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

References (78)

  • Van Essen, D. (2004) Organization of visual areas in macaque and human cerebral cortex. In The Visual Neurosciences...
  • R. Vogels et al.

    How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey

    J. Neurosci.

    (1990)
  • J. Moran et al.

    Selective attention gates visual processing in the extrastriate cortex

    Science

    (1985)
  • J.M. Fuster et al.

    Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task

    J. Neurosci.

    (1982)
  • M.N. Shadlen et al.

    Motion perception: seeing and deciding

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • Kaas, J.H. (2004) The evolution of the visual system in primates. In The Visual Neurosciences (Vol. 2), (Chalupa, L.M....
  • D. Van Essen et al.

    Neural mechanisms of form and motion processing in the primate visual system

    Neuron

    (1994)
  • N.K. Logothetis

    Neurophysiological investigation of the basis of the fMRI signal

    Nature

    (2001)
  • K. Grill-Spector et al.

    fMR-adaptation: a tool for studying the functional properties of human cortical neurons

    Acta Psychol. (Amst.)

    (2001)
  • N.K. Logothetis

    Functional imaging of the monkey brain

    Nat. Neurosci.

    (1999)
  • Orban, G.A. (2002) Functional MRI in the awake monkey: the missing link. (Editorial). J. Cogn. Neurosci. 14,...
  • K. Nakahara

    Functional MRI of macaque monkeys performing a cognitive set-shifting task

    Science

    (2002)
  • W. Vanduffel

    Extracting 3D from motion: Differences in human and monkey intraparietal cortex

    Science

    (2002)
  • W. Vanduffel

    Visual motion processing investigated using contrast-agent enhanced fMRI in awake behaving monkeys

    Neuron

    (2001)
  • D.Y. Tsao

    Stereopsis activates V3A and caudal intraparietal areas in macaques and humans

    Neuron

    (2003)
  • D.Y. Tsao

    Faces and objects in macaque cerebral cortex

    Nat. Neurosci.

    (2003)
  • D. Fize

    The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys

    J. Neurosci.

    (2003)
  • G.A. Orban

    Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI

    Neuropsychologia

    (2003)
  • Denys, K. et al. The processing of visual shape in the cerebral cortex of human and nonhuman primates: an fMRI study....
  • Denys, K. et al. Strong visual activation in monkey but not human prefrontal cortex. J. Cogn. Neurosci. (in...
  • M. Koyama

    Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans

    Neuron

    (2004)
  • A.S. Tolias

    Motion processing in the macaque: revisited with functional magnetic resonance imaging

    J. Neurosci.

    (2001)
  • M.E. Sereno

    Three-dimensional shape representation in monkey cortex

    Neuron

    (2002)
  • A.A. Brewer

    Visual areas in macaque cortex measured using functional magnetic resonance imaging

    J. Neurosci.

    (2002)
  • Z. Kourtzi

    Integration of local features into global shapes: monkey and human fMRI studies

    Neuron

    (2003)
  • F. Ramus

    Language discrimination by human newborns and by cotton-top tamarin monkeys

    Science

    (2000)
  • A. Poremba

    Species-specific calls evoke asymmetric activity in the monkey's temporal poles

    Nature

    (2004)
  • N. Molko

    Visualizing the neural bases of a disconnection syndrome with diffusion tensor imaging

    J. Cogn. Neurosci.

    (2002)
  • J.W. Lewis et al.

    Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey

    J. Comp. Neurol.

    (2000)
  • M.I. Sereno

    Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging

    Science

    (1995)
  • S. Zeki

    A direct demonstration of functional specialization in human visual cortex

    J. Neurosci.

    (1991)
  • R.B. Tootell

    Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging

    J. Neurosci.

    (1995)
  • E.A. DeYoe

    Mapping striate and extrastriate visual areas in human cerebral cortex

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • A.C. Huk

    Retinotopy and functional subdivision of human areas MT and MST

    J. Neurosci.

    (2002)
  • D.C. Van Essen

    Mapping visual cortex in monkeys and humans using surface-based atlases

    Vision Res.

    (2001)
  • S.V. Astafiev

    Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing

    J. Neurosci.

    (2003)
  • Z. Kourtzi et al.

    Cortical regions involved in perceiving object shape

    J. Neurosci.

    (2000)
  • O. Simon

    Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe

    Neuron

    (2002)
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