Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T06:03:02.880Z Has data issue: false hasContentIssue false

Development of visual inhibitory interactions in kittens

Published online by Cambridge University Press:  02 June 2009

M. Concetta Morrone
Affiliation:
Scuola Normale Superiore, Pisa, Italy
Harriet D. Speed
Affiliation:
Department of Psychology, University of Western Australia, Nedlands, Western Australia, 6009, Australia
David C. Burr
Affiliation:
Istituto di Neurofisiologia del CNR, Via S. Zeno 51, Pisa 56100, Italy

Abstract

This study was designed to monitor the development of inhibitory interactions elicited in the cat visual system by oriented visual stimuli. Steady-state visual-evoked potentials (VEPs) were recorded from the scalp of 11 behaving and alert kittens while they viewed contrast-reversed sinusoidal gratings. In adult cats, the form of VEP contrast-response curves (the amplitude of second harmonic modulation as a function of stimulus contrast) was modified by superimposing a mask grating on the test. Parallel masks displaced the curves to a higher contrast region (probably via contrast gain-control mechanisms), increasing contrast threshold without affecting the slope of the curve. Orthogonal gratings, on the other hand, decrease the slope of the curve without affecting threshold (so called cross-orientation inhibition: Morrone et al., 1981). These effects are similar to those previously reported in human VEPs (Morrone & Burr, 1986; Burr & Morrone, 1987) and single cortical cat cells (Morrone et al., 1982). For young kittens of 20 days, the orthogonal mask had no effect whatsoever on the response curves, and the effect of the parallel mask was much less than for adult cats. At about 40 days, the orthogonal mask began to attenuate responses multiplicatively, and by 50 days the amount of multiplicative attenuation had reached adult levels. The effect of the parallel mask (as indicated by the increase in threshold elevation) increased gradually from 20–50 days. The results are consistent with the existence of at least two types of inhibition in cat visual neurones that develop at different rates.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology (London) 347, 713739.Google Scholar
Albus, K. & Wolf, W. (1984). Early post-natal development of neuronal function in the kitten's visual cortex: a laminar analysis. Journal of Physiology (London) 348, 153185.Google Scholar
Anderson, S.J. & Burr, D.C. (1991). The two-dimensional spatial and spatial frequency properties of motion-sensitive mechanisms in human vision. Journal of the Optical Society of America (in press).Google ScholarPubMed
Atkinson, J., Hood, B., Watten-Bell, J., Anker, S. & Tricklebank, J. (1988). Development of orientation discrimination in infancy. Perception 17, 587595.CrossRefGoogle ScholarPubMed
Berardi, N. & Morrone, M.C. (1984a). The role of γ-aminobutyric acid mediated inhibition in the response properties of cat lateral geniculate nucleus neurones. Journal of Physiology 357, 505523.CrossRefGoogle ScholarPubMed
Berardi, N. & Morrone, M.C. (1984b). Development of γ-aminobutyric acid mediated inhibition of X cells of the cat lateral geniculate nucleus. Journal of Physiology 357, 525537.CrossRefGoogle ScholarPubMed
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology (London) 231, 3160.Google Scholar
Blakemore, C. & Price, D.J. (1987). The organization of postnatal development of area 18 of the cat's visual cortex. Journal of Physiology (London) 384, 263292.Google Scholar
Blakemore, C. & van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology (London) 248, 663716.Google Scholar
Bonds, A.B. (1979). Development of orientation tuning in the visual cortex of kittens. In Developmental Neurobiology of Vision ed. Freeman, R.D., pp. 3141. New York: Plenum Press.CrossRefGoogle Scholar
Braadstad, B.O. & Heggelund, P. (1985). Development of spatial receptive-field organization and orientation selectivity in kitten striate cortex. Journal of Neurophysiology 53, 11581178.CrossRefGoogle Scholar
Braddick, O.J., Wattam-Bell, J. & Atkinson, J. (1986). Orientation specific cortical responses develop in early infancy. Nature (London) 320, 617619.Google Scholar
Burr, D.C. & Morrone, M.C. (1987). Inhibitory interactions in the human visual system revealed in pattern-evoked potentials. Journal of Physiology (London) 389, 121.Google Scholar
Burr, D.C., Morrone, M.C. & Maffei, L. (1981). Intracortical inhibition prevents simple cells from responding to textured patterns. Experimental Brain Research 43, 455458.Google Scholar
Campbell, F.W., Maffei, L. & Piccolino, M. (1973). The contrast sensitivity of the cat. Journal of Physiology (London) 229, 719731.Google Scholar
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974). An intracellular analysis of cortical neurones to moving stimuli: responses in a cooperative neuronal network. Experimental Brain Research 21, 251274.CrossRefGoogle Scholar
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1988). Selective responses of visual cortical cells do not depend on shunting inhibition. Nature 332, 642644.CrossRefGoogle Scholar
Eccles, J.C. (1969). The Inhibitory Pathways of the Central Nervous System. Liverpool: University Press.Google Scholar
Ferster, D. (1986). Orientation selectivity of synaptic potentials in neurones of cat primary visual cortex. Journal of Neuroscience 6, 12841301.CrossRefGoogle ScholarPubMed
Fregnac, Y. & Imbert, M. (1978). Early development of visual cortical cells in normal and dark-reared kittens: relationship between orientation selectivity and ocular dominance. Journal of Physiology (London) 278, 2744.Google Scholar
