Chapter 12 Multiple visual areas in the posterior parietal cortex of primates

T.P. Hicks, S. Molotchnikoff and T. On0 (Eds.) Progress in Brain Research, Val. 95 0 1993 Elsevier Science Publishers B.V. All rights reserved.

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CHAPTER 12

Multiple visual areas in the posterior parietal cortex of primates Carmen Cavada' and Patricia S. Goldrnan-Rakic2 I

'

Departamento de Morfologia, Facultad de Medicina, Universidad Autonoma de Madrid, 28029 Madrid, Spain, and Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, U.S.A.

Introduction

Visual perception and visuo-motor functions are characteristically altered following posterior parietal damage in man and non-human primates. Posterior parietal lesions also produce defects in other sensory and motor domains, including misperception of self body parts and inaccurate limb movements (see reviews by Lynch, 1980; Hyvarinen, 1982; Andersen, 1987). These disorders seem to be qualitatively comparable in humans and monkeys, although their severity is greater in man, especially after lesions of the non-dominant hemisphere. For example, ignorance or neglect to stimuli present on the side contralateral to the lesioned hemisphere is a prominent symptom of parietal damage in man (Critchley, 1953). In macaques, the deficit is less pronounced, but nonetheless similar in nature: neglect for contralateral stimuli may not be fully apparent, but when the animals are confronted with two stimuli simultaneously, they ignore the one located contralateral to the parietal ablation (Schwartz and Eidelberg, 1968; Heilman et al., 1970), a condition known as extinction. This milder form of neglect is also present, and in fact was initially described, in human patients suffering from parietal injury (Bender and Furlow, 1944; DennyBrown et al., 1952). Thus, it is our assumption that the study of the neural organization of the posterior parietal cortex in a species, like the macaque monkey, amenable to experimental investigation

and whose symptoms after parietal damage appear comparable to those in man, may shed light on the mechanisms at function in this large expanse of primate association cortex. The variety of disorders that follow injury to the posterior parietal cortex bespeaks a functional heterogeneity. The purpose of this chapter is to review the evidence in macaques in support of a topographic heterogeneity within the posterior parietal cortex involved in visual and visuo-motor functions. This extensive cortical territory appears to contain multiple areas, each characterized by its unique array of connections with other brain regions. The inference could thus be made that the anatomical parcellation of the posterior parietal region has a bearing on its functional and clinical diversity. The parietal territory concerned with vision and eye movements encompasses most of Brodmann's area 7 (Brodmann, 1909), and is located posteriorly and medially to the somatosensory parietal cortex. Therefore, except for brief references in the architectonic survey section, we shall not cover the most anterior and lateral portions of the posterior parietal cortex, including areas 5 and 7b, whose main functional and anatomical affiliations are with the somaticsensory system (Jones and Powell, 1969; Duffy and Burchfield, 1971; Mountcastle et al., 1975; Hyvarinen and Shelepin, 1979; Leinonen et al., 1979; Robinson and Burton, 1980; Cavada and Goldman-Rakic, 1989a).

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Physiological evidence for a parcellation of macaque area 7

The seminal studies carried out in the seventies on the functional properties of cells of the posterior

parietal cortex of monkeys by Hyvarinen, Mountcastle, and Robinson and their colleagues (see for example, Hyvarinen and Poranen, 1974; Mountcastleetal., 1975; Robinsonet al., 1978)werenot aimed primarily at the elucidation of the topographical

visual oculornotor cutaneous somatomotor

adapted from Hyvarinen, 1981

A

visual somatosensory eye position saccade rehicc!

/

adapted from Andersen et al., 1907 Fig. 1. Evidence for a parcellation of the posterior parietal cortex as revealed by physiological studies. Depicted in this figure are representative examples of the topographic location of units recorded in the posterior parietal lobe and adjacent cortex of the intraparietal sulcus. The work of Hyvarinen and colleagues showed that neurons responsive to cutaneous or somatomotor stimuli are located more anteriorly and laterally in the posterior parietal lobe than those related to visual and oculomotor stimuli. The investigations of Andersen and colleagues, while confirming these previous findings, have emphasized the preferential distribution of saccade-related units within the posterior bank of the intraparietal sulcus (see also Blatt et al., 1990).

