Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-24T01:45:36.491Z Has data issue: false hasContentIssue false

Removal of two halves restores the whole: Reversal of visual hemineglect during bilateral cortical or collicular inactivation in the cat

Published online by Cambridge University Press:  02 June 2009

Stephen G. Lomber
Affiliation:
Laboratory for Visual Perception and Cognition, Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
Bertram R. Payne
Affiliation:
Laboratory for Visual Perception and Cognition, Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston

Abstract

The purpose of the present study was to compare visual orienting behavior in the adult cat during (1) unilateral and bilateral cooling deactivation of posterior-middle suprasylvian (pMS) sulcai cortex, and (2) unilateral and bilateral deactivation of the superior colliculus. As expected, unilateral cooling deactivation of either pMS cortex or the superior colliculus resulted in a profound visual neglect of the contracooled hemifield. The addition of cooling the homotopic region in the opposite hemisphere largely reversed this deficit and restored visual orienting into the previously neglected hemifield. These results show that (1) pMS cortex and the superior colliculus are essential for normal detection and orienting to visual targets, and (2) unilateral visual neglect results from an imbalance of activities in the two hemispheres induced at either cortical or subcortical levels. These conclusions have implications for understanding neural bases of visual hemineglect following unilateral lesions in humans.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrews, E.J., Bennett, B.T., Clark, J.D., Houpt, K.A., Pascoe, P.J., Robinson, G.W. & Boyce, J.R. (1993). Report of the American Veterinary Medical Association Panel on Euthanasia. Journal of the American Veterinary Medical Association 202, 229249.CrossRefGoogle Scholar
Bénita, M. & Condé, H. (1972). Effects of local cooling upon conduction and synaptic transmission. Brain Research 36, 133151.CrossRefGoogle ScholarPubMed
Boussaoud, D. & Joseph, J.P. (1985). Role of the cat substantia nigra pars reticulata in eye and head movements. II. Effects of local pharmacological injections. Experimental Brain Research 57, 297304.Google Scholar
Critchley, M. (1953). The Parietal Lobes. New York: Hefner.Google Scholar
Guitton, D. & Munoz, D. (1991). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. I. Identification, localization, and effects of behavior on sensory responses. Journal of Neurophysiology 66, 16051623.CrossRefGoogle ScholarPubMed
Hardy, S.C. & Stein, B.E. (1988). Small lateral suprasylvian cortex lesions produce visual neglect and decreased visual activity in the superior colliculus. Journal of Comparative Neurology 273, 527542.Google Scholar
Harris, L.R. (1980). The superior colliculus and movements of the head and eyes in cats. Journal of Physiology 300, 367391.CrossRefGoogle ScholarPubMed
Harting, J.K. & Van Lieshout, D.P. (1991). Spatial relationships of axons arising from the substantia nigra, spinal trigeminal nucleus, and pedunculopontine tegmental nucleus within the intermediate gray of the cat superior colliculus. Journal of Comparative Neurology 305, 543558.Google Scholar
Harting, J.K., Huerta, M.F., Weber, J.T. & Van Lieshout, D.P. (1988). Neuroanatomical studies of the nigrotectal projection in the cat. Journal of Comparative Neurology 278, 615631.CrossRefGoogle ScholarPubMed
Harting, J.K., Updyke, B.V. & Van Lieshout, D.P. (1992). Corticotectal projections in the cat: Anterograde transport studies of twentyfive cortical areas. Journal of Comparative Neurology 324, 379414.CrossRefGoogle ScholarPubMed
Hikosaka, O. & Wurtz, R.H. (1983 a). Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. Journal of Neurophysiology 49, 12301253.CrossRefGoogle ScholarPubMed
