The Visual Parietal Areas in the Macaque Monkey: Current Structural Knowledge and Ignorance

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1 NeuroImage 14, S21 S26 (2001) doi: /nimg , available online at on The Visual Parietal Areas in the Macaque Monkey: Current Structural Knowledge and Ignorance Carmen Cavada 1 Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, Madrid, Spain Received November 24, 2000 Classic and current parcellations of the posterior parietal cortex are reviewed. Whereas earlier studies relied on subjective observation of cortical cytoarchitecture, present parcellations are mostly based on connectional and physiological criteria. These criteria have led to the identification of five areas in the intraparietal sulcus with alleged visual function: VIP, MIP, PIP, AIP, and LIP. Other visual parietal areas are 7a, in the lateral parietal surface, and, in the medial parietal wall, 7m, and V6A. Present knowledge of the dimensions, boundaries, and connections of the various visual parietal areas is uneven: whereas LIP, 7a, and 7m have been extensively explored in anatomical and physiological studies, only scant information is available for most of the intraparietal areas. It is suggested that future studies address the anatomical and functional parcellation of the posterior parietal cortex using manifold objective means of study that allow comparison by independent researchers Academic Press INTRODUCTION The identification of parietal areas has relied on different criteria over time. The initial studies were based on cytoarchitectural observations and led to various parcellations of the parietal cortical surface. At present, the parcellation of the parietal cortex is based on identification of areas with specific functions; therefore, data from connections and physiological recordings are additionally, or preferentially, considered. ARCHITECTONIC PARCELLATION OF POSTERIOR PARIETAL CORTEX The primate anterior parietal cortex holds the primary somatosensory cortex while the posterior parietal 1 Address correspondence and reprint requests to author at Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, Arzobispo Morcillo s/n, Madrid, Spain. Fax: (34) carmen.cavada@uam.es. cortex holds association areas involved in somatosensory and visual processing. In the macaque monkey the posterior parietal cortex extends through the posterior part of the anterior parietal lobule, both banks of the intraparietal sulcus, and the posterior parietal lobule. The cytoarchitecture of this wide cortical region has been studied by different anatomists who, over time, have reached increasingly complex and not always compatible conclusions (Fig. 1). Brodmann identified in the monkey posterior parietal cortex areas 5 and 7, with the intraparietal sulcus mostly sandwiched between them, and proposed that both areas extended onto the medial surface of the hemisphere (Brodmann, 1909). The Vogts further subdivided areas 5 and 7 into areas 5a and 5b and 7a and 7b (Vogt and Vogt, 1919) (Fig. 1). The more recent studies by Von Bonin and Bailey (1947) and Pandya and Seltzer (1982) use Von Economo s (1929) lettering nomenclature. Von Bonin and Bailey, like the Vogts, recognized two areas in both the anterior and the posterior parietal lobules. However, Von Bonin and Bailey, unlike Brodmann, considered the cortex in the medial parietal wall to be comparable to the anterior parietal lobule cortex but not to the posterior parietal lobule cortex. The view of Pandya and Seltzer was closer to that of Brodmann regarding most of the medial parietal cortex. Pandya and Seltzer identified still more subdivisions in the posterior parietal cortex, including specific areas in the cingulate, intraparietal, and superior temporal sulci (Fig. 1). The diversity of maps proposed by different authors on the basis of cytoarchitectonic observations illustrates how uncertain this approach is. The future for structural parcellation of the cerebral cortex should attempt to establish sound grounds for consensus among different investigators. I consider the approach proposed by Schleicher and colleagues (1999) very promising. It is an observer-independent, quantitative method for analyzing cortical cytoarchitecture. A modern standard operating procedure to study cerebral architectonics should be based, first, on a manifold outlook, that is, analysis of cyto-, myelo-, and chemo- S /01 $35.00 Copyright 2001 by Academic Press All rights of reproduction in any form reserved.