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location of the different types of neurons they identified. The various groups focused on particular features of the units that were recorded. Thus, the early work of Mountcastle and colleagues emphasized the relationship of neuronal firing with movement, whereas Robinson’s studies called attention to the activation of parietal neurons by visual stimuli (see for example, the review and accompanying discussion in Lynch, 1980). Hyvarinen and colleagues examined neurons responsive to both visual stimulation, and visual fixation or eye movements (Hyvarinen and Poranen, 1974; Hyvarinen, 1982). In all these studies the dependence of the recorded responses upon behavioral factors was emphasized: parietal neurons tended to fire most intensely when the stimulus had significance for the animal, suggesting strong limbic influences (Hyvarinen and Poranen, 1974; Mountcastle et al., 1975; Lynch et al., 1977; Robinson et al., 1978). Despite the emphasis on the physiological attributes of the recorded units, crude topological indications were already given in these early investigations, and were further defined subsequently. As summarized in Fig. 1 , somatosensory and visually driven neurons appeared concentrated in anterior and posterior portions, respectively, of the posterior parietal cortex; and units concerned with motor mechanisms of the eyes predominated medially (Mountcastle et al., 1975; Hyvarinen and Shelepin, 1979; Robinson and Burton, 1980; Hyvarinen, 1981; Andersen et al., 1987). The parcellation of macaque area 7 based on architectonics

Historically, the oldest evidence for a partition of Brodmann’s area 7 in monkeys was its division into two areas, 7a and 7b, by Vogt and Vogt (1919), who, like Brodmann, studied the brain of Cercopithecus (Fig. 2). Areas 7a and 7b, as defined by the Vogts, included practically the entire extent of the convexity of the posterior parietal lobe. Von Bonin and Bailey (1 947) later adopted for the macaque monkey the lettering terminology introduced by Von Economo in his studies of the human brain. They

alsorecognized two areas (PGandPF) on theexposed surface of the posterior parietal lobe (Fig. 2), and considered that there was a gradual transition, rather than a sharp boundary, between them. The more recent study of Pandya and Seltzer (1982) has partitioned the convexity of the posterior parietal lobe further, into five subdivisions (Fig. 2): areas PG and PF, a transitional area between them termed PFG, two areas in the parietal operculum (PGop and PFop), and area Opt, located in the most posterior part of the lobe and thus lying in the posterior portion of area 7a of Vogt and Vogt (or PG of Von Bonin and Bailey). In Brodmann’s map, area 7 extended onto the medial surface of the hemisphere to occupy the dorsal portion of the precuneate gyrus, anterior to prestriate area 19 and posterior to a medial extension of area 5 (Fig. 2). This same region was considered comparable to the cortex of the anterior parietal lobe by Von Bonin and Bailey, who therefore named it P E (area 5 in Brodmann’s terminology; see Fig. 2). Pandya and Seltzer’s view, however, is more in accord with Brodmann’s original description: their area PGm in the precuneate gyrus lies between the prestriate cortex and the medial extension of the anterior parietal cortex (Fig. 2). The cortex lining the banks of the intraparietal sulcus was considered by Von Bonin and Bailey (1947) analogous to the cortex of the adjacent convexities, and thus they labeled it accordingly: area PE in the medial bank, and areas PG and PF in the lateral bank. Seltzer and Pandya (1980), however, recognized a separate area in the lateral bank: POa, with internal (POa-i) and external (POa-e) divisions. Connectional evidence for a parcellation of area 7

It seems fair to conclude from the above overview that there is little consensus on the partition of macaque area 7 relying upon architectonic criteria. In fact, in the last decade, additional subdivisions within Brodmann’s area 7 have come to light, principally on the basis of connectional criteria: VIP

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n

Vogt & Vogt, 1919 Brodmann, 1909

Von Bonin & Bailey, 1947

-

Pandya & Seltzer, 1982

Fig. 2. Cytoarchitectonic parcellations of the posterior parietal cortex in Cercopithecus (Brodmann, 1909; Vogt and Vogt, 1919) and macaque (Von Bonin and Bailey, 1947; Pandya and Seltzer, 1982) monkey brains. Reproduced, with permission, from Cavada and Goldman-Rakic (1989a).

