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Complex motion selectivity in PMLS cortex following early lesions of primary visual cortex in the cat

Published online by Cambridge University Press:  12 April 2007

B.G. OUELLETTE
Affiliation:
École d'Optométrie, Université de Montréal, Montréal, Quebec, Canada Département de Psychologie, Université de Montréal, Montréal, Quebec, Canada
K. MINVILLE
Affiliation:
École d'Optométrie, Université de Montréal, Montréal, Quebec, Canada
D. BOIRE
Affiliation:
École d'Optométrie, Université de Montréal, Montréal, Quebec, Canada
M. PTITO
Affiliation:
École d'Optométrie, Université de Montréal, Montréal, Quebec, Canada
C. CASANOVA
Affiliation:
École d'Optométrie, Université de Montréal, Montréal, Quebec, Canada

Abstract

In the cat, the analysis of visual motion cues has generally been attributed to the posteromedial lateral suprasylvian cortex (PMLS) (Toyama et al., 1985; Rauschecker et al., 1987; Rauschecker, 1988; Kim et al., 1997). The responses of neurons in this area are not critically dependent on inputs from the primary visual cortex (VC), as lesions of VC leave neuronal response properties in PMLS relatively unchanged (Spear & Baumann, 1979; Spear, 1988; Guido et al., 1990b). However, previous studies have used a limited range of visual stimuli. In this study, we assessed whether neurons in PMLS cortex remained direction-selective to complex motion stimuli following a lesion of VC, particularly to complex random dot kinematograms (RDKs). Unilateral aspiration of VC was performed on post-natal days 7–9. Single unit extracellular recordings were performed one year later in the ipsilateral PMLS cortex. As in previous studies, a reduction in the percentage of direction selective neurons was observed with drifting sinewave gratings. We report a previously unobserved phenomenon with sinewave gratings, in which there is a greater modulation of firing rate at the temporal frequency of the stimulus in animals with a lesion of VC, suggesting an increased segregation of ON and OFF sub-regions. A significant portion of neurons in PMLS cortex were direction selective to simple (16/18) and complex (11/16) RDKs. However, the strength of direction selectivity to both stimuli was reduced as compared to normals. The data suggest that complex motion processing is still present, albeit reduced, in PMLS cortex despite the removal of VC input. The complex RDK motion selectivity is consistent with both geniculo-cortical and extra-geniculate thalamo-cortical pathways in residual direction encoding.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284299.CrossRefGoogle Scholar
Azzopardi, P., Fallah, M., Gross, C.G. & Rodman, H.R. (2003). Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions. Neuropsychologia 41, 17381756.CrossRefGoogle Scholar
Bender, D.B. (1983). Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Research 279, 258261.CrossRefGoogle Scholar
Benevento, L.A. & Standage, G.P. (1982). Demonstration of lack of dorsal lateral geniculate nucleus input to extrastriate areas MT and visual 2 in the macaque monkey. Brain Research 252, 161166.CrossRefGoogle Scholar
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455474.CrossRefGoogle Scholar
Boire, D., Matteau, I., Casanova, C. & Ptito, M. (2004). Retinal projections to the lateral posterior-pulvinar complex in intact and early visual cortex lesioned cats. Experimental Brain Research 159, 185196.CrossRefGoogle Scholar
Collins, C.E., Lyon, D.C. & Kaas, J.H. (2003). Responses of neurons in the middle temporal visual area after long-standing lesions of the primary visual cortex in adult new world monkeys. Journal of Neuroscience 23, 22512264.Google Scholar
Cornwell, P. & Payne, B. (1989). Visual discrimination by cats given lesions of visual cortex in one or two stages in infancy or in one stage in adulthood. Behavioral Neuroscience 103, 11911199.CrossRefGoogle Scholar
Desautels, A. & Casanova, C. (2001). Response properties in the pulvinar complex after neonatal ablation of the primary visual cortex. Progress in Brain Research 134, 8395.CrossRefGoogle Scholar
Dinse, H.R. & Kruger, K. (1994). The timing of processing along the visual pathway in the cat. Neuroreport 5, 893897.CrossRefGoogle Scholar
