VPM ventroposteromedial nucleus VPMpc ventroposteromedial nucleus, parvicelhlar

portion X area X

sites, and identification of the boundaries of thalamic nu- ZI zona incerta

410 E.H. YETERIAN AND D.N. PANDYA

Fig. 1. Photomicrographs to show the locations of different thalamic nuclei in the coronal plane from rostra1 to caudal, levels A-F, in a Nissl-stained rhesus monkey brain.

CORTICOTHALAMIC CONNECTIONS

Fig, 2. Photomicrographs to show the locations of different thalamic nuclei in the coronal plane through levels A (rostraltF (caudal) in an acetylcholinesterasestained rhesus monkey brain.

411


szewski because of its widespread use. These coronal sections show the boundaries of thalamic nuclei according to the plane of cut used in this study.

RESULTS In describing the results, the posterior parietal cortex will

be divided into two major regions: the superior parietal lobule (SPL), which includes the superior and medial parietal cortex, and the inferior parietal lobule (IPL). Ros- trally, both of these regions border the postcentral gyrus, and are contiguous with area 2 of Brodmann (Fig. 3A,B). The modified architectonic parcellation of Pandya and Seltzer ('82a) of the posterior parietal lobe is also used in this paper to describe the cortical areas involved in the various isotope injections (Fig. 3C,D). Although the purpose of this study is to investigate the corticothalamic connections of the posterior parietal cortex, certain rostral isotope injections involve a bordering portion of area 2.

Superior and medial parietal cortex In nine cases, separate injections of tritated amino acids

were placed in various subregions caudal to the superior postcentral dimple. Resulting silver grains were observed over several thalamic nuclei: pulvinar, lateral posterior, ventroposterolateral, ventrolateral, dorsomedial, and the intralaminar and reticular nuclei.

In two cases isotope injections involved the rostral portion of the superior parietal lobule. As shown in Figure 5 , in case 1 the injection involved area PE on the convexity of SPL, whereas in case 2 the injection included areas PE and PEa in the upper bank of the intraparietal sulcus (IPS). The resulting silver grains were observed in the caudal portion of the ventrolateral WLc) and ventroposterolateral (VPLc) nuclei. More caudally, evidence of terminal label was found in the lateral posterior (LP) nucleus and, in case 1, the lateral pulvinar (PL) nucleus. Additionally, some clusters of silver grains were seen laterally in the oral (PO)' and medial (PM) pulvinar nuclei, and in the reticular (Ret) nucleus along the lateral border of the thalamus. Although the basic thalamic projection patterns in these two cases were similar, some differences were noted. For example, in case 2 with the injection extending into area PEa in the intraparietal sulcus, the label was more marked in the PM and PO nuclei. Additionally in this case, label was observed in the centrolateral (CL) division of the intralaminar nuclei.

In another four cases, injections occupied the caudal portion of the superior parietal lobule, area PEc, and extended into the adjacent cortex of the intraparietal sulcus. Al- though case 6 was located more caudally than cases 3-5, the patterns of terminal label were similar in these four cases. As shown in Figure 6, for case 3 with an injection in caudal area PE (Fig. 4B), grains were first observed in the caudal portion of the VL nucleus and in lesser amount in the dorsomedial (MD) thalamic nucleus. Further caudally, distinct clusters of grains were observed over a major portion of the LP nucleus. Additional grains were seen in the dorsal portion of the PO nucleus, and in the rostral portion of the PM nucleus. As in cases 1 and 2, the dorsal portion of the reticular nucleus adjacent to the LP nucleus showed

'The term PO in this paper refers specifically t o the rostralmost division of the pulvinar nucleus, and shouId not be confused with similar nomenclature which has been used to designate the posterior nuclear complex of the thalamus.

evidence of terminal label. Moreover, case 3 showed silver grains over the intralaminar nuclei, specifically CL and centralis lateralis superior (CSL).