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(ventral intraparietal; Maunsell and Van Essen, 1983) located near the fundus of the intraparietal sulcus; LIP (lateral intraparietal; Andersen et al., 1985; Asanuma et al., 1985), which is largely coextensive with the posterior part of POa of Seltzer and Pandya (1980); MIP (medial intraparietal; Colby et al., 1988) and PIP (posterior intraparietal; Felleman et al., 1987; Colby et al., 1988), situated in the posterior end of the medial and lateral banks, respectively, of the intraparietal sulcus. In general, these newly defined areas were characterized by their connections with other visual areas or with the prefrontal cortex. Thus, VIP was described by Maunsell and Van Essen (1983) as the intraparietal target of projections from area MT. However, in a subsequent study of MT projections, Ungerleider and Desimone (1986) observed that the area MT target cortex in the intraparietal sulcus was not restricted to the fundal region but extended further superficially in the sulcus, into a heavily myelinated zone, and they termed the new region

VIP*. LIP was defined by its prominent connections with the posterior prefrontal cortex (Andersen et al., 1985). Recently, Blatt et al. (1990) have defined ventral and dorsal subdivisions within area LIP (LIPv and LIPd, the former possibly coextensive with POa-i and VIP* of other authors). Areas MIP and PIP were described on the basis of their connections with visual prestriate areas, most notably with area PO (parieto occipital; Colby et al., 1988). Considering that these newly defined sectors of area 7, particularly that portion of it lying in the intraparietal sulcus, were made in the context of investigations focusing on areas outside the posterior parietal cortex itself, the study of the connectional patterns of several major subdivisions of area 7, altogether encompassing a significant expanse of this cortical region, should help to clarify their identity and, in addition, their functional ascription. In the present chapter we review our studies on the complete sets of cortico-cortical connections of three area 7 subdivisions that are associated with

7ip

7a

7m

Fig. 3. Location of the subdivisions of the posterior parietal cortex addressed in the present study. Areas 7a and 7m are approximately coextensive with areas 7a of Vogt and Vogt (1919), and PGm of Pandya and Seltzer (1982), respectively. Area 7ip corresponds to area POa of Pandya and Seltzer (1982). Only the posterior part of 7ip (equivalent to area LIP of Andersen et al., 1985) was investigated here because of its selective linkage with the frontal eye field and with visual areas (see Cavada and Goldman-Rakic, 1989a,b, for additional details). The cytoarchitectonic features of areas 7ip, 7a and 7m are distinct as shown on the right half of the figure. The present study focused on the analysis of their circuitry and revealed marked differences among them, allowing inferences on their functional significance.

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Fig. 4. Connections of areas 7ip, 7a and 7m with the thalamus. The nuclei most strongly connected with each subdivision are shown in bold type. The data used to construct this figure were taken from our own observations and the reports of Asanuma et al. (1985), Yeterian and Pandya (1985), and Schamahmann and Pandya (1990). It should be noted then, that the topographic relationships shown in the bottom diagrams of coronal thalamic sections were taken from different experimental cases, and therefore this figure does not attempt to depict the fine details on the overlap or segregation of the thalamic territories connected with each subdivision. Abbreviations: AM, anterior medial nucleus; AV, anterior ventral nucleus; CL, central lateral nucleus; CM, centromedian nucleus; Csl, central superior lateral nucleus; GL, lateral geniculate nucleus; GM, medial geniculate nucleus; H, habenula; LD, lateral dorsal nucleus; Li, limitans nucleus; LP, lateral posterior nucleus; MD, medial dorsal nucleus; Pcn, paracentral nucleus; Pf, parafascicular nucleus; Pul 1, pulvinar nucleus, pars inferior; Pul L, pulvinar nucleus, pars lateralis; Pul M, pulvinar nucleus, pars medialis; Pul 0, pulvinar nucleus, pars oralis; R, reticular nucleus; SG, suprageniculatenucleus; VA, ventral anterior nucleus; VLps, ventral lateral nucleus, pars postrema; VPL, ventral posterior lateral nucleus; VPLc, ventral posterior lateral nucleus, pars caudalis; VPM, ventral posterior medial nucleus.

