Summary
A novel procedure was used to rear kittens under conditions of controlled visual experience: one eye was exposed only to vertical lines while the other eye, simultaneously, was exposed only to horizontal lines. Stimuli were presented in a mask which the animals wore whenever they were in a lighted environment. At the conclusion of the rearing period elongated receptive fields of units recorded from the visual cortex of these animals were oriented either horizontally or vertically. This is in contrast to the full complement of receptive field orientations found in normal cats. Furthermore, units with vertically oriented fields were predominantly or exclusively activated by the eye which had been exposed to vertical lines, while neurons with horizontally oriented fields were predominantly or exclusively activated by the eye which had been exposed to horizontal lines. Normally, 80–90% of the neurons in the visual cortex of the cat are activated by both eyes. The consequences of this controlled visual experience provide evidence for highly selective modification of neuronal connectivity by environmental conditions prevailing during development. Sufficient control of the visual environment was achieved to allow direct comparison between single unit response characteristics and the specific stimuli presented during rearing.
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Barlow, H.B., Blakemore, C., Pettigrew, J.D.: The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.) 193, 327–342 (1967).
Baumgartner, G., Brown, J.L., Schulz, A.: Responses of single units in the cat visual system to rectangular stimulus patterns. J. Neurophysiol. 28, 1–18 (1965).
Bishop, P.O., Kozak, W., Vakkur, G.J.: Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co-ordinates and optics. J. Physiol. (Lond.) 163, 466–502 (1962a).
—, Burke, W., Davis, R.: Interpretation of the extracellular response of single lateral geniculate cells. J. Physiol. (Lond.) 162, 409–431 (1962b).
Blakemore, C., Cooper, G.F.: Development of the brain depends on the visual environment. Nature (Lond.) 228, 477–478 (1970).
Campbell, F.W., Cleland, B.G., Cooper, G.F., Enroth-Cugell, C.: The angular selectivity of visual cortical cells to moving gratings. J. Physiol. (Lond.) 198, 237–250 (1968).
Creutzfeldt, O., Ito, M.: Functional synaptic organization of primary visual cortex neurones in the cat. Exp. Brain Res. 6, 324–352 (1968).
Denney, D.: Unpublished experiments 1967. Cited from Jung (1968).
Ganz, L., Fitch, M., Satterberg, J.A.: The selective effect of visual deprivation on receptive field shape determined neurophysiologically. Exp. Neurol. 22, 614–637 (1968).
Hein, A., Held, R.: Dissociation of the visual placing response into elicited and guided components. Science 158, 390–392 (1967).
Henry, G.H., Bishop, P.O., Coombs, J.S.: Inhibitory and sub-liminal excitatory receptive fields of simple units in cat striate cortex. Vision Res. 9, 1289–1296 (1969).
Hirsch, H.V.B.: The modification of receptive field orientation and visual discrimination by selective exposure during development. Unpublished Ph.D. Thesis, Stanford University (1970).
—, Spinelli, D.N.: Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science 168, 869–871 (1970).
Horn, G., Hill, R.M.: Modifications of receptive fields of cells in the visual cortex occurring spontaneously and associated with bodily tilt. Nature (Lond.) 221, 186–188 (1969).
Hubel, D.H., Wiesel, T.N.: Receptive fields of single neurons in the cat's striate cortex. J. Physiol. (Lond.) 148, 574–591 (1959).
—: Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).
—: Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26, 994–1002 (1963).
—: Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289 (1965a).
—: Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041–1059 (1965b).
—: Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).
—: The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206, 419–436 (1970).
Jung, R.: Optisch-vestibuläre Regulation der Augenbewegung, des Bewegungssehens und der Vertikal-Horizontal-Wahrnehmung: Ein Beitrag zur optisch-vestibulären, optisch-oculomotorischen und optisch-gravizeptorischen Integration. In: Brain and Mind Problems, pp. 204–205 (from 185–226). Ed. by G. Alema et al. Roma: Il Pensiero Scientifico 1968.
Lettvin, J.R., Maturana, H.R., McCulloch, W.S., Pitts, W.H.: What the frog's eye tells the frog's brain. Proc. Inst. Radio Engr. 47, 1940–1951 (1959).
Otsuka, R., Hassler, R.:Über Aufbau und Gliederung der corticalen Sehsphäre bei der Katze. Arch. Psychiat. Nervenkr. 203, 212–234 (1962).
Pettigrew, J.D., Nikara, T., Bishop, P.O.: Responses to moving slits by single units in the cat striate cortex. Exp. Brain Res. 6, 373–390 (1968).
Siegel, S.: Non-parametric Statistics. New York: McGraw-Hill 1956.
Spinelli, D.N.: Receptive field organization of ganglion cells in the cat's retina. Exp. Neurol. 19, 291–315 (1967).
—: Recognition of visual patterns. Proceedings for Research in Nervous and Mental Disease. 48, 139–149 (1968).
—, Barrett, T.W.: Visual receptive field organization of single units in the cat's visual cortex. Exp. Neurol. 24, 76–98 (1969).
Wiesel, T.N., Hubel, D.H.: Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).
—: Comparison of the effects of unilateral and bilateral eye closure on cortical cell responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).
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Note added in press: This aspect of the work is being pursued further. (Spinelli, D.N., Hirsch, H.V.B.: Genesis of receptive field shapes in single units of cat's visual cortex. Federation Proceedings 30, 615 Abs (1971)).
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Hirsch, H.V.B., Spinelli, D.N. Modification of the distribution of receptive field orientation in cats by selective visual exposure during development. Exp Brain Res 12, 509–527 (1971). https://doi.org/10.1007/BF00234246
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DOI: https://doi.org/10.1007/BF00234246