In three other cases, isotope injections involved the medial surface of the parietal lobe. The injection in case 7 occupied the caudal portion of the cingulate sulcus, area PEci, whereas in case 8 (Fig. 4C) and case 9, the injections were confined to the parietal cortex below the cingulate sulcus, area PGm. The overall pattern of terminal label was similar in the latter two cases, whereas the former exhibited a quite different projection pattern. As shown in Figure 7 (case 81, the silver grains were first noticed in the caudal and dorsal portion of the VL nucleus. The next region containing terminal label was the LP nucleus, throughout its rostrocaudal extent (Fig. 1lA). Likewise, heavy labeling was observed in the lateral portion of the PM nucleus (Fig. 11B) with lighter labeling in the PO nucleus. In the pulvinar, the quantity of grain was consid- erably more than in the cases involving lateral portions of the SPL, as shown above, and occurred in branching clusters. As in cases 3-6, silver grains were also identified in a small area of the MD nucleus, as well as in the reticular nucleus, and in CL and CSL of the intralaminar nuclei. The label in case 7 with isotope injection in the caudal tip of the cingulate sulcus (area PEci) was found mainly in the VL nucleus. The grains in other thalamic nuclei were con- siderably less and were found in VPL, PL, and the lateral portion of the PO and PM nuclei. As in all the above cases some grains were present in the CL and reticular nuclei.

Inferior parietal cortex In ten animals, isotope injections were placed in different

subregions of the inferior parietal lobule (IPL). In three cases OO-Z!), injections involved the rostral portion of the inferior parietal lobule, area PF, and adjacent parts of the intraparietal sulcus. Whereas in cases 10 and 12, the isotope was confined to a portion of area PF, in case 11 (Fig. 4D) the injection extended rostrally and dorsally to encom- pass the area at the tip of the IPS. In all three cases the injection also involved the adjacent portion of area 2 of the postcentral gyrus. The overall pattern of terminal label in all three cases was similar. Figure 8 shows the major projection patterns in cases 11 and 12. The first appearance of silver grains occurred at the level of the anterior thalamic nuclei. Here, grains were observed in area X and the VL nucleus, in its medial and ventral portion. Further caudally, the bulk of the grains was found in the ventral thalamus, that is, in the ventroposteromedial parvicellular WPMpc), ventroposteromedial WPM), and ventroposteroin- ferior WPI) nuclei (Fig. 1lC). The next area showing silver grains was the PO nucleus (Fig. 11D) with the immediately adjacent rostral PM nucleus showing some grains as well. All three cases also showed a small amount of label in the lateral and ventral portion of the MD nucleus. The intralaminar nuclei showed a substantial amount of grain in the nucleus paracentralis (Pcn), the ventral and lateral portion of CL, and the centromedian (CM) nucleus. In case 11, with extension of isotope into the rostral tip of IPS, additional evidence of terminal label was seen in the suprageniculate region of the medial geniculate complex (Figs. 8, 11D). the medial geniculate complex (Figs. 8, 11D).

In another three cases (13-13, isotope injections involved middle portions of the inferior parietal lobule. In case 13, the injection involved the dorsal portion of area PFG and the adjacent intraparietal sulcal cortex. Case 14 involved

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CORTICOTHALAMIC CONNECTIONS 415

primarily the central portion of area PFG, whereas case 15 (Fig. 4E) occupied the ventral portion of area PFG, and extended into the adjacent lateral sulcal cortex. Unlike the rostral inferior parietal cases, most of the ventral thalamic nuclei failed to show any silver grains in these cases (Fig. 9). The main bulk of terminal label was observed in the PO nucleus and in the central portion of the PM nucleus. Only sparse label was seen at occasional levels of the VPL, VL, and MD nuclei. Intralaminar label was seen mainly in the CL nucleus. There were slight differences among these cases in terms of the topographic distribution of fiber ter- minals. Thus, in case 13 with an injection extending into the intraparietal sulcus, grains tended to occupy more of the PM nucleus than in cases 14 and 15. Additionally, in cases 13 and 14 some grains were seen over the reticular nucleus.

