Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-30T05:28:46.669Z Has data issue: false hasContentIssue false

Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties

Published online by Cambridge University Press:  02 June 2009

Charles M. Gray
Affiliation:
Max-Planck-lnstitute fur Hirnforschung, Deutschordenstrasse 46, 6000 Frankfurt a.M.71, Germany
Andreas K. Engel
Affiliation:
Max-Planck-lnstitute fur Hirnforschung, Deutschordenstrasse 46, 6000 Frankfurt a.M.71, Germany
Peter König
Affiliation:
Max-Planck-lnstitute fur Hirnforschung, Deutschordenstrasse 46, 6000 Frankfurt a.M.71, Germany
Wolf Singer
Affiliation:
Max-Planck-lnstitute fur Hirnforschung, Deutschordenstrasse 46, 6000 Frankfurt a.M.71, Germany

Abstract

Previously, we have demonstrated that a subpopulation of visual cortical neurons exhibit oscillatory responses to their preferred stimuli at a frequency near 50 Hz (Gray & Singer, 1989). These responses can selectively synchronize over large distances of cortex in a stimulus-specific manner (Gray et al., 1989; Engel et al., 1990a). Here we report the results of a new analysis which reveals the fine temporal structure inherent in these interactions. We utilized pairs of recordings of the local field potential (LFP) activity from area 17 in the anesthetized cat which met two criteria. The LFP was correlated with the underlying unit activity at each site and the recording sites were at least 5 mm apart in cortex. A moving-window technique was applied to compute cross correlograms on 100-ms epochs of data repeated at intervals of 30 ms for a period of 3 s during each direction of stimulus movement. A statistical test was devised to determine the significance of detected correlations. In this way we were able to determine the magnitude, phase difference, frequency, and duration of correlated oscillations as a function of time. The results demonstrate that (1) the duration of synchrony is variable and lasts from 100–900 ms; (2) the phase differences between and the frequencies of synchronized responses are also variable within and between events and range from +3 to —3 ms and 40–60 Hz, respectively; and (3) multiple correlation events often occur within a single stimulus period. These results demonstrate a high degree of dynamic variability and a rapid onset and offset of synchrony among interacting populations of neurons which is consistent with the requirements of a mechanism for feature integration.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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