2 S22 CARMEN CAVADA FIG. 1. Parcellations of the monkey posterior parietal cortex based on cytoarchitectonics [Cercopithecus in Brodmann (1909) and Vogt and Vogt (1919); Macaca in Von Bonin and Bailey (1947) and Pandya and Seltzer (1982)]. architectures with a battery of markers, and second, and probably more important, on the use of common tools for analysis by different investigators so as to achieve conclusions that are as objective and concordant as possible. VISUAL PARIETAL AREAS Architectonic knowledge alone is, of course, insufficient to assign a function to the areas identified. In fact, the present parcellation into posterior parietal areas with a known visual function for the most part relies on data from connections and is supported by neurophysiological studies. Figure 2 shows a current parcellation of the lateral and medial parietal surfaces, in which the areas with known visual function are indicated. This parcellation is derived from a complete parcellation of the macaque cerebral cortex published recently (Cavada et al., 2000). There are five areas in the intraparietal sulcus. Their names allude to their location rather than to earlier architectonic parcellations: VIP, ventral intraparietal; MIP, medial intraparietal; PIP, posterior intraparietal; AIP, anterior intraparietal; LIP, lateral

3 VISUAL AREAS IN MACAQUE PARIETAL CORTEX S23 FIG. 2. A current parcellation of the visual parietal cortex in the macaque monkey. This parcellation is based on diverse criteria (cytoarchitecture, connections, and physiological recording data). The names in bold type allude to areas attributed with visual function. The bases for their identification are given in the text. Relevant sulci are schematically depicted open with their banks in a dark shade of gray (IPS, intraparietal sulcus; LS, lunate sulcus; POS, parietooccipital sulcus; STS, superior temporal sulcus). Synonyms for several areas appear next to the enlarged lateral and medial views of the parietal cortex (top right and bottom left, respectively). intraparietal. These areas have been recognized on the basis of some particular connections or on the basis of their cellular responses. Thus, VIP was identified by Maunsell and Van Essen (1983) as the target of projections from areas MT (middle temporal) and V2. As in area VIP, connections were the original grounds for identifying MIP and PIP as specific areas: they were designated by Colby and colleagues (1988) based on their connections with visual area PO, or V6 (plus a narrow rim of the currently recognized V6A, see below). Even though Colby, Duhamel, and their colleagues have also studied neuronal activity in VIP and MIP, their boundaries, as well as those of PIP, are still not well defined. Both visual and somatosensory responses can be recorded in VIP and MIP; VIP is thought to represent perioral space and MIP, immediate extrapersonal space (Colby and Duhamel, 1991; Duhamel et al., 1997; reviewed in Colby and Goldberg, 1999). Area AIP has been designated and studied neurophysiologically principally by Sakata and colleagues who, based on neuronal responses in behavioral situa-

