Visuomotor integration is associated with zero time-lag synchronization among cortical areas

INFORMATION processing in the cerebral cortex invariably involves the activation of millions of neurons that are widely distributed over its various areas. These distributed activity patterns need to be integrated into coherent representational states. A candidate mechanism for the integration and coordination of neuronal activity between different brain regions is synchronization on a fine temporal scale1–3. In the visual cortex, synchronization occurs selectively between the responses of neurons that represent related features2–5 and that need to be integrated for the generation of coherent percepts; neurons in other areas of the cerebral cortex also synchronize their discharges6–10. However, little is known about the patterns and the behavioural correlates of synchrony among widely separated cortical regions. Here we report that synchronization occurs between areas of the visual and parietal cortex, and between areas of the parietal and motor cortex, in the awake cat. When cats responded to a sudden change of a visual pattern, neuronal activity in cortical areas exhibited synchrony without time lags; this synchrony was particularly strong between areas subserving related functions. During reward and inter-trial episodes, zero-time-lag synchrony was lost and replaced by interactions exhibiting large and unsystematic time lags.

[1]  F. Horvath,et al.  Electroencephalogram Rhythms correlated with Milk Reinforcement in Cats , 1964, Nature.

[2]  A. Nieoullon,et al.  Somatotopic localization in cat motor cortex , 1976, Brain Research.

[3]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[4]  J. Bouyer,et al.  Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations. , 1981, Electroencephalography and clinical neurophysiology.

[5]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[6]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[7]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[8]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[9]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[11]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[12]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[13]  Paul Antoine Salin,et al.  Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17 and 18 in the cat. , 1992, Visual neuroscience.

[14]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[15]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[16]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[18]  S. Bressler,et al.  Episodic multiregional cortical coherence at multiple frequencies during visual task performance , 1993, Nature.

[19]  R. Eckhorn,et al.  Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. , 1994, Neuroreport.

[20]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[21]  C. Blakemore,et al.  Analysis of connectivity in the cat cerebral cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J Bullier,et al.  Structural basis of cortical synchronization. II. Effects of cortical lesions. , 1995, Journal of neurophysiology.

[23]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[24]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[25]  D. Contreras,et al.  Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  W. Singer,et al.  The Role of Neuronal Synchronization in Response Selection: A Biologically Plausible Theory of Structured Representations in the Visual Cortex , 1996, Journal of Cognitive Neuroscience.

[27]  W. Singer,et al.  Role of Reticular Activation in the Modulation of Intracortical Synchronization , 1996, Science.