Comparative mapping of higher visual areas in monkeys and humans

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Abstract

The advent of functional magnetic resonance imaging (fMRI) in non-human primates has facilitated comparison of the neurobiology of cognitive functions in humans and macaque monkeys, the most intensively studied animal model for higher brain functions. Most of these comparative studies have been performed in the visual system. The early visual areas V1, V2 and V3, as well as the motion area MT are conserved in humans. Beyond these areas, differences between human and monkey functional organization are increasingly evident. At the regional level, the monkey inferotemporal and intraparietal complexes appear to be conserved in humans, but there are profound functional differences in the intraparietal cortex suggesting that not all its constituent areas are homologous. In the long term, fMRI offers opportunities to compare the functional anatomy of a variety of cognitive functions in the two species.

Section snippets

Complications in relating human fMRI to monkey studies

Even in this favorable case of the visual system, establishing the relationship between non-invasive functional imaging in humans and invasive single-cell, lesion or anatomical studies in monkeys is far from straightforward. Making comparisons across species and techniques raises several challenges (see Box 1). Humans and macaques diverged from a small-brained common ancestor ∼30 million years ago [7]. Because the ensuing expansion of cerebral cortex was far greater in the human lineage, the

Monkey fMRI fills a missing link

Monkey fMRI [11], particularly in the awake monkey, should accelerate progress on many of these questions [12]. It allows comparison of fMRI signals with single-cell properties such as selectivity or adaptation in the same individual. Furthermore, fMRI-based functional neuroanatomy (localization of functional properties in the brain) can be compared directly in humans and monkey 13, 14. The main focus of this review is on the latter question as applied to the visual system. A growing number of

Defining cortical areas

Cortical visual areas have been identified using one or more among four major criteria: (1) cyto- and myeloarchitecture, (2) connectivity, (3) retinotopic organization and (4) function, as revealed by single-cell, lesion and neuroimaging analyses. Each of these criteria has significant limitations and does not apply equally well to all regions or across species. For example, some areas lack clear retinotopy, and cytoarchitectonic subdivisions are often very subtle. Connectivity studies are

Conserved early visual areas

As noted above, the retinotopic organization of early visual areas V1, V2 and V3 is similar in monkeys and humans 18, 25, 31, 34. fMRI has revealed important functional similarities in these early areas. These include similarities in local integration of line elements in V1 and V2 [26], in the effect of scrambling in V1 [20] (Figure 3c,d), and in the involvement of V2 and V3 in the extraction of 3D-structure from motion (SFM) [14] (Figure 5a,b).

Other studies have revealed modest species

Likely homology: area V3A

Human V3A has a retinotopic organization similar to that of monkey V3A: a complete representation of the visual field split by a horizontal meridian, which also adjoins V3d 18, 25, 42. This constitutes strong evidence for homology even in the face of evidence for significant divergence in function. V3A is stereo sensitive in both species 16, 45. However, as mentioned earlier, human V3A is motion sensitive [42], 2D-shape sensitive [46], and involved in the extraction of 3D SFM 14, 47 whereas

The IT complex: an example of ‘regional’ homology

The monkey IT complex and the human LO complex are relatively similar [20]. They are located in similar positions relative to neighboring regions (e.g. MT) in the brain, and they lack a clear retinotopic organization, yet there is some evidence for separate central representations in humans [55] and in monkeys 18, 25. On the one hand, in both species the activation by scrambled patterns decreases along a posterior-to-anterior gradient, object-related responses show adaptation 46, 66, 67, and

Conclusions

The macaque is the primary animal model for neurophysiological and lesion studies of cognitive functions. Monkey fMRI is essential for establishing informed relationships between human fMRI and a diverse portfolio of non-human primate data and can pave the way for enhanced progress in systems and cognitive neuroscience (see also Box 3). Despite several functional differences, many areas are homologous, especially at early levels of the visual hierarchy. In higher-order cortex, ‘regional’

Acknowledgements

This work would not have been possible without the technical support or help of R Vogels, K. Nelissen, K. Denys, D. Fize, H. Sawamura, H. Peuskens, M. De Paep, W. Depuydt, C. Franssen, A. Coeman, P. Kayenbergh, G. Meulemans, G. Vanparrys, Y. Celis, D. Hanlon and J. Harwell. The work was supported by the Queen Elizabeth medical foundation (GSKE), The medical council of Flanders (FWO, G 0112.00), Belgian Science Policy (IUAP P4/22 and P5/04), the regional ministry of education (GOA 2000/11), HFSP

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