4 S24 CARMEN CAVADA tions, have suggested that it is a hand manipulation region (Sakata et al., 1995, 1998). Paraphrasing Colby and Goldberg (1999), AIP may contribute to a spatial representation dedicated to the visual guidance of grasping with the hand. Areas LIP and 7a are far better known than the aforementioned. LIP is the parietal eye field; it has received a lot of attention from both anatomical and neurophysiological points of view (Cavada and Goldman-Rakic, 1989a,b, 1991, 1993; Andersen et al., 1990a,b; Blatt et al., 1990; Barash et al., 1991; Mazzoni et al., 1996a,b; Bracewell et al., 1996; Stricanne et al., 1996; Thier and Andersen, 1998; Li et al., 1999; Grunewald et al., 1999; Linden et al., 1999). The same is true for area 7a, whose connections are well known and whose neuronal responses were investigated early in the classic studies by Hyvärinen, Mountcastle, Lynch, Robinson, and their colleagues (Mountcastle et al., 1975; Lynch et al., 1977; Robinson et al., 1978; Hyvärinen and Shelepin, 1979; Hyvärinen, 1982; Cavada and Goldman-Rakic, 1989a,b, 1991, 1993). On the medial parietal surface we find areas V6, V6A, and 7m. Areas V6 and V6A have been studied principally by Galletti and colleagues (1996, 1999a,b; Matelli et al., 1998). The designation of V6 was published by Zeki in In 1988 Colby and colleagues studied the connections of areas V6 and V6A (at that time V6 and the adjacent part of V6A were considered a single area, then called PO, or parietooccipital) and demonstrated that they were linked to a constellation of visual areas, including V1. The anatomical and physiological investigations by Galletti s group (1996, 1999a,b) have revealed the dimensions and boundaries of V6 and V6A and have shown that both areas contain visual neurons whose responses are related to the orientation and direction of moving stimuli; in addition, V6A contains complex units that include neurons with craniotopic receptive fields and neurons related to attention. Based on these studies and the fact that only V6 shows retinotopic organization, V6 can be considered a typical prestriate visual area, whereas the complexity of the recorded units in V6A argues for its inclusion among the parietal visual areas. Area 7m was so designated by us in an attempt to respect historical precedents and to use an internally consistent terminology for the various subdivisions of Brodmann s area 7 (Cavada and Goldman-Rakic, 1989a). We showed that, among a wider constellation of corticocortical connections, 7m is linked to visual cortices (Cavada and Goldman-Rakic, 1989a,b, 1993). Caminiti and colleagues (1997) have studied neuronal activity in 7m and proposed that its neurons were involved in the interactions between gaze angle and hand position in the visual field during hand reaching tasks. Thier and Andersen (1998) have evoked saccades by electrical microstimulation of a dorsal portion of 7m lying in the lower bank of the cingulate sulcus and adjacent convexity cortex. THE CONNECTIONS OF VISUAL PARIETAL AREAS Current knowledge of the complete sets of subcortical and cortical connections for the various visual parietal areas is uneven. Patricia Goldman-Rakic and I have extensively studied both the corticocortical and the subcortical connections of areas LIP (which we called 7ip), 7a, and 7m (Cavada and Goldman-Rakic, 1989a,b, 1991; the interested reader may find helpful the review in Cavada and Goldman-Rakic, 1993). The extensive work of Pandya and colleagues, in particular, and that of other authors as well, has also addressed the connections of these areas in depth (Mesulam et al., 1977; Pandya and Seltzer, 1982; Seltzer and Pandya, 1984, 1986; Petrides and Pandya, 1984; Yeterian and Pandya, 1985, 1993; Andersen et al., 1990b; Schmahmann and Pandya, 1990). In contrast, no studies have been aimed at revealing the complete sets of connections of VIP, MIP, PIP, and AIP. A possible reason is that these areas are located in the banks and fundus of the intraparietal sulcus and are therefore difficult for anatomical investigation to approach. Uncertainty about their boundaries and the burden of comprehensive hodological studies may also contribute to the lack of connectional information on the intraparietal visual areas. The connections of the medial parietal visual areas have been reported with diverse detail. The subdivision of the original area PO into areas V6 and V6A argues for the necessity of further studies addressing their specific connections (see Colby et al., 1988; Matelli et al., 1998), including the subcortical connections (which are practically unknown). Regarding 7m, both its cortical and its major subcortical connections have been reported (see review in Cavada and Goldman-Rakic, 1993). CONCLUDING REMARKS The evidence reviewed above shows that there is no objective parcellation of the macaque parietal cortex based on architectonic criteria. In fact, the currently accepted visual parietal areas have been, for the most part, identified on the basis of criteria other than their architecture, i.e., connections with prestriate visual areas and recordings of neuronal responses to visual and other sensory stimuli. Moreover, present knowledge of the connections of the visual parietal areas with subcortical regions and other cortical areas is far from complete. The parcellation and functional understanding of the primate posterior parietal cortex should rely on as many sources of information as possible. Novel, objec-

5 VISUAL AREAS IN MACAQUE PARIETAL CORTEX S25 tive, and comprehensive approaches are needed to unveil the architecture of the posterior parietal cortex, and attempts should be made to correlate the identified territories with those characterized by specific connections and physiological activity. ACKNOWLEDGMENTS This work was supported by Grants BIOTECH ERB-BIO4-CT from the European Commission and PB from the Ministry of Education and Culture, Spain. REFERENCES Andersen, R. A., Asanuma, C., Essick, G., and Siegel, R. M. 1990a. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J. Comp. Neurol. 296: Andersen, R. A., Bracewell, R. M., Barash, S., Gnadt, J. W., and Fogassi, L. 1990b. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J. Neurosci. 10: Barash, S., Bracewell, R. M., Fogassi, L., Gnadt, J. W., and Andersen, R. A. 1991a. 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