Rapid feature selective neuronal synchronization through correlated latency shifting

Spontaneous brain activity could affect processing if it were structured, . We show that neuron pairs in cat primary visual cortex exhibited correlated fluctuations in response latency, particularly when they had overlapping receptive fields or similar orientation preferences. Correlations occurred within and across hemispheres, but only when local field potentials (LFPs) oscillated in the gamma-frequency range (40–70 Hz). In this range, LFP fluctuations preceding response onset predicted response latencies; negative (positive) LFPs were associated with early (late) responses. Oscillations below 10 Hz caused covariations in response amplitude, but exhibited no columnar selectivity or coordinating effect on latencies. Thus, during high gamma activity, spontaneous activity exhibits distinct, column-specific correlation patterns. Consequently, cortical cells undergo coherent fluctuations in excitability that enhance temporal coherence of responses to contours that are spatially contiguous or have similar orientation. Because synchronized responses are more likely than dispersed responses to undergo rapid and joint processing, spontaneous activity may be important in early visual processes.

[1]  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.

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

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

[4]  I. Lampl,et al.  Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. , 1993, Journal of neurophysiology.

[5]  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.

[6]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[7]  M. Steriade,et al.  Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation. , 1995, Journal of neurophysiology.

[8]  D Contreras,et al.  State-dependent fluctuations of low-frequency rhythms in corticothalamic networks , 1996, Neuroscience.

[9]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[10]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

[11]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[12]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[13]  R. Reid,et al.  Precisely correlated firing in cells of the lateral geniculate nucleus , 1996, Nature.

[14]  T. Jung,et al.  Tonic, phasic, and transient EEG correlates of auditory awareness in drowsiness. , 1996, Brain research. Cognitive brain research.

[15]  D. Snodderly,et al.  Response Variability of Neurons in Primary Visual Cortex (V1) of Alert Monkeys , 1997, The Journal of Neuroscience.

[16]  Maria V. Sanchez-Vives,et al.  Influence of low and high frequency inputs on spike timing in visual cortical neurons. , 1997, Cerebral cortex.

[17]  W. Singer,et al.  Functional Specificity of Long-Range Intrinsic and Interhemispheric Connections in the Visual Cortex of Strabismic Cats , 1997, The Journal of Neuroscience.

[18]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[19]  W. Singer,et al.  Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential , 1998, Neuroscience.

[20]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

[21]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[22]  W. Singer,et al.  Correlation analysis of corticotectal interactions in the cat visual system. , 1998, Journal of neurophysiology.

[23]  Nicholas V. Swindale,et al.  Orientation tuning curves: empirical description and estimation of parameters , 1998, Biological Cybernetics.

[24]  C. Gilbert,et al.  Topography of contextual modulations mediated by short-range interactions in primary visual cortex , 1999, Nature.

[25]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[26]  D. Ferster,et al.  Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex , 1999, Neuron.

[27]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[28]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[29]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[30]  W. Singer,et al.  Precisely Synchronized Oscillatory Firing Patterns Require Electroencephalographic Activation , 1999, The Journal of Neuroscience.

[31]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.