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Dynamics of the orientation tuning of postsynaptic potentials in the cat visual cortex

Published online by Cambridge University Press:  02 June 2009

M. Volgushev
Affiliation:
Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen-Nikolausberg, Germany Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia
T.R. Vidyasagar
Affiliation:
Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen-Nikolausberg, Germany Center for Visual Science and Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, Australia
Xing Pei
Affiliation:
Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Göttingen-Nikolausberg, Germany

Abstract

We evaluated the dynamic aspects of the orientation tuning of the input to cat visual cortical neurons by analyzing the postsynaptic potentials (PSPs) evoked by flashing bars of light. The PSPs were recorded using in vivo whole-cell technique, and we analyzed the orientation tuning during subsequent temporal windows after stimulus onset and offset. Our results show that the amplitudes of the postsynaptic potential are reliably tuned to orientation and matching that of the spike responses only during certain temporal windows. During the first 100 ms after stimulus presentation, orientation tuning of the membrane potential underwent regular changes. Within particular intervals, orientation tuning of the input was much sharper than that estimated according to the whole response. In most cells, optimal orientation was usually stable over the whole period. In several cells which had a second hump of EPSPs in the response, this second hump was tuned to the same orientation as the first one, but always showed sharper tuning. Estimation of the integration time revealed sufficient delay between the appearance of EPSPs and spikes, to let inhibition influence spike generation. These results show that orientation selectivity of the input to cortical cells is a dynamic function, and also indicate the possibility of temporal coding in the visual system.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Best, J., Mallot, H., Krüger, K. & Dinse, H.R.O. (1989). Dynamics of visual information processing in cortical systems. In Neural Networks: From Models to Applications, ed. Personnaz, L. & Dreyfus, G., pp. 107116. Paris, France: IDSET.Google Scholar
Celebrimi, S., Thorpe, S., Trotter, Y. & Imbert, M. (1993). Dynamics of orientation coding in area V1 of the awake primate. Visual Neuroscience 10, 811825.CrossRefGoogle Scholar
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974). An intracellular analysis of visual cortical neurons to moving stimuli: Responses in a co-operative neuronal network. Experimental Brain Research 21, 251275.CrossRefGoogle Scholar
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1991). An intracellular analysis of the visual responses of neurons in cat visual cortex. Journal of Physiology 440, 659696.CrossRefGoogle ScholarPubMed
Edwards, F.A., Konnerth, A., Sakmann, B. & Takahashi, T. (1989). A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflügers Archiv 414, 600612.Google Scholar
Ferster, D. & Jagadeesh, B. (1992). EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. Journal of Neuroscience 12, 12621274.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archiv 391, 85100.CrossRefGoogle ScholarPubMed
Henry, G.H. (1977). Receptive field classes of cells in the striate cortex of the cat. Brain Research 133, 128.CrossRefGoogle ScholarPubMed
Nelson, S., Toth, L., Sheth, B. & Sur, M. (1994). Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 774777.CrossRefGoogle ScholarPubMed
Palmer, L.A. & Davis, T.L. (1981). Receptive-field structure in cat striate cortex. Journal of Neurophysiology 46, 260275.Google Scholar
Pei, X., Volgushev, M.A., Vidyasagar, T.R. & Creutzfeldt, O.D. (1991 a). Whole-cell recording and conductance measurements in cat visual cortex in vivo. Neuro Report 2, 485488.Google ScholarPubMed
Pei, X., Volgushev, M. & Creutzfeldt, O.D. (1991 b). Postsynaptic potentials of visual cortical neurons in vivo: II. Receptive-field structure and oscillation. European Journal of Neuroscience (Suppl.) 4, 50.Google Scholar
Pei, X., Vidyasagar, T.R., Volgushev, M. & Creutzfeldt, O.D. (1994). Receptive-field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. Journal of Neuroscience 14, 71307140.Google Scholar
Sakmann, B. & Neher, E. (1983). Single-Channel Recording. Plenum Press, New York.Google Scholar
Shevelev, I.A. & Sharaev, G.A. (1981). Dynamics of orientation tuning of cat visual cortical neurons. Neurophysiology 13, 315320.CrossRefGoogle Scholar
Shevelev, I.A., Sharaev, G.A., Volgushev, M.A., Pyshnyi, M.F. & Verderevskaya, N.N. (1982). Receptive-field dynamics of neurons in the cat visual cortex and lateral geniculate body. Neurophysiology 14, 622630.Google Scholar
Shevelev, I.A., Volgushev, M.A. & Sharaev, G.A. (1992). Dynamics of responses of VI neurons evoked by stimulation of different zones of receptive fields. Neuroscience 51, 445450.CrossRefGoogle Scholar
Shevelev, I.A., Sharaev, G.A., Lazareva, N.A., Novikova, R.V. & Tikhomirov, A.S. (1993). Dynamics of orientation tuning in the cat striate cortex neurons. Neuroscience 56, 865876.CrossRefGoogle ScholarPubMed
Shou, T.D. & Leventhal, A.G. (1989). Organized arrangement of orientation-sensitive relay cells in the cats dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 42874302.Google Scholar
Sillito, A.M., Jones, H.E., Gerstein, G.L. & West, D.C. (1994). Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479482.CrossRefGoogle ScholarPubMed
Soodak, R.E. (1987). Two-dimensional modelling of visual receptive fields using gaussian subunits. Proceedings of the National Academy of Sciences of the U.S.A. 83, 92599263.CrossRefGoogle Scholar
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGN neurons with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157169.Google Scholar
Volgushev, M., Pei, X., Vidyasagar, T.R. & Creutzfeldt, O.D. (1993). Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Visual Neuroscience 10, 11511155.CrossRefGoogle ScholarPubMed