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Direction selectivity and physiological compensation in the superior colliculus following removal of areas 17 and 18

Published online by Cambridge University Press:  02 June 2009

Janine D. Mendola  and
Bertram R. Payne
Janine D. Mendola
Affiliation:
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
Bertram R. Payne
Affiliation:
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
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Abstract

Previous studies indicate that cortical areas 17 and 18 play a prominent role in generating the direction selectivities of neurons in the superior colliculus of the cat. This hypothesis was tested by quantifying the activities of neurons in the superficial collicular layers in intact cats and cats which incurred ablation of areas 17 and 18 and part of area 19. In addition, since behavioral and anatomical studies suggest a functional adjustment in the superior colliculus following removal of inputs from areas 17, 18, and 19 in the neonatal cat, we included a group of neonatally lesioned cats. Computation of an index of directionality indicated that the majority of neurons in intact cats preferred movement in one direction, thus confirming reports of others. Following ablation of areas 17 and 18 and part of area 19 in both groups of lesioned cats, only modest changes in the population indices were detected when poorly responsive neurons were eliminated from the analyses. Based upon levels of visually evoked neuronal activity, our data suggest a physiological compensation by neurons in stratum griseum superficiale following removal of areas 17, 18, and 19 inputs. In the intact and neonatally operated groups, activity in stratum griseum superficiale is high, whereas in the adult lesioned group activity is low. In stratum opticum, neuronal activity was similar in all three groups of cats. These results show that neurons in stratum griseum superficiale undergo a physiological compensation following removal of immature areas 17 and 18.

Keywords

Brain damageSparing of functionNeonateVisual cortexReceptive fieldsBlindness
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 6 , November 1993 , pp. 1019 - 1026
Copyright
Copyright © Cambridge University Press 1993