Dumbrava, D., Faubert, J. & Casanova, C. (2001). Global motion integration in the cat's lateral posterior-pulvinar complex. European Journal of Neuroscience 13, 22182226.CrossRefGoogle Scholar
Fries, W. (1981). The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey. Proceedings of the Royal Society of London. Series B 213, 7386.CrossRefGoogle Scholar
Galuske, R.A., Schmidt, K.E., Goebel, R., Lomber, S.G. & Payne, B.R. (2002). The role of feedback in shaping neural representations in cat visual cortex. Proceedings of the National Academy of Science U S A 99, 1708317088.CrossRefGoogle Scholar
Girard, P., Salin, P.A. & Bullier, J. (1992). Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. Journal of Neurophysiology 67, 14371446.Google Scholar
Grant, S. & Hilgetag, C.C. (2005). Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex. European Journal of Neuroscience 22, 681696.CrossRefGoogle Scholar
Guido, W., Spear, P.D. & Tong, L. (1990a). Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Experimental Brain Research 83, 219224.Google Scholar
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, 455466.Google Scholar
Guido, W., Tong, L. & Spear, P.D. (1990b). Afferent bases of spatial- and temporal-frequency processing by neurons in the cat's posteromedial lateral suprasylvian cortex: Effects of removing areas 17, 18, and 19. Journal of Neurophysiology 64, 16361651.Google Scholar
Hendrickson, A. & Dineen, J.T. (1982). Hypertrophy of neurons in dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neuroscience Letters 30, 217222.CrossRefGoogle Scholar
Huppé-Gourgue, F., Bickford, M.E., Boire, D., Ptito, M. & Casanova, C. (2006). Distribution, morphology and synaptic targets of corticothalamic terminals in the cat lateral posterior-pulvinar complex that originates from the posteromedial lateral suprasylvian cortex. Journal of Comparative Neurology 45, 137145.Google Scholar
Huxlin, K.R. & Pasternak, T. (2001). Long-term neurochemical changes after visual cortical lesions in the adult cat. Journal of Comparative Neurology 429, 221241.3.0.CO;2-6>CrossRefGoogle Scholar
Illig, K.R., Danilov, Y.P., Ahmad, A., Kim, C.B. & Spear, P.D. (2000). Functional plasticity in extrastriate visual cortex following neonatal visual cortex damage and monocular enucleation. Brain Research 882, 241250.CrossRefGoogle Scholar
Kaas, J.H. & Krubitzer, L.A. (1992). Area 17 lesions deactivate area MT in owl monkeys. Visual Neuroscience 9, 399407.CrossRefGoogle Scholar
Kalil, R.E., Tong, L.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, 512525.CrossRefGoogle Scholar
Katsuyama, N., Tsumoto, T., Sato, H., Fukuda, M. & Hata, Y. (1996). Lateral suprasylvian visual cortex is activated earlier than or synchronously with primary visual cortex in the cat. Neuroscience Research 24, 431435.CrossRefGoogle Scholar
Kim, J.N., Mulligan, K. & Sherk, H. (1997). Simulated optic flow and extrastriate cortex. I. Optic flow versus texture. Journal Neurophysiology 77, 554561.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 projection to the pulvinar in cats. Journal of Comparative Neurology 197, 639659.CrossRefGoogle Scholar
Long, K.D., Lomber, S.G. & Payne, B.R. (1996). Increased oxidative metabolism in middle suprasylvian cortex following removal of areas 17 and 18 from newborn cats. Experimental Brain Research 110, 335346.Google Scholar
Majaj, N., Carandini, M., Smith, M.A. & Movshon, J.A. (1999). Local integration of features for the computation of pattern direction by neurons in macaque area MT. Society for Neuroscience Abstracts 25, 674.Google Scholar
Maunsell, J.H., Nealey, T.A. & DePriest, D.D. (1990). Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. Journal of Neuroscience 10, 33233334.Google Scholar
Moore, T., Rodman, H.R. & Gross, C.G. (2001). Direction of motion discrimination after early lesions of striate cortex (V1) of the macaque monkey. Proceedings of the National Academy of Science U S A 98, 325330.CrossRefGoogle Scholar
Moore, T., Rodman, H.R., Repp, A.B., Gross, C.G. & Mezrich, R.S. (1996). Greater residual vision in monkeys after striate cortex damage in infancy. Journal of Neurophysiology 76, 39283933.Google Scholar
Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. (1986). The analysis of moving visual patterns. In Pattern recognition mechanisms, ed. Chagas, C., Gattas, R. & Gross, C., pp. 148164. New York: Springer Verlag.