visual processing (Cavada and Goldman-Rakic, 1989a,b). Our results lead to the conclusion that each of them participates in different distributed cortico-cortical networks formed by a constellation of visual, limbic, frontal association and motor areas. Moreover, analysis of the known physiological properties of these areas will allow some inferences about the functional role of each network. Finally, we will correlate the distinct networks of interconnected cortical areas to specific subcortical motor targets associated with each area 7 subdivi-

sion (see Cavada and Goldman-Rakic, 1991, and sections below). We have adopted a simple and internally consistent terminology, that also respects cytoarchitectonic features and historical precedents (Fig. 3): areas 7a and 7b (after the Vogts), in the convexity of the posterior parietal lobe; area 7ip, in the posterior bank of the intraparietal suIcus (coextensive with area POa of previous studies); and 7m, on the medial surface of the parietal lobe (equivalent to PGm). Examination of the cytoarchitectonic pat-

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terns of these subdivisions reveals clear differences between them (see Fig. 3). However, the present report will focus on the analysis of axonally transported tracers placed in areas 7a, 7m and posterior 7ip (coextensive with area LIP), all of which sustain prominent connections with visual areas. The posterior sector of 7ip was chosen because, unlike anterior 7ip, it is selectively linked with the frontal cortex engaged in eye and head movements, and because in the sensory domain, it is connected to a set of visual cortices (see Cavada and Goldman-Rakic, 1989a, for additional details, and for accurate descriptions of the methods employed and of the placement of the injected tracers).

Thalarnic connections of areas 7ip, 7a and 7rn The thalamic nuclei connected with areas 7ip, 7a and 7m are specified in Fig. 4. Fig. 5 shows a representative example of topographic similarities and differences in the connections of areas 7ip, 7a and 7m with the lateral and medial pulvinar nuclei, which are the main targets and sources of the thalamic connections of these area 7 subdivisions. The prominent connections of area 7m with these particular nuclei should be noted. It is this association which led us to conclude that this portion of medial parietal cortex is a genuine sector of area 7, and not of area 5. This attribution is in keeping with the cytoarchitectonic criteria of Brodmann (1909) and Pandya and Seltzer (1982), but not with the parcellation of the parietal cortex made by Von Bonin and Bailey (1947; Fig. 2). Additional support for this conclusion are the strong links between area 7m and several visual areas (see below), a characteristic Of most area subdivisions, but not Of area 5. If we are correct, this may be still another example in which Connectional Criteria may prove essential in the evaluation of the organization and function of the different territories of the cerebral cortex (see somatosensory also the recent review on the and Van Essen, and motor cortices in 1991).

Fig, 5 . Topographic differences in the thalamic labeling following HRP-WGA injections into areas 7ip ( A ) ,7a (B) and 7m (0. The darkfield photomicrographs were taken from coronal sections at approximately the same posterior level of the pulvinar complex. The arrow in C points to a patch of fabeling in the medial part of the superior colliculus. Abbreviations: Pul L, pulvinar nucleus, pars lateralis; Pul M, pulvinar nucleus, pars medialis; V, lateral ventricle. The calibration bar is the same for all three micrographs.