In another four cases (16-191, isotope injections were placed in various regions of the caudal inferior parietal lobule, areas PG and Opt. In three cases (16, 18, and 19), the injections were confined to the lateral surface of IPL; Figure 4F shows the injection site in case 18. In case 17, the injection involved the dorsal portion of caudal IPL and extended into the adjacent cortex of the lower bank of the intraparietal sulcus. The overall pattern of label in these cases was similar (Fig. 10). Just as in the previous cases involving the middle portion of the IPL, the main bulk of terminal label occurred in the pulvinar. However, the grains in these cases were located predominantly in the PM nucleus, and appeared as interconnected bands and patches (Fig. 1lF). In terms of quantity and distribution, these projections resembled those observed in cases involving the medial parietal cortex (see case 8 above), but extended up to the caudal pole of the thalamus. Additionally, grains were observed in the LP nucleus, as well as in dorsolateral portions of the MD nucleus. Unlike any of the other cases described above, in each of the caudal IPL cases a distinct cluster of silver grains was observed over the laterodorsal nucleus (Figs. 10, 11E). Finally, in each of these cases, a sizable amount of grain was observed over the intralaminar nuclei, in the CSL and dorsal CL nuclei as well as in the dorsal reticular nucleus. In addition, in case 17 a small amount of grain was noted in the Pcn nucleus.

Corticothalamic fiber pathways The use of autoradiographic techniques has allowed us to

trace the corticothalamic fiber trajectory leading from each of the injection sites. In each case, the central white matter core underlying the injection site contained two dense fiber bundles heading medially. One of the bundles occurred ventrally, remaining lateral to the body of the caudate nucleus. From this bundle, labeled fibers could be followed ventrally up to the lateral border of the thalamus (Fig. 11D). At this point in each case, the thalamic fibers seemed to form a compact mesh within the lateral thalamic pedun- cle at a dorsal-ventral level coincident with that of the thalamic nuclei in which they terminate. From this area, the fibers appeared to penetrate the lateral border of the thalamus toward the thalamic nuclei of termination (Fig. l lB, F).

Fig. 4. A. Photopaph of the medial surface of the cerebral hemisphere of a rhesus monkey depicting the plane of cu t (shown by arrowheads) used in this study for cortex as well as thalamus. B-F. Photomicrographs of five representative isotope injection sites from cases involving various areas of the posterior parietal cortex (B, case 3; C, case 8; D, case 11; E, case 13, F, case 18).

DISCUSSION

The somatosensory cortex of the postcentral gyrus (areas 3, 1, and 2 of Brodmann) is heavily interconnected with the ventrobasal complex of the thalamus (Jones and Powell, '70a; Whitsel et al., '78; Jones et al., '79). The corticothalamic projections are topographically organized, with those from the lower postcentral gyrus connected to the VPM nucleus, and those from the dorsal postcentral gyrus to the VPL nucleus (Jones and Powell '70a; Jones et al., '79). Additionally, these areas have been shown to project to the VL thalamic nucleus (Jones et al., '79). More recently, Friedman and Jones ('81) and Jones and Friedman ('82) have further described the thalamic connections leading to the pre- and postcentral gyri (areas 4, 3a, 3b, 1, and 2). In terms of corticocortical connections, the dorsal and ventral portions of the postcentral gyrus project to the adjoining superior and inferior parietal cortices, areas PE and PF, respectively (Jones and Powell, '69, '70b; Pandya and Kuy- pers, '69; Vogt and Pandya, '78). In the present study as well as in that of Jones et al. ('79), it is shown that the rostral SPL, area 5 or area PE, projects mainly to the VL, VPL, PO, and LP thalamic nuclei. Likewise, rostral IPL, including area 7b, or area PF, and the adjacent portion of area 2, projects to the VL, VPM, VPMpc, VPI, PO, and the rostralmost portion of the PM nuclei. Thus, the projections from the rostral SPL and IPL seem to be related to specific somatosensory thalamic nuclei WPL, VPM, VPI) on one hand, and to association nuclei (PO, PM, LP) on the other. It should be pointed out, however, that the projections to VPM and VPI from the rostral IPL cases could result from the involvement of area 2 in all three injections. According to the recent observations of Weber and Yin ('84), an injection limited strictly to area PF did not result in terminal label in the ventrobasal complex.