Hikosaka, O. & Wurtz, R.H. (1983 b). Visual and oculomotor functions of monkey substantia nigra pars reticulata. II. Visual responses related to fixation of gaze. Journal of Neurophysiology 49, 12541267.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1983 c). Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. Journal of Neurophysiology 49, 12851301.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1985 a). Modification of saccadic eye movements by GABA-related substances. 1. Effects of muscimol and bicuculline in monkey superior colliculus. Journal of Neurophysiology 53, 266291.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1985 b). Modification of saccadic eye movemnets by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. Journal of Neurophysiology 53, 292308.Google Scholar
Horel, J.A. (1984). Cold lesions in inferotemporal cortex produce reversible deficits in learning and retention of visual discriminations. Physiological Psychology 12, 259270.CrossRefGoogle Scholar
Horel, J.A. (1991). Use of cold to reversibly suppress local brain function in behaving animals. In Lesions and Transplantation: Methods in Neurosciences, Vol. 7, ed. Conn, R.M., pp. 97110. San Diego, New York: Academic Press.CrossRefGoogle Scholar
Jasper, H.H., Shacter, D.G. & Montplaisir, J. (1970). The effect of local cooling upon spontaneous and evoked electrical activity of cerebral cortex. Canadian Journal of Physiology and Pharmacology 48, 640652.Google Scholar
Joseph, J.P. & Boussaoud, D. (1985). Role of the cat substantia nigra pars reticulata in eye and head movements. I. Neural activity. Experimental Brain Research 57, 286296.Google Scholar
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 159, 319337.CrossRefGoogle Scholar
Keating, E.G. & Gooley, S.G. (1988). Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures. Brain Research 438, 247255.Google Scholar
Kinsbourne, M. (1987). Mechanisms of unilateral neglect. In Neurophysiological and Neuropsychological Aspects of Unilateral Neglect, ed. Jeannerod, M., pp. 6986. North-Holland: Elsevier.CrossRefGoogle Scholar
Lomber, S.G., Cornwell, P., Sun, J.S., MacNeil, M.A. & Payne, B.R. (1994). Reversible inactivation of visual processing operations in middle suprasylvian cortex of the behaving cat. Proceedings of the National Academy of Sciences of the U.S.A. 91, 29993003.CrossRefGoogle ScholarPubMed
Lomber, S.G., Payne, B.R. & Cornwell, P. (1996 a). Learning and recall of form discriminations during reversible cooling deactivation of ventral-posterior suprasylvian cortex in the cat. Proceedings of the National Academy of Sciences of the U.S.A. 33, 16541658.CrossRefGoogle Scholar
Lomber, S.G., Payne, B.R., Cornwell, P. & Long, K.D. (1996 b). Perceptual and cognitive visual functions of parietal and temporal cortices in the cat. Cerebral Cortex (in press).CrossRefGoogle Scholar
Long, K.D., Lomber, S.G. & Payne, B.R. (1996). Increased oxidative metabolism in middle suprasylvian cortex following removal of areas 17 & 18 in newborn cats. Experimental Brain Research 110, 335346.Google Scholar
McHaffie, J.G., Norita, M., Dunning, D.D. & Stein, B.E. (1993). Corticotectal relationships: Direct and “indirect” corticotectal pathways. Progress in Brain Research 95, 139150.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1981). A cortical network for directed attention and unilateral neglect. Annals of Neurology 10, 309325.CrossRefGoogle Scholar
Ogasawara, K., McHaffie, J.G. & Stein, B.E. (1984). Two visual corticotectal systems in cat. Journal of Neurophysiology 52, 12261245.CrossRefGoogle ScholarPubMed
Pasternak, T. & Merigan, W.H. (1994). Motion perception following lesions of the superior temporal sulcus in the monkey. Cerebral Cortex 4, 247259.Google Scholar
Payne, B.R. (1990). Representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex. Visual Neuroscience 4, 445474.CrossRefGoogle ScholarPubMed
Payne, B.R. & Lomber, S.G. (1996). Age dependent modification of cytochrome oxidase activity in the cat dorsal lateral geniculate nucleus following removal of primary visual cortex. Visual Neuroscience 13, 805816.CrossRefGoogle ScholarPubMed
Payne, B.R., Lomber, S.G., Geeraerts, S., van der Gucht, E. & Vandenbussche, E. (1996). Reversible visual hemineglect. Proceedings of the National Academy of Sciences of the U.S.A. 93, 290294.Google Scholar
Payne, B.R., Siwek, D.F. & Lomber, S.G. (1991). Complex transcallosal interactions in visual cortex. Visual Neuroscience 6, 283289.CrossRefGoogle ScholarPubMed