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Connections with sensory areas

Connections with limbic and prefrontal areas

Connections with motor areas

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He.& Do&

8 lateral

Body: Dorsal, central, latent Caudate nuclws & ventral (posterlor) Tall: Dorsal

Putamen

Medial

I

Head: Dorsal 6 dorsomedial

Caudate nucleus Bodr DOMI DOMI&& medial (anterlor) I TaN: raN: Ventromedial Putamen Dorsomedial.lateral a ventral (anterior)

Head: Donal & dorsolateral

Caudate Bodp Dorsal Half (antedor) Caudate nucleus 'W? Tall: Dorsal

Putamen Dorsal a lateral (antenor)

Dorsomedial

Dorsomedial

Tad

Fig. 7. Topography of the projections of areas 7ip, 7aand 7m to theneostriatum. The striatal territories receiving thedensest projections from each subdivision are shown in bold type. The left caudate nucleus and putamen are viewed from above. The data used to prepare this composite figure are from Cavada and Goldman-Rakic (1991), and as in the case of Figs. 4 and 9 the connections of each subdivision were studied in different experimental animals. Therefore, this diagram is not intended to depict the fine details of the mutual relationships of the striatal territories innervated by each subdivision.

Fig. 6 . Intrahemispheric cortico-cortical connections of areas 7ip, 7a and 7m. The data upon which this figure is based are from Cavada and Goldman-Rakic (1989a,b). The reader may wish to refer to these publications for more information about the nomenclature and criteria used in the identification of the various cortical areas. With the exception of the projections to the presubiculum, all corticocortical connections of each parietal subdivision are reciprocal. Moderate or heavy connections are shown in thick lines, whereas weak connections are in thin lines. Abbreviations: CmL, caudomedial lobule; dPfC, dorsal prefrontal convexity; DPl, dorsal prelunate area; dPmC, dorsal premotor cortex; FEF, frontal eye field; FST, fundal superior temporal area; IT, inferior temporal cortex; MDP, mediodorsal parietal area of Colby et al. (1988); MT, middle temporal area; MTp, peripheral middle temporal area; ObfC, orbitofrontal cortex; PO, parieto occipital area; PS, principal sulcus; Psb, presubiculum; Rsa, retrosplenial cortex, agranular portion; Rsg, retrosplenial cortex, granular portion; SEF, supplementary eye field; SMA, supplementary motor area; SSA, supplementary somatosensory area; STP, superior temporal polysensory area; V2, visual area 2; V3A, visual area 3, anterior portion; V3d, visual area 3, dorsal portion; V ~ Vvisual , area 3, ventral portion; V4, visual area 4; VMC, visual motion cortex of the upper bank of the superior temporal sulcus; vPfC, ventral prefrontal convexity; vPmC, ventral premotor cortex.

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Fig. 8. Representative darkfield photomicrographs showing striatal territories heavily labeled after HRP-WG.4 injections into areas 7ip (A: at the level of the transition between body and tail of the caudate nucleus), 7a (B: head of the caudate nucleus), and 7m (c:head of the caudate nucleus). Abbreviations: Cd, caudate nucleus; pt, putamen; v, lateral ventricle. The calibration bar is the same for all three micrographs.

Connections of areas 7ip, 7a and 7m with sensory cortices Probably the connectivity of the area 7 subdivisions with cortices whose sensory or motor properties are known in some detail are the best aid in the analysis of the functional affiliation of those subdivisions. Fig. 6 summarizes the complete sets of intrahemispheric cortico-cortical connections of areas 7ip, 7a and 7m with sensory, limbic, prefrontal and motor areas. Only some salient features of these connections are commented upon below. For a lengthier discussion the reader may wish to refer to the original descriptions in Cavada and GoldmanRakic (1989a,b), and to subsequent confirmations by Andersen et al. (1990), Blatt et al. (1990) and Baizer et al. (1991). In the sensory domain, area 7ip is the most widely interconnected with visual areas. These include V2, V3, PO, MT and V4, all of which are connected with the primary visual cortex, and also areas involved in higher levels of visual information processing, like IT, STP, DP1, MTp and FST (see Felleman and Van Essen, 1991, for a recent comprehensive account of visual cortico-cortical connections). The connections of areas 7aand 7m with regions connected with the striate cortex are more restricted, and include areas V2 and PO. Both 7a and 7m are connected with the motion visual areas of the upper bank of the superior temporal sulcus (VMC), and area 7a has in addition strong connections with the STP area. The connections of each subdivision with the various visual areas are reciprocal and selective, involving particular portions of each. For example, the anterior part of area PO, containing the representation of the upper visual field, is preferentially connected with 7m and 7a, whereas posterior PO, where the lower visual field is mapped, is connected with 7ip. Area 7m departs from the other subdivisions in that it is also connected to somatosensory areas, including SSA and area 5 . Common among the sensory affiliations of all three area 7 subdivisions is their linkage with visual areas, Or portions thereof, where the periphery Of the visual field is mapped (v2, v3, Po), and with areas involved in the analysis of visual motion (MT,