Fregnac, Y. & Imbert, M. (1984). Development of neuronal selectivity in primary visual cortex of cat. Physiological Reviews 64, 325434.CrossRefGoogle ScholarPubMed
Fries, W., Albus, K. & Creutzfeldt, O.D. (1977). Effects of interacting visual patterns on single-cell responses in cat's striate cortex. Vision Research 17, 10011008.CrossRefGoogle Scholar
Hata, Y., Tsumoto, T., Hagihara, K. & Tamura, H. (1988). Inhibition contributes to orientation selectivity in visual cortex of cat. Nature (London) 335, 815817.Google Scholar
Heggelund, P. & Moors, J. (1983). Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells. Experimental Brain Research 52, 235247.Google ScholarPubMed
Komatsu, Y. (1983). Development of cortical inhibition in kitten striate cortex investigated by a slice preparation. Developmental Brain Research 8, 136139.CrossRefGoogle Scholar
Legge, G.E. & Foley, J.M. (1980). Contrast masking in human vision. Journal of the Optical Society of America 70, 14581471.CrossRefGoogle ScholarPubMed
Milleret, C., Gary-Bobo, E. & Buisseret, P. (1988). Comparative development of cell properties in cortical area 18 of normal and darkreared kittens. Experimental Brain Research 71, 820.CrossRefGoogle ScholarPubMed
Mitchell, D.E. & Timney, B. (1984). Post-natal development of function in the mammalian visual system. In Handbook of Physiology: Nervous System, Vol. III, ed. Darion-Smith, I., pp. 507555. Bethesda: American Physiology Society.Google Scholar
Morrone, M.C. & Burr, D.C. (1986). Evidence for the existence and development of visual inhibition in humans. Nature (London) 321, 235237.Google Scholar
Morrone, M.C. & Burr, D.C. (1991). A model of human feature detection based on matched features. In Robots and Biological Systems, ed. Dario, P., Sandini, G. & Aebischer, P.Berlin: Springer-Verlag.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional significance of cross-orientational inhibition, Pt. I: Neurophysiology. Proceedings of the Royal Society B (London) 216, 335354.Google Scholar
Morrone, M.C., Burr, D.C. & Ross, J. (1983). Added noise restores recognizability of coarse quantized images. Nature (London) 305, 226228.Google Scholar
Morrone, M.C., Burr, D.C. & Speed, H.D. (1987). Cross-orientation inhibition in cat is GABA-mediated. Experimental Brain Research 67, 635644.CrossRefGoogle ScholarPubMed
Ohzawa, I., Sclar, G. & Freeman, R.D. (1982). Contrast gain control in the cat visual cortex. Nature (London) 298, 266268.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.CrossRefGoogle ScholarPubMed
Ramoa, A.S., Shadlen, M., Skottun, B.C. & Freeman, R.D. (1986). A comparison of inhibition in orientation and spatial-frequency selectivity of cat visual cortex. Nature 321, 237239.CrossRefGoogle ScholarPubMed
Sclar, G., Ohzawa, I. & Freeman, R.D. (1985). Contrast gain control in the kitten's visual system. Journal of Neurophysiology 54, 668673.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. In Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, G.J., pp. 263346. Oxford: Pergamon Press.Google Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology (London) 318, 161179.Google Scholar
Shaw, C., Needler, M.C., Wilkinson, M., Aoki, C. & Cynader, M. (1985). Modification of neurotransmitter receptor sensitivity in cat visual cortex during the critical period. Developmental Brain Research 22, 6773.CrossRefGoogle Scholar
Sherk, H. & Stryker, M.P. (1976). Quantitative study of cortical orientation selectivity in visually inexperienced kittens. Journal of Neurophysiology 39, 6370.CrossRefGoogle Scholar
Sherman, M.S. & Spear, P.D. (1982). Organization of visual pathways in normal and visual deprived cats. Physiological Reviews 62, 738855.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1975a). The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. Journal of Physiology (London) 250, 287304.Google Scholar
Sillito, A.M. (1975b). The contribution of inhibitory mechanisms to the receptive-field properties of neurones in the striate cortex of the cat. Journal of Physiology (London) 250, 305329.Google Scholar
Sillito, A.M. (1979). Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. Journal of Physiology (London) 289, 3353.Google Scholar
Sillito, A.M., Kemp, J.A., Milson, J.A. & Berardi, N. (1980). A reevaluation of the mechanisms underlying simple cortical cell activity. Brain Research 194, 517520.CrossRefGoogle Scholar
Tolhurst, D.J. & Dean, A.F. (1987). Spatial summation by simple cells in the striate cortex of the cat. Experimental Brain Research 66, 607620.CrossRefGoogle ScholarPubMed
Toyama, K., Kimura, M. & Tanaka, K. (1981). Organization of cat visual cortex as investigated by cross-correlation technique. Journal of Neurophysiology 46, 202214.CrossRefGoogle ScholarPubMed
Tsumoto, T. & Sato, H. (1985). GABAergic inhibition and orientation selectivity of neurones in the kitten visual cortex at the time of eye-opening. Vision Research 25, 383388.CrossRefGoogle ScholarPubMed
Tsumoto, T., Eckart, W. & Creutzfeldt, O.D. (1979). Modifications of orientation selectivity of cat visual cortex neurones by removal of GABA-mediated inhibition. Experimental Brain Research 34, 351363.CrossRefGoogle Scholar
Vidyasagar, T.R. & Heide, W. (1986). The role of GABAergic inhibition in the response properties of neurones in cat visual area 18. Neuroscience 17, 4955.CrossRefGoogle ScholarPubMed
Winfield, D.A. (1981). The post-natal development of synapses in the visual cortex of the cat and the effects of eye-lid closure. Brain Research 206, 166171.CrossRefGoogle Scholar
Wolf, W., Hicks, T.P. & Albus, K. (1986). The contribution of GABA-mediated inhibitory mechanisms to visual response properties of neurones in the kitten striate cortex. Journal of Neuroscience 6, 27792795.CrossRefGoogle Scholar