Trends in Cognitive Sciences
Comparative mapping of higher visual areas in monkeys and humans
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)
- et al.
Neural mechanisms of form and motion processing in the primate visual system
Neuron
(1994) - et al.
fMR-adaptation: a tool for studying the functional properties of human cortical neurons
Acta Psychol. (Amst.)
(2001) Visual motion processing investigated using contrast-agent enhanced fMRI in awake behaving monkeys
Neuron
(2001)Stereopsis activates V3A and caudal intraparietal areas in macaques and humans
Neuron
(2003)Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI
Neuropsychologia
(2003)Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans
Neuron
(2004)Three-dimensional shape representation in monkey cortex
Neuron
(2002)Integration of local features into global shapes: monkey and human fMRI studies
Neuron
(2003)Mapping visual cortex in monkeys and humans using surface-based atlases
Vision Res.
(2001)Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe
Neuron
(2002)
Differential processing of objects under various viewing conditions in the human lateral occipital complex
Neuron
Human cortical regions involved in extracting depth from motion
Neuron
The topography of high-order human object areas
Trends Cogn. Sci.
Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys
Neuron
Nature versus nurture revisited: an old idea with a new twist
Prog. Neurobiol.
A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus)
Brain Res.
Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla
NeuroImage
How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey
J. Neurosci.
Selective attention gates visual processing in the extrastriate cortex
Science
Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task
J. Neurosci.
Motion perception: seeing and deciding
Proc. Natl. Acad. Sci. U. S. A.
Neurophysiological investigation of the basis of the fMRI signal
Nature
Functional imaging of the monkey brain
Nat. Neurosci.
Functional MRI of macaque monkeys performing a cognitive set-shifting task
Science
Extracting 3D from motion: Differences in human and monkey intraparietal cortex
Science
Faces and objects in macaque cerebral cortex
Nat. Neurosci.
The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys
J. Neurosci.
Motion processing in the macaque: revisited with functional magnetic resonance imaging
J. Neurosci.
Visual areas in macaque cortex measured using functional magnetic resonance imaging
J. Neurosci.
Language discrimination by human newborns and by cotton-top tamarin monkeys
Science
Species-specific calls evoke asymmetric activity in the monkey's temporal poles
Nature
Visualizing the neural bases of a disconnection syndrome with diffusion tensor imaging
J. Cogn. Neurosci.
Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey
J. Comp. Neurol.
Cited by (484)
Two fine-scale channels for encoding motion and stereopsis within the human magnocellular stream
2023, Progress in NeurobiologyThe marmoset as a model for investigating the neural basis of social cognition in health and disease
2022, Neuroscience and Biobehavioral Reviews