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Conservation of receptive-field properties of superior colliculus cells after developmental rearrangements of retinal input

Published online by Cambridge University Press:  02 June 2009

S. L. Pallas  and
B. L. Finlay
S. L. Pallas
Affiliation:
Section of Neurobiology and Behavior, Cornell University, Ithaca
B. L. Finlay
Affiliation:
Department of Psychology, Cornell University, Ithaca
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Abstract

The formation of topographic maps requires not only that afferents synapse with the appropriate targets, but that the spatial relationships between the afferents be maintained. During development, in addition to the formation of the topographic map, the connectivity patterns responsible for the receptive-field properties of the target cells are being formed. The extent of interaction between these two processes is unknown. The present study addresses this question by manipulating afferent/target ratios during development, thus altering the topography of the map, and studying the effects of this alteration on the receptive-field properties of single target cells in the adult.

Partial unilateral lesions of the superior colliculus (SC) were made in neonatal hamsters. These lesions result in a compression of the retinotopic map onto the remaining collicular fragment. Single cells were recorded from the superficial gray layer of the SC in the adult in response to visual stimuli. Receptive-field properties observed in lesioned animals were compared to those in normal animals and in sham operates.

Receptive-field properties were largely unaffected by the change in the topographic map. There was no difference in the receptive-field size of single tectal cells of lesioned and unlesioned animals. Stimulus velocity and stimulus size tuning functions remained the same. This raises the possibility that, rather than the expected increase in convergence of retinal ganglion cells (RGC) onto single collicular cells, single SC cells receive input from ganglion cells representing the same amount of retinal area as in unlesioned animals. The excess ganglion cells created by the partial target removal would then project elsewhere and/or reduce their arbor within the SC. Regardless of the mechanism, it is clear from our results that circuitry in the retinotectal system of the hamster can compensate for conditions of increased afferent availability and thus maintain receptive-field properties.

Keywords

Superior colliculusReceptive fieldsAxonal arborizationAfferent/target convergenceNeuronal development
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 2 , February 1989 , pp. 121 - 135
Copyright
Copyright © Cambridge University Press 1989