Bergen, J.R. & Julesz, B. (1983). Parallel versus serial processing in rapid pattern discrimination. Nature 303, 696698.CrossRefGoogle ScholarPubMed
Biederman, I. (1981). On the semantics of a glance at a scene. In Perceptual Organization, ed. Kubovy, M. & Pomerantz, J.R.Hillsdale, New Jersey: Erlbaum.Google Scholar
Crick, F. & Koch, C. (1990). Towards a neurobiological theory of consciousness. Seminars in Neuroscience 2 (4), 263275.Google Scholar
Damasio, A.R. (1989). The brain binds entities and events by multiregional activation from convergence zones. Neural Computation 1, 123132.CrossRefGoogle Scholar
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M. & Reitboeck, H.J. (1988). Coherent oscillations: a mechanism of feature linking in the visual cortex? Biological Cybernetics 60, 121130.CrossRefGoogle ScholarPubMed
Edelman, C.M. & Mountcastle, V.B. (1978). The Mindful Brain. Cambridge, Massachusetts: MIT Press.Google Scholar
Engel, A.K., Konig, P., Gray, C.M. & Singer, W. (1990a). Stimulus-dependent neuronal oscillations in cat visual cortex: inter-columnar interaction as determined by cross-correlation analysis. European Journal of Neuroscience 2, 588606.CrossRefGoogle ScholarPubMed
Engel, A.K., Konig, P., Kreiter, A.K., Gray, C.M. & Singer, W. (1990b). Temporal coding by coherent oscillations as a potential solution to the binding problem: physiological evidence. In Nonlinear Dynamics and Neural Networks, ed. Schuster, H. & Singer, W., pp. 326. Weinheim.Google Scholar
Engel, A.K., Konig, P., Kreiter, A.K. & Singer, W. (1991a). Interhemispheric synchronization of oscillatory responses in cat visual cortex. Science 252, 11771179.CrossRefGoogle ScholarPubMed
Engel, A.K., Kreiter, A.K., KÖNig, P. & Singer, W. (1991b). Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proceedings of the National Academy of Sciences of the U.S.A. 88, 60486052.CrossRefGoogle ScholarPubMed
Freeman, W.J. (1985). Analytic techniques used in the search for the physiological basis for the EEG. In Handbook of Electroen-cephalography and Clinical Neurophysiology, Vol. 3 A, Part 2, ed. Gevins, A. & Remond, A., Chap. 18. Amsterdam: Elsevier.Google Scholar
Gerstein, G.L., Bedenbaugh, P. & Aertsen, A.M.H.J. (1989). Neuronal assemblies. IEEE Transactions on Biomedical Engineering 36 (1), 414.CrossRefGoogle ScholarPubMed
Gray, C. & Singer, W. (1987). Stimulus-specific neuronal oscillations in the cat visual cortex: a cortical functional unit. Society for Neuroscience Abstracts 13, 404–3.Google Scholar
Gray, C.M. & Skinner, J.E. (1988). Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Experimental Brain Research 69, 378386.CrossRefGoogle ScholarPubMed
Gray, C. & Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 86, 16981702.CrossRefGoogle ScholarPubMed
Gray, C., KÖnig, P., Engel, A.K. & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334337.CrossRefGoogle ScholarPubMed
Gray, C., Engel, A.K., KÖNig, P. & Singer, W. (1990a). Stimulus-dependent neuronal oscillations in cat visual cortex: receptive field properties and feature dependence. European Journal of Neuroscience 2, 607619.CrossRefGoogle ScholarPubMed
Gray, C., KÖNig, P., Engel, A.K. & Singer, W. (1990b). Synchronization of oscillatory responses in visual cortex: a plausible mechanism for scene segmentation. In Synergetics of Cognition, ed. Haken, H. & Stadler, M., pp. 8298. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Hebb, D.O. (1949). The Organization of Behavior: A Neuropsychological Theory. New York: Wiley.Google Scholar
Intraub, H. (1981). Identification and naming of briefly glimpsed visual scenes. In Eye Movements: Cognition and Visual Perception, ed., Fisher, D.F., Monty, R.A. & Senders, J.W.Hillsdale, New Jersey: L. Erlbaum Associates.Google Scholar
Jacadeesh, B., Ferster, D. & Gray, C.M. (1991). Visually evoked oscillations of membrane potential in neurons of cat area 17. Society for Neuroscience Abstracts, 17, 73.2.Google Scholar
Malsburg, C. Von Der (1981). The correlation theory of the brain. Internal Report, Max-Planck-Institute for Biophysical Chemistry, Gottingen, Germany.Google Scholar
Malsburg, C. Von Der (1985). Nervous structures with dynamical links. Ber. Bunsenges. Phys. Chem. 89, 703710.CrossRefGoogle Scholar
Michalski, A., Gerstein, G.L., Czarkowska, J. & Tarnecki, R. (1983). Interactions between cat striate cortex neurons. Experimental Brain Research 51, 97107.CrossRefGoogle ScholarPubMed
Milner, P. (1974). A model for visual shape recognition. Psychological Review 8 (6), 521535.CrossRefGoogle Scholar
Mioche, L. & Singer, W. (1989). Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties. Journal of Neurophysiology 62(1), 185197.CrossRefGoogle ScholarPubMed
Palm, G. (1982). Neural Assemblies-Studies of Brain Functions, Vol. 7, New York: Springer.Google Scholar
Potter, M. C. (1975). Meaning in visual search. Science 187, 965966.CrossRefGoogle ScholarPubMed
Raether, A., Gray, C.M. & Singer, W. (1989). Intercolumnar interactions of oscillatory neuronal responses in the visual cortex of alert cats. European Neuroscience Association Abstracts 11, 72.5.Google Scholar
Singer, W. (1990). Search for coherence: a basic principle of cortical self-organization. Concepts in Neuroscience 1(1), 126.Google Scholar
Ts'o, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6(4), 11601170.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuro-science 8(5), 17121727.Google ScholarPubMed
Weisstein, N. & Harris, C.S. (1974). Visual detection of line segments: an object superiority effect. Science 186, 752755.CrossRefGoogle ScholarPubMed