In terms of the functional role of these two areas, that is, rostral SPL, behavioral studies have indicated their function to be of a more complex nature than that of areas 3, 1, and 2 in the somatosensory sphere. Thus, whereas the postcentral gyrus subserves basic proprioceptive and discrimi- native function (such as texture and two-point discrimination) as well as angularity discrimination (Critchley, '53; Randolph and Semmes, '741, rostral posterior parietal cortex has been shown to be involved in reaching (Moffett et al., '67). Likewise, physiological studies have shown a hier- archical trend in terms of the trigger features of the cells in areas 3, 1, 2, and 5. Whereas the cells in area 3 respond preferentially to passive cutaneous stimulation, those in area 5 respond primarily to stimulation of multiple joints; cells in areas 1 and 2 show intermediate response charac- teristics (Powell and Mountcastle, '59; Duffy and Burchfiel, '71; Sakata, '75). Thus, the differential corticothalamic connectivity of the postcentral gyrus and rostral SPL and IPL may, in part, mediate the differential functional aspects of these regions. Moreover, the rostral SPL and IPL show different overall patterns of corticothalamic connectivity. Consistent with the close relationship that the rostral SPL maintains with the postcentral gyrus, this region projects to the VPL nucleus (Jones et al., '79).

The functional role of additional projections, from rostral SPL to the LP and dorsal PO nuclei, and from rostral IPL to the ventral PO and to the PM nuclei, is not clear. How- ever, one can speculate that this connectivity may be involved in higher-order associative activity in the somatosensory modality. In this regard, it should be pointed


CASE 1

A

B

E

Fig. 5. Diagrammatic representation of isotope injections in two cases in the rostral superior parietal lobule (shown as black regions on the hemispheres) and resulting label in coronal thalamic sections A-E, rostral to caudal. Fibers are represented by thin lines, and terminations by dots.


CASE 3

C

Fig. 6. Diagrammatic representation of isotope injections in one case in the caudal superior parietal lobule, and resulting label in coronal thalamic sections A-E, rostral to caudal.

out that area 2 adjacent to the posterior parietal cortex is shown to contain somatosensory re-representations (Kaas et al., '81; Merzenich et al., '81). These representations occupy an intermediate position between the SI representation in area 3 and the areas of the posterior parietal cortex involved in higher-order functions, The corticothalamic connections of these intermediate regions to specific thalamic nuclei on one hand and to thalamic association nuclei on the other may indicate a functional role for these connectivities intermediate to that of SI and the more caudal parietal areas.

The projections from rostral IPL to VPI, VPMpc, and the suprageniculate (SG) nuclei are quite interesting. Accord- ing to recent observations, the VPI nucleus receives input from the Pacinian receptors and in turn projects to area SII (Friedman et al., '83; Burton, '84). Thus, the rostral IPL (area 7b) has a definite role in somatosensory processing. Furthermore, the projections to the VPMpc and VPI nuclei suggest a role for those corticothalamic connections in gustatory function, since both the VPMpc and VPI nuclei have been shown to receive afferents from gustatory brainstem nuclei (Beckstead et al., '80), and are connected with the cortical gustatory areas in the frontal operculum and rostral insula (Bornstein, '40; Benjamin and Welker, '57; Rob- erts and Akert, '63). Additionally, rostral IPL has been shown to have connections with the gustatory cortical area

in the frontal operculum (Pandya et al., '80). The distinctive projection t o the VPI and SG nuclei from rostral IPL indicates its role in yet another sensory modality. Afferents from brainstem vestibular nuclei are shown to project to the VPI (Liedgren et al., '76; Deecke et al., '77; Buttner and Lang, '79) and SG nuclei (Liedgren et al., '76). The rostral IPL, specifically the cortex at the rostral tip of the IPS (which projects to the VPI and SG nuclei), has been identified as a cortical vestibular area by Fredrickson et al. ('66). Thus, these corticothalamic projections of rostral IPL, which borders a somatosensory representation of head, face, and neck (Woolsey, '58) and receives connections from these areas (Pandya and Kuypers, '69; Jones and Powell, '70b), and also contains a vestibular representation and face-responsive neurons (Leinonen and Nyman, '79), may be involved in complex activity contingent upon more than one sensory modality. In this regard, it is of interest to note that the neuronal activity of both thalamic and cortical vestibular regions (the VPI and SG nuclei; rostral tip of IPS) is often bimodal-that is, somatosensory as well as vestibular (Schwarz and Fredrickson, '71).

