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Influence of the superior colliculus on responses of lateral geniculate neurons in the cat

Published online by Cambridge University Press:  02 June 2009

Jin-Tang Xue ,
Charlene B.Y. Kim ,
Rodney J. Moore  and
Peter D. Spear
Jin-Tang Xue
Affiliation:
Department of Psychology and Center for Neuroscience, University of Wisconsin, Madison
Charlene B.Y. Kim
Affiliation:
Department of Psychology and Center for Neuroscience, University of Wisconsin, Madison
Rodney J. Moore
Affiliation:
Department of Psychology and Center for Neuroscience, University of Wisconsin, Madison
Peter D. Spear
Affiliation:
Department of Psychology and Center for Neuroscience, University of Wisconsin, Madison
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Abstract

The superior colliculus (SC) projects to all layers of the cat's lateral geniculate nucleus (LGN) and thus is in a position to influence information transmission through the LGN. We investigated the function of the tecto-geniculate pathway by studying the responses of cat LGN neurons before, during, and after inactivating the SC with microinjections of lidocaine. The LGN cells were stimulated with drifting sine-wave gratings that varied in spatial frequency and contrast. Among 71 LGN neurons that were studied, 53 showed a statistically significant change in response during SC inactivation. Control experiments with mock injections indicated that some changes could be attributed to slow waxing and waning of responsiveness over time. However, this could not account for all of the effects of SC inactivation that were observed. Forty cells showed changes that were attributed to the removal of tecto-geniculate influences. About equal numbers of cells showed increases (22 cells) and decreases (18 cells) in some aspect of their response to visual stimuli during SC inactivation. The proportion of cells that showed tecto-geniculate influences was somewhat higher in the C layers (68% of the cells) than in the A layers (44% of the cells). In addition, among cells that showed a significant change in maximal response to visual stimulation, the change was larger for cells in the C layers (64% average change) than in the A layers (26% average change) and it was larger for W cells (61% average change) than for X and Y cells (29% average change). Nearly all of the X cells that showed changes had an increase in response, and nearly all of the Y cells had a decrease in response. In addition, across all cell classes, 80% of the cells with receptive fields < 15 deg from the area centralis had an increase in response, and 80% of the cells with receptive fields > 15 deg from the area centralis had a decrease in response. None of the LGN cells had significant changes in spatial resolution, and only three cells had changes in optimal spatial frequency. Ten cells had a change in contrast threshold, 25 cells had a change in contrast gain, and 29 cells had a change in the maximal response to a high-contrast stimulus. Thus, our results suggest that the tecto-geniculate pathway has little or no effect on spatial processing by LGN neurons. Rather, the major influence is on maximal response levels and the relationship between response and stimulus contrast. Several hypotheses about the role of the tecto-geniculate pathway in visual behavior are considered.

Keywords

Dorsal lateral geniculateSuperior colliculusX cellY cellW cellTecto-geniculate influenceSpatial frequencyContrast
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 6 , November 1994 , pp. 1059 - 1076
Copyright
Copyright © Cambridge University Press 1994