Posner, M.I. & Raichle, M.E. (1994). Images of Mind. New York: Freeman, p. 206.Google Scholar
Rafal, R.D. (1994). Neglect. Current Opinion in Neurobiology 4, 231236.Google Scholar
Reinoso-Suárez, F. (1961). Topographischer Hirnatlas der Katz fur experimentale physiologische Untersuchungen. [Topographical atlas of the cat brain for experimental-physiological research.] Darmstad, Federal Republic of Germany: Merck.Google Scholar
Rizzolatti, G. & Berti, A. (1990). Neglect as a neural representation deficit. Revue Neurologique 146, 626634.Google Scholar
Royce, G.J. & Laine, E.J. (1984). Efferent connections of the caudate nucleus, including cortical projections of the striatum and other basal ganglia: An autoradiographic and horseradish peroxidase investigation in the cat. Journal of Comparative Neurology 226, 2849.Google Scholar
Sanides, F. & Hoffmann, J. (1969). Cyto- and myelo-architecture of the visual cortex of the cat and of the surrounding integration cortices. Journal fur Hirnforschung 11, 79104.Google Scholar
Segal, R.L. & Beckstead, R.M. (1984). The lateral suprasylvian corticotectal projection in cats. Journal of Comparative Neurology 225, 259275.CrossRefGoogle ScholarPubMed
Sherman, S.M. (1977). The effect of superior colliculus lesions upon the visual fields of cats with cortical ablations. Journal of Comparative Neurology 172, 211230.Google Scholar
Spear, P.D., Miller, S. & Ohman, L. (1983). Effects of lateral suprasylvian cortex lesions on visual localization, discrimination and attention in cats. Behavioural Brain Research 10, 339359.CrossRefGoogle ScholarPubMed
Sprague, J.M. (1966). Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153, 15441547.CrossRefGoogle ScholarPubMed
Sprague, J.M. (1972). The superior colliculus and pretectum in visual behavior. Investigative Ophthalmology 11, 473482.Google Scholar
Sprague, J.M. & Meikle, T.H. Jr., (1965). The role of the superior colliculus in visually guided behavior. Experimental Neurology 11, 115146.CrossRefGoogle ScholarPubMed
Sprague, J.M., Berlucchi, G. & Di Berardino, A. (1970). The superior colliclus and pretectum in visually guided behavior and visual discrimination in the cat. Brain, Behavior, and Evolution 3, 285294.Google Scholar
Stein, B.E. & Meredith, M.A. (1991). Functional organization of the superior colliculus. In The Neural Bases of Visual Function, ed. Leventhal, A.G., pp. 85110. Hampshire, UK: Macmillan.Google Scholar
Sun, J.S., Lomber, S.G. & Payne, B.R. (1994). Expansion of suprasylvian cortex projection into the superficial layers of the superior colliculus following damage of areas 17 and 18 in developing cats. Visual Neuroscience 11, 1322.CrossRefGoogle ScholarPubMed
Symonds, L.L. & Rosenquist, A.C. (1984). Laminar origins of visual corticocortical connections in the cat. Journal of Comparative Neurology 229, 3947.Google Scholar
Tortelly, A., Reinoso-Suárez, F. & Llamas, A. (1980). Projections from non-visual cortical areas to the superior colliculus demonstrated by retrograde transport of HRP in the cat. Brain Research 188, 543549.Google Scholar
Updyke, B.V. (1993). Organization of visual corticostriatal projections in the cat, with observations on visual projections to claustrum and amygdala. Journal of Comparative Neurology 327, 159193.Google Scholar
Vallar, G. (1993). The anatomical basis of spatial neglect in humans. In Unilateral Neglect: Clinical and Experimental Studies, ed. Robertson, I.H. & Marshall, J.C., pp. 2762. Hillsdale, New Jersey: Lawrence Erlbaum.Google Scholar
Wallace, S.F., Rosenquist, A.C. & Sprague, J.M. (1989). Recovery from cortical blindness mediated by destruction of nontectotectal fibers in the commissure of the superior colliculus in the cat. Journal of Comparative Neurology 284, 429450.Google Scholar
Wallace, S.F., Rosenquist, A.C. & Sprague, J.M. (1990). Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behavior in the hemianopic cat. Journal of Comparative Neurology 296, 222252.CrossRefGoogle ScholarPubMed
Watson, R.T., Valenstein, E., Day, A. & Heilman, K.M. (1994). Posterior neocortical systems subserving awareness and neglect. Archives of Neurology 51, 10141021.Google Scholar