Murphy, E.H. & Kalil, R. (1979). Functional organization of lateral geniculate cells following removal of visual cortex in the newborn kitten. Science 206, 713716.CrossRefGoogle Scholar
Murphy, E.H., Mize, R.R. & Schechter, P.B. (1975). Visual discrimination following infant and adult ablation of cortical areas 17, 18, and 19 in the cat. Experimental Neurology 49, 386405.CrossRefGoogle Scholar
Naito, J. & Kawamura, K. (1982). Thalamocortical neurons projecting to the areas surrounding the anterior and middle suprasylvian sulci in the cat. A horseradish peroxidase study. Experimental Brain Research 45, 5970.Google Scholar
Nowlan, S.J. & Sejnowski, T.J. (1995). A selection model for motion processing in area MT of primates. Journal of Neuroscience 15, 11951214.Google Scholar
Ouellette, B.G. & Casanova, C. (2006). Overlapping visual response latency distributions in visual cortices and LP-pulvinar complex of the cat. Experimental Brain Research 175, 332341.CrossRefGoogle Scholar
Ouellette, B.G., Minville, K., Faubert, J. & Casanova, C. (2004). Simple and complex visual motion response properties in the anterior medial bank of the lateral suprasylvian cortex. Neuroscience 123, 231245.CrossRefGoogle Scholar
Palmer, L.A., Rosenquist, A.C. & Tusa, R.J. (1978). The retinotopic organization of lateral suprasylvian visual areas in the cat. Journal of Comparative Neurology 177, 237256.CrossRefGoogle Scholar
Pasternak, T., Tompkins, J. & Olson, C.R. (1995). The role of striate cortex in visual function of the cat. Journal of Neuroscience 15, 19401950.Google Scholar
Payne, B.R. (2004). Neuroplasticity in the cat's visual system: test of the role of the expanded retino-geniculo-parietal pathway in behavioral sparing following early lesions of visual cortex. Experimental Brain Research 155, 6980.CrossRefGoogle Scholar
Payne, B.R., Foley, H.A. & Lomber, S.G. (1993). Visual cortex damage-induced growth of retinal axons into the lateral posterior nucleus of the cat. Visual Neuroscience 10, 747752.CrossRefGoogle Scholar
Payne, B.R. & Lomber, S.G. (1998). Neuroplasticity in the cat's visual system. Experimental Brain Research 12, 334349.CrossRefGoogle Scholar
Rauschecker, J.P. (1988). Visual function of the cat's LP/LS subsystem in global motion processing. Progress in Brain Research 75, 95108.CrossRefGoogle Scholar
Rauschecker, J.P., von Grunau, M.W. & Poulin, C. (1987). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. Journal of Neuroscience 7, 943958.Google Scholar
Reichardt, W. (1961). Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory communication, ed. Rosemblich, W., pp. 303317. MIT Press, New York.