The next areas to be considered are the caudal SPL (area 5 , or areas PE and PEc) and mid-IPL (rostral area 7a, or area PFG). At this stage, there is only scant evidence of projections from these areas to the ventrobasal complex. Instead, caudal SPL is connected predominantly with the


CASE 7

CASE a

Fig. 7. Diagrammatic representation of isotope injections i n two cases in the medial parietal region, and resulting label in coronal thalamic sections A-E, rostra1 to caudal.


CASE 12

Fig. 8. Diagrammatic representation of isotope injections in two cases in the rostral inferior parietal lobule, and resulting label in coronal thalamic sections A-E, rostral to caudal.


CASE 13

Fig. 9. Diagrammatic representation of isotope injections in two cases in the middle portion of the inferior parietal lobule, and resulting label in coronal thalamic sections A-E, rostra1 to caudal,

CORTICOTHALAMIC CONNECTIONS 42 1

CASE 17

CASE 18

Fig. 10. Diagrammatic representation of isotope injections in two cases in the caudal inferior parietal lobule, and resulting label in coronal thalamic sections A-E, rostra1 to caudal.

Figure 11


LP nucleus, and to some extent with the dorsal PM nucleus. Additionally, this area continues to have projections to the VL nucleus. In contrast, the main projections of mid-IPL are to the PO and ventral PM nuclei. These connections suggest that there are differential projection systems for the caudal SPL and mid-IPL, with some degree of communality in the PM nucleus. The virtual absence of projections from these areas to the ventrobasal nuclei on the one hand, and their strong connectivity with the LP-pulvinar nuclei on the other, indicates that these pathways are involved in still higher-order associative activity in the somatosensory modality. The fact that SPL even at this stage maintains distinct connections with VL, whereas mid-IPL has only very weak connectivity with VL, suggests a role for caudal SPL in sensorimotor integration of the trunk and limbs. It is of interest to note that cells with simpler, primary response properties (joint position, cutaneous sensitivity, and deep pressure) are distributed in the rostral SPL, while those with more complex response properties (e.g., cells responsive to reaching or hand manipulation) are more posterior (Lynch, '80). Similarly, reach and hand manipulation cells are found in the mid-IPL region (Hyvarinen, '82b). The lack of behavioral studies restricted to either caudal SPL or mid-IPL precludes us from putting forth a precise functional proposal regarding this corticothalamic connectivity.

Finally, the medial SPL (Brodmann's medial area 7, or area PGm) and the caudal IPL (caudal area 7a, or areas PG and Opt) have strikingly different corticothalamic connections. Both regions have strong connections to the PM nucleus, which extend to the caudal pole of the pulvinar. Within the PM nucleus, however, medial SPL projections are directed relatively more medially than those of caudal IPL, although there is some degree of communality caudally. Unlike caudal SPL and mid-IPL, these areas show only minor projections to the LP and PO nuclei. The major difference between the medial SPL and caudal IPL is that caudal IPL has a substantial projection to the laterodorsal (LD) nucleus. The strong PM nucleus projections from both medial SPL and caudal IPL suggest that this corticothalamic relationship may subserve even more complex associative functions than the corticothalamic connections of more rostral parietal areas.

On the basis of behavioral and physiological observations, different functional roles for subregions of the posterior parietal lobe have been proposed (Denny-Brown and Cham- bers, '58; Heilman et al., '70; Eidelberg and Schwartz, '71; Robinson and Goldberg, '78; Yin and Mountcastle, '78; Lynch, '80; Hyvarinen, '82a,b; Mishkin and Ungerleider, '82; Mishkin et al., '82). The corticothalamic connectivity described above is consistent with these data. Within the superior parietal lobule, there is a rostral-to-caudal progression in connectivity from modality-specific nuclei to association nuclei. This progressive corticothalamic connectivity parallels the increasing functional complexity shown in physiological studies of rostral versus caudal SPL (Powell and Mountcastle, '59; Duffy and Burchfiel, '71) pertaining

