Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

In primates, lesions of striate cortex (V1) result in scotomas in which only rudimentary visual abilities remain. These aspects of vision that survive V1 lesions have been attributed to direct thalamic pathways to extrastriate areas, including the middle temporal area (MT). However, studies in New World monkeys and humans have questioned this interpretation, suggesting that remnants of V1 are responsible for both the activation of MT and residual vision. We studied the visual responses of neurons in area MT in New World marmoset monkeys in the weeks after lesions of V1. The extent of the scotoma in each case was estimated by mapping the receptive fields of cells located near the lesion border and by histological reconstruction. Two response types were observed among the cells located in the part of MT that corresponds, in visuotopic coordinates, to the lesioned part of V1. Many neurons (62%) had receptive fields that were displaced relative to their expected location, so that they represented the visual field immediately surrounding the scotoma. This may be a consequence of a process analogous to the reorganization of the V1 map after retinal lesions. However, another 20% of the cells had receptive fields centered inside the scotoma. Most of these neurons were strongly direction-selective, similar to normal MT cells. These results show that MT cells differ in their responses to lesioning of V1 and that only a subpopulation of MT neurons can be reasonably linked to residual vision and blindsight.

[1]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  M G Rosa,et al.  Monocular focal retinal lesions induce short–term topographic plasticity in adult cat visual cortex , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  K. Rockland,et al.  Single axon analysis of pulvinocortical connections to several visual areas in the Macaque , 1999, The Journal of comparative neurology.

[4]  A. Cowey,et al.  Blindsight in monkeys , 1995, Nature.

[5]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

[6]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[7]  W. B. Spatz,et al.  Distribution of cytochrome oxidase and parvalbumin in the primary visual cortex of the adult and neonate monkey, Callithrix jacchus , 1994, The Journal of comparative neurology.

[8]  T. Robbins,et al.  Distribution of seven major neurotransmitter receptors in the striate cortex of the new world monkey callithrix jacchus , 1993, Neuroscience.

[9]  M. Rosa,et al.  Responsiveness of cat area 17 after monocular inactivation: limitation of topographic plasticity in adult cortex. , 1995, The Journal of physiology.

[10]  M G Rosa,et al.  Retinotopic orgarnzation of the primary visual cortex of flying foxes (Pteropus poliocephalus and pteropus scapulatus) , 1993, The Journal of comparative neurology.

[11]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[12]  David Troilo,et al.  Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus) , 1993, Vision Research.

[13]  L. Weiskrantz,et al.  Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[15]  L. Weiskrantz Blindsight : a case study and implications , 1986 .

[16]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. I. A changing space for synaptogenesis , 1993, The Journal of comparative neurology.

[17]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[18]  Jean Bullier,et al.  The Role of Area 17 in the Transfer of Information to Extrastriate Visual Cortex , 1994 .

[19]  C. Gilbert,et al.  Long‐term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. , 1993, The Journal of physiology.

[20]  J. Bullier,et al.  Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. , 1989, Journal of neurophysiology.

[21]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[22]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[23]  Michael S. Gazzaniga,et al.  Blindsight Reconsidered , 1994 .

[24]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

[25]  J. Kaas,et al.  Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? , 1999, The European journal of neuroscience.

[26]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Perenin,et al.  Discrimination of motion direction in perimetrically blind fields. , 1991, Neuroreport.

[28]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[29]  M. Gazzaniga,et al.  Residual vision in a scotoma: implications for blindsight. , 1992, Science.

[30]  L. Schmued A rapid, sensitive histochemical stain for myelin in frozen brain sections. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[31]  A. Cowey PROJECTION OF THE RETINA ON TO STRIATE AND PRESTRIATE CORTEX IN THE SQUIRREL MONKEY, SAIMIRI SCIUREUS. , 1964, Journal of neurophysiology.

[32]  Alison M. Harman,et al.  Blindsight in Subjects with Homonymous Visual Field Defects , 1999, Journal of Cognitive Neuroscience.

[33]  M. Rosa,et al.  Visuotopic reorganization in the primary visual cortex of adult cats following monocular and binocular retinal lesions. , 1996, Cerebral cortex.

[34]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[35]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[36]  R B Tootell,et al.  Organization of intrinsic connections in owl monkey area MT. , 1997, Cerebral cortex.

[37]  J. Kaas,et al.  Area 17 lesions deactivate area MT in owl monkeys , 1992, Visual Neuroscience.

[38]  M G Rosa,et al.  Visual areas in the dorsal and medial extrastriate cortices of the marmoset , 1995, The Journal of comparative neurology.

[39]  R. Born,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1993, Nature.

[40]  Y. Chino Adult plasticity in the visual system. , 1995, Canadian journal of physiology and pharmacology.

[41]  L. Weiskrantz Blindsight revisited , 1996, Current Opinion in Neurobiology.