Rodman, H.R., Gross, C.G. & Albright, T.D. (1989). Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. Journal of Neuroscience 9, 20332050.Google Scholar
Rodman, H.R., Gross, C.G. & Albright, T.D. (1990). Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. Journal of Neuroscience 10, 11541164.Google Scholar
Rosa, M.G., Tweedale, R. & Elston, G.N. (2000). Visual responses of neurons in the middle temporal area of new world monkeys after lesions of striate cortex. Journal of Neuroscience 20, 55525563.Google Scholar
Rudolph, K.K. & Pasternak, T. (1996). Lesions in cat lateral suprasylvian cortex affect the perception of complex motion. Cerebral Cortex 6, 814822.CrossRefGoogle 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, 101108.CrossRefGoogle Scholar
Shen, W., Liang, Z., Chen, X. & Shou, T. (2006). Posteromedial lateral suprasylvian motion area modulates direction but not orientation preference in area 17 of cats. Neuroscience 142, 905916.CrossRefGoogle Scholar
Skottun, B.C., Grosof, D.H. & De Valois, R.L. (1991). On the responses of simple and complex cells to random dot patterns. Vision Research 31, 4346.CrossRefGoogle Scholar
Smith, D.C. & Spear, P.D. (1979). Effects of superior colliculus removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 42, 5775.Google Scholar
Smith, M.A., Majaj, N.J. & Movshon, J.A. (2005). Dynamics of motion signaling by neurons in macaque area MT. Nature Neuroscience 8, 220228.CrossRefGoogle Scholar
Sorenson, K.M. & Rodman, H.R. (1999). A transient geniculo-extrastriate pathway in macaques? Implications for “blindsight.” Neuroreport 10, 32953299.CrossRefGoogle Scholar
Spear, P.D. (1988). Influence of areas 17, 18, and 19 on receptive-field properties of neurons in the cat's posteromedial lateral suprasylvian visual cortex. Progressive Brain Research 75, 197210.CrossRefGoogle Scholar
Spear, P.D. (1995). Plasticity following neonatal visual cortex damage in cats. Canadian Journal of Physiology and Pharmacology 73, 13891397.CrossRefGoogle Scholar
Spear, P.D. & Baumann, T.P. (1979). Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 42, 3156.Google Scholar
Stepniewska, I., Qi, H.X. & Kaas, J.H. (1999). Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? European Journal of Neuroscience 11, 469480.Google Scholar
Symonds, L.L. & Rosenquist, A.C. (1984). Laminar origins of visual corticocortical connections in the cat. Journal of Comparative Neurology 229, 3947.CrossRefGoogle Scholar
Thiele, A., Distler, C., Korbmacher, H. & Hoffmann, K.P. (2004). Contribution of inhibitory mechanisms to direction selectivity and response normalization in macaque middle temporal area. Proceedings of the National Academy of Science USA 101, 98109815.CrossRefGoogle Scholar
Tong, L., Kalil, R.E. & Spear, P.D. (1982). Thalamic projections to visual areas of the middle suprasylvian sulcus in the cat. Journal of Comparative Neurology 212, 103117.CrossRefGoogle Scholar
Tong, L., Kalil, R.E. & Spear, P.D. (1984). Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats. Journal of Neurophysiology 52, 941960.Google Scholar
Tong, L., Spear, P.D. & Kalil, R.E. (1987). Effects of corpus callosum section on functional compensation in the posteromedial lateral suprasylvian visual area after early visual cortex damage in cats. Journal of Comparative Neurology 256, 128136.CrossRefGoogle Scholar
Tong, L.L., Kalil, R.E. & Spear, P.D. (1991). Development of the projections from the dorsal lateral geniculate nucleus to the lateral suprasylvian visual area of cortex in the cat. Journal of Comparative Neurology 314, 526533.CrossRefGoogle Scholar
Toyama, K., Komatsu, Y., Kasai, H., Fujii, K. & Umetani, K. (1985). Responsiveness of Clare-Bishop neurons to visual cues associated with motion of a visual stimulus in three-dimensional space. Vision Research 25, 407414.CrossRefGoogle Scholar
Tucker, T.J., Kling, A. & Scharlock, D.P. (1968). Sparing of photic frequency and brightness discriminations after striatectomy in neonatal cats. Journal of Neurophysiology 31, 818832.Google Scholar
Tumosa, N., McCall, M.A., Guido, W. & Spear, P.D. (1989). Responses of lateral geniculate neurons that survive long-term visual cortex damage in kittens and adult cats. Journal of Neuroscience 9, 280298.Google Scholar
Updyke, B.V. (1981). Projections from visual areas of the middle suprasylvian sulcus onto the lateral posterior complex and adjacent thalamic nuclei in cat. Journal of Comparative Neurology 201, 477506.CrossRefGoogle Scholar
Villeneuve, M.Y., Ptito, M. & Casanova, C. (2006). Global motion integration in the postero-medial part of the lateral suprasylvian cortex in the cat. Experimental Brain Research 172, 485497.CrossRefGoogle Scholar
von Grunau, M. & Frost, B.J. (1983). Double-opponent-process mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area. Experimental Brain Research 49, 8492.CrossRefGoogle Scholar
Wetzel, A.B., Thompson, V.E., Horel, J.A. & Meyer, P.M. (1965). Some consequences of perinatal lesions of the visual cortex in the cat. Psychonomic Science 3, 381382.CrossRefGoogle Scholar