Fig. 11. Darkfield photomicrographs of coronal sections showing evi dence of terminal label in the thalamus. A and B show label over the LP and PM nuclei after an isotope injection in the medial parietal region (case 8). C and D show label over the VPM, PO, and SG nuclei followinp an

to limb and trunk representation. Additionally, whereas the lateral SPL may be involved in progressively complex somatic sensory function, the medial portion of SPL, by virtue of its strong connections with the PM nucleus, may subserve more integrative functions within the somatosensory system. Furthermore, the other connections of medial SPL to the cingulate gyrus (Petrides and Pandya, '84) and to a polysensory area (TPO) in superior temporal sulcus (STS) (Seltzer and Pandya, '83) add support to this notion.

The IPL also shows a progression in corticothalamic connectivity from its rostral to its caudal subregions. As in SPL, this increasing connectional complexity parallels the differential functional complexity seen in rostral versus caudal portions of IPL (Moffett et al., '67; Mountcastle et al., '75; Robinson and Goldberg, '78; Lynch, '80; Hyvarinen, 82a,b). However, in contrast to SPL, the IPL is also shown to contain representations of vestibular (Schwarz and Fred- rickson, '71) and visual (Yin and Mountcastle, '78; Hyvari- nen, '81) modalities. The rostral IPL (area 7b), which receives input from area 2 containing somatic representations of head, neck, and face, and additionally has a vestibular representation, is shown to project mainly to the VPI, VPMpc, and SG nuclei. These nuclei have been implicated in the gustatory and vestibular systems (Blum et al., '43; Patton et al., '44; Benjamin and Burton, '68; Benjamin et al., '68; Deecke et al., '72, '73, '74, '77; Buttner and Henn, '76; Buttner and Lang, '79; Beckstead et al., '80). Thus, this corticothalamic connectivity of rostral IPL might be involved in the integration of these three modalities. The middle IPL has relatively sparse connections with the ventrobasal complex, but has substantial connectivity with the PO nucleus, and some with the LP nucleus. These connections seem to be parallel to those observed for medial SPL (see above). Additionally, it is interesting to note that mid- IPL projects to some extent to STS (Seltzer and Pandya, '84) and to medial SPL (Pandya and Seltzer, '82a). Therefore, the corticothalamic connections of mid-IPL (area PFG) may be involved in higher-order somatosensory activity related to the face, head, and neck regions. It should be noted also that Hyvarinen ('81) and others have shown that the neurons in this area (PFG) are responsive to visual as well as somatosensory stimulation. Anatomical studies have not demonstrated direct projections from visual cortex to this region. However, projections from peristriate cortex to the lower bank of the intraparietal sulcus (IPS) (area POa) adjacent to area PFG have been reported (Kuypers et al., '65; Rockland and Pandya, '79; Seltzer and Pandya, '80; Ungerleider and Mishkin, '82).

The caudal portion of IPL (area 7a or area PG-Opt) shows strong projections to the PM nucleus, as does medial SPL (area PGm). In addition it has a substantial connection with the laterodorsal nucleus (LD). In terms of cortical connections, this area has strong links with the cingulate and parahippocampal gyri, presubiculum, and perirhinal cortex, as well as with polymodal areas within STS (Pandya and Kuypers, '69; Jones and Powell, '70b; Seltzer and Pan- dya, '76, '84; Seltzer and Van Hoesen, '79; Pandya and Seltzer, '82b). Furthermore, caudal IPL is shown to be connected with the peristriate belt (Rockland and Pandya, '79; Ungerleider and Mishkin, '82). Thus, the corticothalamic and corticocortical connectivity of the caudal IPL region distinguishes it from other parietal areas, and reflects its

isotope injection in the rostral inferior parietal lobule (case 11). E and F show label over the LD and PM nuclei after an isotope injection in the caudal inferior parietal lobule (case 18). The large white arrowhead in D

distinctive functional role as shown by physiological and 70; Hyvarinen and 'Or- studies (Heilman et

indicates the trajectory of corticothalamic fibers. anen, '74; Hyvarinen, '81; Mountcastle et al., '75; Petrides


and Iversen, '78; Robinson and Goldberg, '78; Yin and Mountcastle, '78; Lynch, '80; Mishkin et al., '82; Mishkin and Ungerleider, '82).