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References

Beckstead, A. & Frankfurter, R.M. (1983). A direct projection from the retina to the intermediate gray layer of the superior colliculus demonstrated by anterograde transport of horseradish peroxidase in monkey, cat, and rat. Experimental Brain Research 52, 261–268.Google Scholar
Behan, M. (1982). Identification and distribution of retinocollicular terminals in the cat: An electron-microscopic autoradiographic study. Journal of Comparative Neurology 199, 1–15.Google Scholar
Behan, M. (1984). An EM-autoradiographic analysis of the projection from cortical areas 17, 18, and 19 to the superior colliculus of the cat. Journal of Comparative Neurology 225, 591–604.Google Scholar
Berlucchi, G., Sprague, J.M., Levy, J. & DiBerardino, A.C. (1972). Pretectum and superior colliculus and visually guided behavior and in flux and form discrimination in the cat. Journal of Comparative and Physiological Psychology Monographs 78, 123–172.CrossRefGoogle ScholarPubMed
Berman, N. & Cynader, M. (1972). Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats. Journal of Physiology (London) 224, 363–389.CrossRefGoogle ScholarPubMed
Berman, N. & Cynader, M. (1975). Receptive fields in cat superior colliculus after visual cortex lesions. Journal of Physiology (London) 245, 261–270.Google Scholar
Berman, N. & Cynader, M. (1976). Early versus late visual cortex lesions: Effects on receptive fields in cat superior colliculus. Experimental Brain Research 25, 131–137.CrossRefGoogle ScholarPubMed
Berson, D.M. (1988). Retinal and cortical inputs to cat superior colliculus: Composition, convergence, and laminar specificity. Progress in Brain Research 75, 17–26.Google Scholar
Casagrande, V.A., Harting, J.K., Hall, W.C., Diamond, I.T. & Martin, G.F. (1972). Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science 177, 444–447.CrossRefGoogle ScholarPubMed
Flandrin, J.M. & Jeannerod, M. (1977). Lack of recovery in collicular neurons from the effects of early deprivation or neonatal cortical lesion in the kitten. Brain Research 120, 362–366.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1975). Anatomical organization of retinotectal afferents in the cat: An autoradiographic study. Brain Research 96, 1–23.Google Scholar
Guido, W., Spear, P.D. & Tong, L. (1990). Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Experimental Brain Research 83, 219–224.CrossRefGoogle ScholarPubMed
Guido, W., Spear, P.D. & Tong, L. (1992). How complete is physiological compensation in extrastriate cortex after visual cortex damage in kittens? Experimental Brain Research 91, 455–466.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, 527–542.CrossRefGoogle ScholarPubMed
Harting, J.K. & Guillery, R.W. (1976). Organization of retinocollicular pathways in the cat. Journal of Comparative Neurology 166, 133–144.CrossRefGoogle ScholarPubMed
Harting, J.K., Updyke, B.V. & Van Lieshout, D.P. (1992). Cortico-tectal projection in the cat: Anterograde transport studies of twenty-five cortical areas. Journal of Comparative Neurology 324, 379–414.CrossRefGoogle Scholar
Hoffmann, K.-P. (1973). Conduction velocity and pathways from retina to superior colliculus in the cat: A correlation with receptive-field properties. Journal of Neurophysiology 36, 409–424.Google Scholar
Hoffmann, K.-P. & Straschill, M. (1971). Influences of corticotectal and intertectal connections on visual responses in the cat's superior colliculus. Experimental Brain Research 12, 120–131.Google Scholar
Kalil, R., Tong, L. & Spear, P.D. (1991). Thalamic projections to the lateral suprasylvian visual area in cats with neonatal or adult visual cortex damage. Journal of Comparative Neurology 314, 512–525.CrossRefGoogle ScholarPubMed
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pre-tectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–338.CrossRefGoogle Scholar
Keating, M.J. & Withington-Wray, D.J. (1989). The role of visual experience in the development of the map of auditory space in the superior colliculus of the guinea pig. Journal of Physiology (London) 412, 45P.Google Scholar
King, A.J., Hutchings, M.E., Moore, D.R. & Blakemore, C. (1988). Developmental plasticity in the visual and auditory representation in the mammalian superior colliculus. Nature 332 73–76.Google Scholar
Labar, D.R., Berman, N.E. & Murphy, E.H. (1981). Short- and long-term effects of neonatal and adult visual cortex lesions on the retinal projections to the pulvinar in cats. Journal of Comparative Neurology 197, 639–659.CrossRefGoogle Scholar
Mendola, J., Siwek, D. & Payne, B.R. (1990). A quantitative reexamination of the influence of visual cortical areas 17 and 18 on the superior colliculus of the cat. Investigative Ophthalmology (Suppl.) 31, 399.Google Scholar
Mize, R.R. & Murphy, E.H. (1976). Alterations of receptive-field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats. Journal of Comparative Neurology 168, 393–424.CrossRefGoogle ScholarPubMed
Ogasawara, K., McHaffie, J.G. & Stein, B.E. (1984). Two visual corticotectal systems in the cat. Journal of Neurophysiology 52, 1226–1245.Google Scholar
Payne, B.R. (1990). The representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex. Visual Neuroscience 4, 445–474.Google Scholar
Payne, B.R. & Peters, A. (1989). Cytochrome oxidase patches and Meynert cells in monkey visual cortex. Neuroscience 28, 353–363.Google Scholar
Payne, B.R., Berman, N. & Murphy, E.H. (1981). A quantitative assessment of eye alignment in cats after corpus callosum transection. Experimental Brain Research 43, 371–376.Google ScholarPubMed
Payne, B.R., Foley, H. & Lomber, S.G. (1993). Visual cortex damage-induced growth of retinal axons into the lateral posterior nucleus of the cat. Visual Neuroscience 10, 747–752.CrossRefGoogle ScholarPubMed
Payne, B.R., Siwek, D.F. & Lomber, S.G. (1991). Complex transcal-losal interactions in visual cortex. Visual Neuroscience 3, 283–289.CrossRefGoogle Scholar
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google Scholar
Rauschecker, J.P. & Harris, L.R. (1983). Auditory compensation of the effects of visual deprivation in the cat's superior colliculus. Experimental Brain Research 50, 69–83.Google Scholar
Rizzolatti, G., Tradardi, V. & Camarda, R. (1970). Unit responses to visual stimuli in the cat's superior colliculus after removal of visual cortex. Brain Research 24, 336–339.Google Scholar
Rosenquist, A.C. (1985). Connections of visual cortical areas in the cat. In Cerebral Cortex, Volume 3, Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 81–117. New York: Plenum Press.Google Scholar
Rosenquist, A.C. & Palmer, L.A. (1971). Visual receptive-field properties of cells of the superior colliculus after cortical lesions in the cat. Experimental Neurology 33, 629–652.Google Scholar
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–118.Google Scholar
Sherk, H. (1979). A comparison of visual response properties in cat's parabigeminal nucleus and superior colliculus. Journal of Neurophysiology 42, 1640–1655.Google Scholar
Sherman, S.M. (1977). The effect of superior colliculus lesions upon the visual fields of cats with cortical ablations. Journal of Comparative Neurology 172, 211–230.CrossRefGoogle ScholarPubMed
Shupert, C, Cornwell, P. & Payne, B.R. (1993). Differential sparing of depth perception, orienting, and optokinetic nystagmus after neonatal versus adult lesions of cortical areas 17, 18, and 19 in the cat. Behavioral Neuroscience 107, 633–650.CrossRefGoogle Scholar
Spear, P.D., Kalil, R.E. & Tong, L. (1980). Functional compensation in lateral suprasylvian visual area following neonatal visual cortex removal in cats. Journal of Neurophysiology 43, 851–869.Google Scholar
Sprague, J.M. (1966). Interactions of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153, 1544–1547.CrossRefGoogle ScholarPubMed
Stein, B.E. & Arigbede, M.O. (1972). A parametric study of movement detection properties of neurons in the cat's superior colliculus. Brain Research 45, 437–454.CrossRefGoogle ScholarPubMed
Stein, B.E. & Magalhaes-Castro, B.E. (1975). Effects of neonatal cortical lesions upon the cat superior colliculus. Brain Research 83, 480–485.Google Scholar
Stein, B.E. & Meredith, M.A. (1991). Functional organization of the superior colliculus. In The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 85–110. Hampshire, U.K.: MacMillan.Google Scholar
Sterling, P. & Wickelgren, B.G. (1969). Visual receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 1–15.CrossRefGoogle ScholarPubMed
Sun, J.-S., Lomber, S.G. & Payne, B.R. (1994). Expansion of suprasylvian cortex projection in the superficial layers of the superior colliculus following damage of areas 17and 18 in developing cats. Visual Neuroscience 11 (in press).CrossRefGoogle Scholar
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.Google Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal of Comparative Neurology 185, 657–678.Google Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1981). Multiple cortical visual areas: Visual-field topography in the cat. In Cortical Sensory Organization: Multiple Visual Areas, ed. Woolsey, C.N., pp. 1–31. Clifton, New Jersey: Humana Press.Google Scholar
Updyke, B.V. (1977). Topographic organization of projections from cortical areas 17, 18, and 19 onto thalamus, pretectum, and superior colliculus in cat. Journal of Comparative Neurology 186, 81–123.Google Scholar
Wickelgren, B.G. & Sterling, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 16–23.Google Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.Google Scholar