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References

Bruce, L.L. & Stein, B.E. (1988). Transient projections from the lateral geniculate to the posteromedial lateral suprasylvian visual cortex in kittens. Journal of Comparative Neurology 278, 287–302.CrossRefGoogle Scholar
Butter, C.M., Weinstein, C., Bender, D.B. & Gross, C.G. (1978). Localization and detection of visual stimuli following superior colliculus lesion in rhesus monkeys. Brain Research 156, 33–49.Google Scholar
Capuano, U. & McIlwain, J. (1981). Reciprocity of receptive field images and point images in the superior colliculus of the cat. Journal of Comparative Neurology 196, 13–24.Google Scholar
Cleland, B.G., Levick, W.R., Morstyn, R. & Wagner, H.G. (1976). Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. Journal of Physiology (London) 255, 299–320.Google Scholar
Dean, P., Redgrave, P. & Westby, G.W.M. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends in Neurosciences 12, 137–147.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual processing in monkey. In Handbook of Neuropsychology, Vol. II, ed. Boller, F. & Grafman, J., pp. 267–299, Amsterdam: Elsevier Science Publishers.Google Scholar
Dreher, B. (1986). Thalamocortical and corticocortical interconnections in the cat visual system: Relation to the mechanisms of information processing. In Visual Neuroscience, ed. Pettigrew, J.D., Sanderson, K.J. & Levick, W.R., pp. 290–314. Cambridge: Cambridge University Press.Google Scholar
Feldon, S., Feldon, P. & Kruger, L. (1970). Topography of the retinal projection upon the superior colliculus of the cat. Vision Research 10, 135–143.Google Scholar
Goldberg, M.E. & Wurtz, R.H. (1972). Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. Journal of Neurophysiology 35, 560–574.Google Scholar
Graham, J. (1977). An autoradiographic study of the efferent connections of the superior colliculus in the cat. Journal of Comparative Neurology 173, 629–654.Google Scholar
Guitton, D. (1992). Control of eye-hand coordination during orienting gaze shifts. Trends in Neurosciences 15, 174–179.Google Scholar
Harting, J.K., Huerta, M.F., Hashikawa, T. & Van Lieshout, D.P. (1991). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 304, 275–306.Google Scholar
Huerta, M.F. & Harting, J.K. (1984 a). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–773. New York: Plenum Press.Google Scholar
Huerta, M.F. & Harting, J.K. (1984 b). Connectional organization of the superior colliculus. Trends in Neurosciences 7, 286–289.Google Scholar
Jeannerod, M. & Putkonen, P.T.S. (1971). Lateral geniculate unit activity and eye movements: Saccade-locked changes in dark and in light. Experimental Brain Research 13, 533–546.Google Scholar
Kul'gavin, L.E. & Kolesnikov, V.G. (1991). Effect of the superior colliculus on function of the contralateral lateral geniculate body in cats. Bulletin of Experimental Biology and Medicine 111, 275–278.Google Scholar
Kurtz, D. & Butter, C.M. (1980). Impairments in visual discrimination performance and gaze shifts in monkeys with superior colliculus lesions. Brain Research 196, 109–124.Google Scholar
Lal, R. & Friedlander, M. J. (1990). Effect of passive eye movement on retinogeniculate transmission in the cat. Journal of Neurophysiology 63, 523–538.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.Google Scholar
Lo, F.-S. & Xie, G.-Y. (1987). Control of recurrent inhibition of the lateral geniculate nucleus by afferents from the superior colliculus of the rabbit: A possible mechanism of saccadic suppression. Experimental Brain Research 68, 421–427.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Schiller, P.H. (1979). A method for reversible inactivation of small regions of brain tissue. Journal of Neuroscience Methods 1, 143–151.Google Scholar
Maunsell, J.H., Nealey, T.A. & DePriest, D. (1990). Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. Journal of Neuroscience 10, 3323–3334.Google Scholar
McIlwain, J.T. (1975). Receptive fields and their images in the superior colliculus of the cat. Journal of Neurophysiology 38, 219–230.Google Scholar
McIlwain, J.T. (1991). Distributed spatial coding in the superior colliculus—A review. Visual Neuroscience 6, 3–13.Google Scholar
Merigan, W.H. (1991). P and M pathway specialization in the macaque. In Pigments to Perception, ed. Valberg, A. & Lee, B.B., pp. 117–125. New York: Plenum Press.Google Scholar
Molotchnikoff, S. & Lachapelle, P. (1980). Evidence of collicular input to the dorsal lateral geniculate nucleus in rabbits–electrophysiology. Experimental Brain Research 40, 221–228.Google Scholar
Molotchnikoff, S. & Lachapelle, P. (1983). Local excitability in the superior colliculus influences evoked responses of lateral geniculate cells in rabbits. Brain Research Bulletin 11, 533–545.Google Scholar
Molotchnikoff, S., Casanova, C., Lachapelle, P. & Delaunais, D. (1983). The superior colliculus simultaneously modifies the responses of the lateral geniculate cells and of the oculomotor nuclei. Brain Research Bulletin 10, 719–722.Google Scholar
Molotchnikoff, S., Delaunais, D., & Casanova, C. (1986 a). Modulations of the lateral geniculate nucleus cell responses by a second discrete conditioning stimulus: Implications of the superior colliculus in rabbits. Experimental Brain Research 62, 321–328.Google Scholar