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MTp, FST, VMC). These connections are likely to make a major contribution to the analysis of movement and spatial relationships of the visual world, the latter for a long time attributed to the posterior parietal cortex (Mishkin et al., 1983; Van Essen and Maunsell, 1983), and whose impairment may underlie at least part of the visual neglect syndrome that follows parietal damage. It is important to add, however, that the posterior parietal subdivisions, most prominently 7ip and 7a, are not exclusively connected with cortices in the “dorsal” visuospatial pathway. Both areas are strongly and selectively linked with the STP area,

-

and 7ip has additional connections with the IT cortex. These two temporalvisual regions are within the “ventral” object recognition visual pathway, therefore suggesting that areas 7ip and 7a have access to information being processed not only in the dorsal spatial, but also in the ventral object recognition visual pathways. This anatomical concurrence of processing streams in two parietal subdivisions adds to the growing evidence of such intermingling at earlier levels of the visual cortico-cortical hierarchy (DeYoe and Van Essen, 1988; Krubitzer and Kaas, 1990;Maunsell et al., 1990;Felleman and Van Essen, 1991).

Superior Colliculus

Pons: DLPN, LPN, PPN € DPN i

Pons: LPN, DLPN, PPN & DPN

Superior Colliculus

Pons: DLPN, LPN, VPN, PMPN, PPN & DPN

Colliculus

Fig. 9. Topography of the connections from areas 7ip, 7a and 7m to the superior colliculus and pons. The territories receiving the heaviest innervation from each subdivision are shown in bold type. The data used in this figure are from our own observations and the reports by Lynch et al. (1985; superior colliculus) and May and Andersen (1986; pons). Abbreviations: DPN, dorsaI pontinenucleus; DLPN, dorsolateral pontine nucleus; LPN, lateral pontine nucleus; VPN, ventral pontine nucleus; PMPN, paramedian pontine nucleus; PPN, peduncular pontine nucleus.

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Connections of areas 7ip, 7a and 7m with limbic and prefrontal areas The existence of limbic influences upon the posterior parietal cortex has long been suspected on the basis of the attentional deficits subsequent to parietal damage and of the importance of the stimulus significance to drive parietal units in conscious active monkeys. All three parietal areas, but most notably 7a and 7m, have strong and selective connections with a wide set of limbic and prefrontal areas (summarized in Fig. 6, and discussed in more detail in Cavada and Goldman-Rakic, 1989a,b). The connections with several components of the hippocampal formation, including the presubiculum, caudomedial lobule and parahippocampal areas TF and TH, give the posterior parietal cortex access to the memory processing functions in which these medial temporal regions are engaged. Perhaps one of the most revealing findings from our study is the remarkably precise circuitry connecting each of the three parietal areas with the prefrontal cortex. We found that each parietal subdivision was reciprocally connected with a distinct portion of the principal sulcus (Cavada and Goldman-Rakic,

1989b). Given the strong evidence now available that this area of prefrontal cortex is critical for visuospatial working memory, the strong connections with the visual spatial centers of the parietal cortex are likely the major source of visuospatial information to this frontal area. Moreover, these connections appear to form a major component of a wider network of areas dedicated to spatial cognition (Selemon and Goldman-Rakic, 1988). Finally, our findings imply that subareas of the principal sulcus may perform specific subfunctions related to their unique parietal inputs.