Our observations of differential topographic projections of rostral, middle, and caudal IPL are substantially in agree- ment with the recently reported findings of Weber and Yin ('84). However, our data suggest that it is the rostral rather than the middle IPL region which has major connectivity with the ventrobasal complex (VPM, VPI, VPMpc). The VPM projections could be the result of involvement of area 2 in the rostral IPL injections. Additionally, we find that the rostral and middle IPL regions, although both appear to have some projections to the PM nucleus, tend to project heavily to the PO nucleus. Finally, the projections to the SG nucleus in our cases seem to derive primarily from the cortex at the rostral tip of the IPS, although a few projections to this nucleus appear to arise from the midventral IPL (case 15). The observation of Weber and Yin that the mid-IPL projects to the SG nucleus is perhaps consistent with a recent report by Grusser et al. ('83). These latter investigators have identified another vestibular representation in the upper bank of the lateral sulcus, at a mid-IPL level.

A distinct architectonic area at the caudal tip of the cingulate sulcus, area PEci, has corticothalamic connections which resemble those of rostral SPL, that is, it projects mainly to the VL, VPL, and LP nuclei. While this connectivity is markedly different from that of the adjacent medial area PGm, it is consistent with the proposed functional role of this area as a supplementary sensory cortex (Murray and Coulter, '81).

In addition to the projections described above, the posterior parietal cortex has distinct connections with the reticular and intralaminar nuclei. The rostral and caudal portion of SPL and the medial parietal region each project to the dorsolateral portion of the thalamic reticular nucleus. Like- wise, each of the sectors, except for the very rostral portion of SPL, has projections to the CSL and dorsal CL nuclei. In contrast to SPL, the IPL has relatively restricted projections to the reticular nucleus. However, this region does project to intralaminar nuclei, though there seems to be a distinct topography. Thus, rostral IPL projects to the Pcn and ventral CL nuclei as well as the CM nucleus, whereas the mid-IPL projects to the dorsal CL nucleus, only mini- mally to the Pcn nucleus, and not a t all to the CM nucleus. The caudal IPL has substantial projections to both the CSL and the dorsal CL nuclei. The SPL projections to the reticular nucleus may be involved in maintaining arousal relating to somatic sensation in the limbs and trunk. In contrast, the projections from caudal and medial SPL, and IPL, to the CSL and CL nuclei may have a role in more specialized attentional mechanisms. In this regard, it is interesting to note that the projection to the Pcn nucleus is derived mainly from the rostral IPL. Physiological studies have indicated that cells in this nucleus respond prior to goal-directed saccades (Schlag and Schlag-Rey, '84; Schlag-Rey and Schlag, '84).

Finally, the caudal and medial SPL and the entire IPL have relatively minor projections to the parvicellular portion of the MD nucleus. These projections may reflect the interrelatedness of the parietal lobe with the frontal cortex, which itself is strongly interconnected with the MD nucleus (Scollo-Lavizzari and Akert, '63; Tobias, '75; Kievit and Kuypers, '77; Kiinzle and Akert, '77; Kunzle, '78; Akert and Hartmann-von Monakow, '80). In particular, the SPI

and IPL are reciprocally interconnected with the dorsolat- era1 prefrontal cortex, a region which also projects to the parvicellular portion of the MD nucleus (Jones and Powell, '70b; Chavis and Pandya, '76; Barbas and Mesulam, '81; Petrides and Pandya, '84). This connectivity may represent a parallel system by which corticocortical integration of the parietal and frontal cortices is reflected at the thalamic level.

ACKNOWLEDGMENTS We are very grateful to Mr. Brian Butler and Ms. CheryI

Potter for excellent technical assistance, and to Ms. Karen Bourassa for typing the manuscript. This study is sup- ported by the Veterans Administration, Edith Nourse Rog- ers Memorial Veterans Hospital, Bedford, Massachusetts 01730, NIH grant 16841, and Colby College social science grants A22085 and A22093.

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corticothalamic connections of the posterior parietal cortex in the rhesus monkey

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