Cerebral Achromatopsia in Monkeys

In human cerebral achromatopsia, extrastriate cortical damage produces a severe or complete loss of colour vision, with relative sparing of non‐chromatic vision. The critical lesion appears to be in a medial occipito‐temporal area, occupying the lingual and caudal fusiform gyri; positron emission tomography has shown that this cortical region is one of several activated in normal human observers during colour vision tasks. Attempts to find an analogous ‘colour centre’ in the cortex of monkeys have not been successful. In particular, ablation of cortical area V4, sometimes thought on physiological grounds to be more involved in wavelength and colour coding than any other visual cortical area, produces only mild impairments in colour discrimination. In the present study we tested the colour vision of monkeys after cortical ablations that mainly or entirely spared area V4. One group of monkeys (group AT) received ablations in the temporal lobe anterior to area V4, and a second group (group MOT) received ablations in a medial occipito‐temporal area roughly corresponding in cranial location to the lesion that produces human cerebral achromatopsia. The animals in group MOT showed no impairment of their colour vision. Group AT, in contrast, had a severe impairment in chromatic vision, with a relative sparing of non‐chromatic vision. Their behaviour was indistinguishable from that of a human patient with total cerebral achromatopsia who had been tested on the same tasks. These results show that area V4 in macaque monkeys is not analogous, and probably not homologous, to the human colour centre. Instead, they suggest that the area of the monkey's brain corresponding to the colour area in the human brain is in the temporal cortex, anterior to area V4.

[1]  C. Gross,et al.  How inferior temporal cortex became a visual area. , 1994, Cerebral cortex.

[2]  Peter H. Schiller,et al.  Area V4 of the Primate Visual Cortex , 1994 .

[3]  S. Clarke,et al.  Modular Organization of Human Extrastriate Visual Cortex: Evidence from Cytochrome Oxidase Pattern in Normal and Macular Degeneration Cases , 1994, The European journal of neuroscience.

[4]  F. Newcombe,et al.  On the role of parvocellular (P) and magnocellular (M) pathways in cerebral achromatopsia. , 1994, Brain : a journal of neurology.

[5]  J H Maunsell,et al.  Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Merigan Wh Colour vision: human V4? , 1993, Current biology : CB.

[7]  S. R. Butler,et al.  The effects of V4 lesions on the visual abilities of macaques: hue discrimination and colour constancy , 1993, Behavioural Brain Research.

[8]  David Gaffan,et al.  A Spurious Category-Specific Visual Agnosia for Living Things in Normal Human and Nonhuman Primates , 1993, Journal of Cognitive Neuroscience.

[9]  S. R. Butler,et al.  The effects of lesions of area V4 on the visual abilities of macaques: colour categorization , 1992, Behavioural Brain Research.

[10]  A. Cowey,et al.  Cortical area V4 and its role in the perception of color , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  S Yamane,et al.  Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  A. Cowey,et al.  The role of the 'face-cell' area in the discrimination and recognition of faces by monkeys. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  F. Newcombe,et al.  Chromatic Discrimination in a Cortically Colour Blind Observer , 1991, The European journal of neuroscience.

[14]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  P. H. Schiller,et al.  The role of the primate extrastriate area V4 in vision. , 1991, Science.

[16]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  D. Foster Inherited and acquired colour vision deficiencies : fundamental aspects and clinical studies , 1991 .

[18]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[19]  S. Zeki,et al.  A century of cerebral achromatopsia. , 1990, Brain : a journal of neurology.

[20]  John P. Aggleton,et al.  Visual impairments in macaques following inferior temporal lesions are exacerbated selectively by additional damage to superior temporal sulcus , 1990, Behavioural Brain Research.

[21]  N. Logothetis,et al.  Functions of the colour-opponent and broad-band channels of the visual system , 1990, Nature.

[22]  J. D. Mollon,et al.  The club-sandwich mystery , 1990, Nature.

[23]  Karl J. Friston,et al.  The colour centre in the cerebral cortex of man , 1989, Nature.

[24]  A. Cowey,et al.  On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  A. Cowey,et al.  A case study of cortical colour "blindness" with relatively intact achromatic discrimination. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[26]  David Gaffan,et al.  Visual Identification following Inferotemporal Ablation in the Monkey , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[27]  D. Gaffan,et al.  Single and Concurrent Discrimination Learning by Monkeys after Lesions of Inferotemporal Cortex , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[28]  W. Cowan,et al.  A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[29]  H. Lipp,et al.  Hereditary covariations of neuronal circuitry and behavior: Correlations between the proportions of hippocampal synaptic fields in the regio inferior and two-way avoidance in mice and rats , 1983, Behavioural Brain Research.

[30]  A. Damasio,et al.  Central achromatopsia , 1980, Neurology.

[31]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[32]  J. C. Meadows Disturbed perception of colours associated with localized cerebral lesions. , 1974, Brain : a journal of neurology.

[33]  M. Wilson,et al.  Visual identification and memory in monkeys with circumscribed inferotemporal lesions. , 1972, Journal of comparative and physiological psychology.

[34]  C. Gross,et al.  Further analysis of visual discrimination deficits following foveal prestriate and inferotemporal lesions in rhesus monkeys. , 1971, Journal of comparative and physiological psychology.