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References

Bastian, J. (1982). Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Aperonotus albifrons. Journal of Comparative Physiology 147, 287–297.CrossRefGoogle Scholar
Chalupa, L.M. & Rhoades, R.W. (1977). Responses of visual, somatosensory, and auditory neurons in the golden hamster's superior colliculus. Journal of Physiology (London) 270, 595–626.CrossRefGoogle ScholarPubMed
Constantine-Paton, M. (1982). The retinotectal hookup: the process of neural mapping. In Developmental Order: Its Origin and Regulation, ed. subtelny, S. & Green, P.B., pp. 317–349. New York: Alan R. Liss.Google Scholar
Crain, B.J. & Hall, W.C. (1980 a). The organization of the lateral posterior nucleus of the golden hamster after neonatal superior colliculus lesions. Journal of Comparative Neurology 193, 383–401.CrossRefGoogle ScholarPubMed
Crain, B.J. & Hall, W.C. (1980 b). The organization of afferents to the lateral posterior nucleus in the golden hamster after different combinations of neonatal lesions. Journal of Comparative Neurology 193, 403–412.CrossRefGoogle Scholar
Emerson, V.P. (1980). Grating acuity of the golden hamster: effects of stimulus orientation and luminance. Experimental Brain Research 38, 43–52.CrossRefGoogle ScholarPubMed
Finlay, B.L. (1979). Experimental manipulations of the development of ordered projections in the mammalian brain. In Developmental Neurobiology of Vision, ed. Freeman, R.A., pp. 391–402. New York: Plenum Press.CrossRefGoogle Scholar
Finlay, B.L. & Berian, C.A. (1985). Visual and somatosensory processes. In The Hamster, ed. Siegel, H.I., pp. 409–433. New York: Plenum Press.CrossRefGoogle Scholar
Finlay, B.L., Schneps, S.E. & Schneider, G.E. (1979 a). Orderly compression of the retinotectal projection following partial tectal ablations in the newborn hamster. Nature 280, 153–154.CrossRefGoogle ScholarPubMed
Finlay, B.L., Wilson, K.G. & Schneider, G.E. (1979 b). Anomalous ipsilateral retinotectal projections in Syrian hamsters with early lesions: topography and functional capacity. Journal of Comparative Neurology 183, 721–740.CrossRefGoogle ScholarPubMed
Finlay, B.L., Schneps, S.E., Wilson, K.G. & Schneider, G.E. (1978). Topography of visual and somatosensory projections to the superior colliculus of the golden hamster. Brain Research 142, 223–235.CrossRefGoogle Scholar
Fraser, S.E. (1985). Cell interactions involved in neuronal patterning: an experimental and theoretical approach. In Molecular Bases of Neural Development, ed. Edelman, G.M., Gall, W.E. & Cowan, W.M., pp. 481–507. New York: Neuroscience Research Foundation.Google Scholar
Frost, D.O., So, K.-F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.CrossRefGoogle ScholarPubMed
Gaze, R.M. & Sharma, S.C. (1970). Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibers. Experimental Brain Research 10, 171–181.CrossRefGoogle Scholar
Hallett, P.E. (1987). The scale of the visual pathways of mouse and rat. Biological Cybernetics 57, 275–286.CrossRefGoogle ScholarPubMed
Hamos, J.E., Van Horn, S.C., Raczkowski, D. & Sherman, S.M. (1987). Synaptic circuits involving an individual retinogeniculate axon in the cat. Journal of Comparative Neurology 259, 165–192.CrossRefGoogle ScholarPubMed
Hartline, P.H. (1984). The optic tectum of reptiles: neurophysiological studies. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 601–618. New York: Plenum Press.CrossRefGoogle Scholar
Hebb, D.O. (1949). The Organization of Behavior. New York: John Wiley & Sons.Google Scholar
Hoffman, K.-P., Stone, J. & Sherman, S.M. (1972). Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 35, 518–531.CrossRefGoogle Scholar
Hubel, D.H., Wiesel, T.N. & Levay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society of London [Biology] 278, 377–409.Google ScholarPubMed
Jhaveri, S.R. & Schneider, G.E. (1974 a). Retinal projections in Syrian hamsters: normal topography and alterations after partial tectum lesions at birth. Anatomical Record 178, 383.Google Scholar
Jhaveri, S.R. & Schneider, G.E. (1974 b). Neuroanatomical correlates of spared or altered function after brain lesions in the newborn hamster. In Plasticity and Recovery of Function in the Central Nervous System, ed. Stein, D.G. et al. pp. 65–109. New York: Academic Press.Google Scholar
Knudsen, E.I. (1982). Auditory and visual maps of space in the optic tectum of the owl. Journal of Neuroscience 2, 1177–1194.CrossRefGoogle ScholarPubMed
Murray, M., Sharma, S. & Edwards, M.A. (1982). Target regulation of synaptic number in the compressed retinotectal projection of goldfish. Journal of Comparative Neurology 209, 374–385.CrossRefGoogle ScholarPubMed
Pallas, S.L. & Finlay, B.L. (1986). Effects of increases on retinocollicular convergence ratios on receptive-field properties of single collicular cells. Society for Neuroscience Abstracts 12, 437.Google Scholar
Pallas, S.L. & Finlay, B.L. (1987). Receptive-field size and stimulus selectivity of single collicular cells do not change following early rearrangements of retinocollicular connectivity. Investigative Opthalmology and Visual Science (Suppl.) 28, 123.Google Scholar
Rhoades, R.W. & Chalupa, L.M. (1976). Directional selectivity in the superior colliculus of the golden hamster. Brain Research 118, 334–338.CrossRefGoogle ScholarPubMed
Rhoades, R.W. & Chalupa, L.M. (1978 a). Functional and anatomical consequences of neonatal visual cortical damage in superior colliculus of the golden hamster. Journal of Neurophysiology 41, 1466–1494.CrossRefGoogle ScholarPubMed
Rhoades, R.W. & Chalupa, L.M. (1978 b). Conduction velocity distribution of the retinocollicular pathway in the golden hamster. Brain Research 159, 396–401.CrossRefGoogle ScholarPubMed
Schein, S.J. & De Monasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.CrossRefGoogle ScholarPubMed
Schmidt, J.T., Cicerone, C.M. & Easter, S.S. (1978). Expansion of the half-retinal projection to the tectum in goldfish: an electrophysiological and anatomical study. Journal of Comparative Neurology 177, 257–278.CrossRefGoogle Scholar
Schneider, G.E. (1973). Early lesions of the superior colliculus: Factors affecting the formation of abnormal retinal projections. Brain, Behavior and Evolution 8, 73–109.CrossRefGoogle ScholarPubMed
Sengelaub, D.R., Dolan, R.P. & Finlay, B.L. (1986). Cell generation, death, and retinal growth in the development of the hamster retinal ganglion cell layer. Journal of Comparative Neurology 246, 527–543.CrossRefGoogle ScholarPubMed
Stein, B.E., Magalhaes-Castro, B. & Kruger, L. (1975). Superior colliculus: visuotopic-somatotopic overlap. Science 189, 224–226.CrossRefGoogle ScholarPubMed
Stelzner, D.J. & Strauss, J.A. (1986). A quantitative analysis of frog optic nerve regeneration: is retrograde ganglion cell death or collateral axonal loss related to selective reinnervation? Journal of Comparative Neurology 245, 83–106.CrossRefGoogle ScholarPubMed
Stone, J. (1965). A quantitative analysis of the distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 124, 337–352.CrossRefGoogle ScholarPubMed
Stone, J. (1978). The number and distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 180, 753–772.CrossRefGoogle ScholarPubMed
Tiao, Y.-C. & Blakemore, C. (1976). Functional organization in the superior colliculus of the golden hamster. Journal of Comparative Neurology 168, 483–504.Google ScholarPubMed
Udin, S.B. (1977). Rearrangements of the retinotectal projection in Rana pipiens after unilateral caudal half-tectum ablation. Journal of Comparative Neurology 173, 561–582.CrossRefGoogle ScholarPubMed
Udin, S.B. & Schneider, G.E. (1981). Compressed retinotectal projection in hamsters: fewer ganglion cells project to tectum after neonatal tectal lesions. Experimental Brain Research 43, 261–269.Google ScholarPubMed
Wikler, K.C. & Finlay, B.L. (1984). Deafferentation of the superior colliculus results in decreased synaptic density. Society for Neuroscience Abstracts 10, 462.Google Scholar
Wikler, K.C., Kirn, J., Windrem, M.S. & Finlay, B.L. (1986). Control of cell number in the developing visual system. II. Effects of partial tectal ablation. Developmental Brain Research 28, 11–21.CrossRefGoogle Scholar
Wilson, J.R. & Sherman, S.M. (1976). Receptive-field characteristics of neurons in cat striate cortex: changes with visual-field eccentricity. Journal of Neurophysiology 39, 512–533.CrossRefGoogle ScholarPubMed
Winer, B.J. (1962). Statistical Principles in Experimental Design (2nd edition). New York: McGraw-Hill.CrossRefGoogle Scholar
Woo, H.H., Jen, L.S. & So, K.-F. (1985). The postnatal development of retinocollicular projections in normal hamsters and in hamsters following neonatal monocular enucleation: a horseradish peroxidase tracing study. Developmental Brain Research 20, 1–13.CrossRefGoogle Scholar