Connections of areas 7ip, 7a and 7m with motor cortices The defects in eye movements that accompany posterior parietal damage, and the physiological properties of neurons in area 7 discussed at the beginning of this chapter strongly suggest that the posterior parietal cortex is involved in motor functions. In the anatomical domain, this suggestion is supported by the posterior parietal connections with a number of areas in the frontal lobe (see Fig. 6 and Cavada and Goldman-Rakic, 1989b), and with

Fig. 10. Darkfield photomicrographs of coronal sections through the pons showing the nuclei labeled from HRP-WGA injections in areas 7ip ( A ) ,7a (B) and 7m (C). Abbreviations as in Fig. 9. The calibration bar is the same for all three micrographs.

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several subcortical motor centers. Probably the most prominent connections of the parietal subdivisions with motor areas, especially of 7ip, but also of 7a and 7m, are with the FEF and SEF cortices, which are specifically involved in the motor control of the eyes and head (Bruce and Goldberg, 1984; Van der Steen et al., 1986; Lynch, 1987; Schlag and SchlagRey, 1987). As is the case in relation to the connections of the parietal subdivisions with sensory, limbic and prefrontal areas, those with motor cortices are selective for each subdivision. For instance, the heaviest links of area 7ip are with the posterior part of the FEF. Only from this sector can low-threshold saccades be elicited by intracortical stimulation (Bruce et al., 1985; Huerta et al., 1986). From the rostra1 part of the FEF, connected with 7a and 7m, high-threshold saccades are obtained, and cortical lesions that include this region produce impairments in eye-head coordination (Robinson and Fuchs, 1969; Bruceet al., 1985;Van der Steen et al., 1986).

Connections of areas 7ip, 7a and 7rn with subcortical motor centers: striatum, superior colliculus, and pons

The connections of areas 7ip, 7a and 7m with the neostriatum are summarized in Fig. 7; Fig. 8 shows representative examples of the striatal territories strongly innervated by each subdivision. Although each area projects to a large antero-posterior extent of both the putamen and the caudate nucleus, including its head, body and tail, the connections are particularly concentrated in some striatal zones. Thus, the main striatal targets of areas 7a and 7m are in the head and anterior part of the body of the caudate nucleus, with area 7a represented more medially than 7m. However, the main target zone of area 7ip in the caudate nucleus includes a sizeable part of the body, with the exclusion only of the most medial part. It is remarkable that this same zone of the caudate nucleus holds the highcst concentration of neurons with activities related to saccadic eye movements (Hikosaka et al., 1989). Area 7ip is also the parietal subdivision that projects most heavily to the superior colliculus (Lynch et al., 1985; Fig. 9),

where neurons discharge before saccades (Hikosaka and Wurtz, 1983). In addition to their output to the striatum and superior colliculus, a further pathway by which the parietal cortex may influence motor performance is via the pontine nuclei, which receive substantial projections from all three areas 7ip, 7a and 7m, specified in Fig. 9. Presumably the pontine territories specifically innervated by each subdivision have selective cerebellar, and in turn thalamic and cortical, targets. However, the precise organization of the sequence of neural connections arising from each parietal territory and impinging upon specific subcortical targets remains an open question at present.

Area 7 as a mosaic of fields integrated in diverse visual and visuo-motor networks The selective constellations formed by the cortical and subcortical structures connected with areas 7ip, 7a and 7m support the conclusion that each subdivision participates in different distributed neural networks engaged in complex visual and visuo-motor functions. The 7ip network, in particular, includes a number of cortical and subcortical regions involved in the analysis of the visual space, visual motion and in oculo-motor functions. The functional domains of the 7a and 7m netw orks are less well defined, but we have shown that each engages unique sets of visual areas, in addition to specific limbic and motor structures. The connectional heterogeneity of the three area 7 subdivisions analyzed here leads to a depiction of the posterior parietal cortex, classically labeled as association cortex, as a complex mosaic of different areas with specific sensory, limbic and motor attributes. Moreover, this topographic diversity is likely the basis for the variety of disorders that follow damage to the posterior parietal cortex.

Acknowledgements The experiments leading to this study were made

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while CC was at Yale University sponsored by Fogarty International Fellowship TW03445. This work was supported by MH 38546 and MH 00298.

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