Molotchnikoff, S., Delaunais, D., Casanova, C. & Lachapelle, P. (1986 b). Influence of a local inactivation in the superior colliculus on lateral geniculate responses in rabbits. Brain Research 375, 66–72.Google Scholar
Molotchnikoff, S. & Cerat, A. (1992). Responses from outside classical receptive fields of dorsal lateral geniculate cells in rabbits. Experimental Brain Research 92, 94–104.Google Scholar
Noda, H. (1975 a). Depression in the excitability of relay cells of lateral geniculate nucleus following saccadic eye movements in the cat. Journal of Physiology (London) 249, 87–102.Google Scholar
Noda, H. (1975 b). Discharges of relay cells in lateral geniculate nucleus of the cat during spontaneous eye movements in light and darkness. Journal of Physiology (London) 250, 579–596.CrossRefGoogle ScholarPubMed
Peck, C.K. (1984). Saccade-related neurons in cat superior colliculus: Pandirectional movement cells with postsaccadic responses. Journal of Neurophysiology 52, 1154–1168.Google Scholar
Peck, C.K. (1989). Visual responses of neurones in cat superior colliculus in relation to fixation of targets. Journal of Physiology (London) 414, 301–315.Google 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
Richmond, B.J. & Wurtz, R.H. (1980). Vision during saccadic eye movements. II. A corollary discharge to monkey superior colliculus. Journal of Neurophysiology 43, 1156–1167.Google Scholar
Robinson, D.A. & Wurtz, R.H. (1976). Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. Journal of Neurophysiology 39, 852–870.Google Scholar
Robinson, D.L. & McClurkin, J.W. (1989). The visual superior colliculus and pulvinar. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.E., pp. 337–360. Amsterdam: Elsevier Science Publishers.Google Scholar
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and transspecies comparisons. Brain, Behavior, and Evolution 23, 121–164.Google ScholarPubMed
Rosenquist, A.C. (1985). Connections of visual cortical areas in the cat. In Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 81–117. New York: Plenum Press.Google Scholar
Schiller, P.H., Malpeli, J.G. & Schein, S.J. (1979). Composition of geniculostriate input to superior colliculus of the rhesus monkey. Journal of Neurophysiology 42, 1124–1133.Google Scholar
Sherman, S.M. (1985). Functional organization of the W-, X-, and Y-cell pathways in the cat: A review and hypothesis. In Progress in Psychobiology and Physiological Psychology, ed. Sprague, J.M. & Epstein, A.N., pp. 233–314. Orlando, Florida: Academic Press.Google Scholar
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: Role of primate superior colliculus. Physiological Reviews 66, 118–171.Google Scholar
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.E., pp. 213–255. Amsterdam: Elsevier Science Publishers.Google Scholar
Spear, P.D. (1985). Neural mechanisms of compensation following neonatal cortex damage. In Synoptic Plasticity and Remodeling, ed. Cotman, C.W., pp. 111–167. New York: Guildford Press.Google Scholar
Spear, P.O., McCall, M.A. & Tumosa, N. (1989). W- and Y-cells in the C layers of the cat's lateral geniculate nucleus: Normal properties and effects of monocular deprivation. Journal of Neurophysiology 61, 58–73.Google Scholar
Stanford, L.R., Friedlander, M.J. & Sherman, S.M. (1983). Morphological and physiological properties of geniculate W-cells of the cat: A comparison with X- and Y-cells. Journal of Neurophysiology 50, 582–608.Google Scholar
Stein, B.E., McHaffie, J.G., Harting, J.K., Huerta, M.F. & Hashikawa, T. (1985). Transient tectogeniculate projections in neonatal kittens: An autoradiographic study. Journal of Comparative Neurology 239, 402–412.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. New York: Plenum Press.Google Scholar
Sur, M. & Sherman, S.M. (1982). Linear and nonlinear W-cells in C-laminae of the cat's lateral geniculate nucleus. Journal of Neurophysiology 47, 869–884.CrossRefGoogle ScholarPubMed
Torrealba, F., Partlow, G.D. & Guillery, R.W. (1981). Organization of the projection from the superior colliculus to the dorsal lateral geniculate nucleus of the cat. Neuroscience 6, 1341–1360.CrossRefGoogle 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, 280–298.Google Scholar
Wilson, P.O., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat's lateral geniculate nucleus: A comparison of W-cells with X-and Y-cells. Journal of Neurophysiology 39, 1193–1209.Google Scholar
Wurtz, R. (1969). Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. Journal of Neurophysiology 32, 975–986.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Mohler, C.W. (1976). Organization of monkey superior colliculus: Enhanced visual response of superficial layer cells. Journal of Neurophysiology 39, 745–765.Google Scholar
Wurtz, R.H. & Aibano, J.E. (1980). Visual-motor function of the primate superior colliculus. Annual Review of Neuroscience 3, 189–226.Google Scholar
Wurtz, R.H., Goldberg, M.E. & Robinson, D.L. (1980). Behavioral modulation of visual response in the monkey: Stimulus selection for attention and movement. In Progress in Psychobiology and Physiological Psychology, Vol. 9, pp. 43–83. New York: Academic Press.Google Scholar