Spontaneously emerging cortical representations of visual attributes

Spontaneous cortical activity—ongoing activity in the absence of intentional sensory input—has been studied extensively, using methods ranging from EEG (electroencephalography), through voltage sensitive dye imaging, down to recordings from single neurons. Ongoing cortical activity has been shown to play a critical role in development, and must also be essential for processing sensory perception, because it modulates stimulus-evoked activity, and is correlated with behaviour. Yet its role in the processing of external information and its relationship to internal representations of sensory attributes remains unknown. Using voltage sensitive dye imaging, we previously established a close link between ongoing activity in the visual cortex of anaesthetized cats and the spontaneous firing of a single neuron. Here we report that such activity encompasses a set of dynamically switching cortical states, many of which correspond closely to orientation maps. When such an orientation state emerged spontaneously, it spanned several hypercolumns and was often followed by a state corresponding to a proximal orientation. We suggest that dynamically switching cortical states could represent the brain's internal context, and therefore reflect or influence memory, perception and behaviour.

[1]  E. Adrian,et al.  THE BERGER RHYTHM: POTENTIAL CHANGES FROM THE OCCIPITAL LOBES IN MAN , 1934 .

[2]  O D Creutzfeldt,et al.  Relations between EEG phenomena and potentials of single cortical cells. II. Spontaneous and convulsoid activity. , 1966, Electroencephalography and clinical neurophysiology.

[3]  W. R. Adey,et al.  Firing variability in cat association cortex during sleep and wakefulness. , 1970, Brain research.

[4]  R. Elul.  The genesis of the EEG. , 1971, International review of neurobiology.

[5]  J. Scherrer,et al.  Organization of spontaneous electrical activity in the neocortex. , 1976, Progress in brain research.

[6]  A. Grinvald,et al.  The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Teuvo Kohonen,et al.  Self-Organizing Maps , 2010 .

[10]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A Grinvald,et al.  Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. , 1995, Journal of neurophysiology.

[12]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

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

[14]  I. Thompson.  Cortical development: A role for spontaneous activity? , 1997, Current Biology.

[15]  D. Fitzpatrick,et al.  Unequal representation of cardinal and oblique contours in ferret visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Bonhoeffer,et al.  Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Håkan Johansson,et al.  Modern Techniques in Neuroscience Research , 1999, Springer Berlin Heidelberg.

[18]  D. McCormick,et al.  Spontaneous Activity: Signal or Noise? , 1999, Science.

[19]  A. Grinvald,et al.  Imaging Cortical Dynamics at High Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999, Neuron.

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

[21]  G. Gerstein,et al.  Trial-to-Trial Variability and State-Dependent Modulation of Auditory-Evoked Responses in Cortex , 1999, The Journal of Neuroscience.

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

[23]  A Grinvald,et al.  In-vivo Optical Imaging of Cortical Architecture and Dynamics , 1999 .

[24]  M. Sur,et al.  Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits. , 1999, Journal of neurobiology.

[25]  M. V. Tsodyks,et al.  Intracortical origin of visual maps , 2001, Nature Neuroscience.

[26]  W. Singer,et al.  Rapid feature selective neuronal synchronization through correlated latency shifting , 2001, Nature Neuroscience.

[27]  R. Lestienne.  Spike timing, synchronization and information processing on the sensory side of the central nervous system , 2001, Progress in Neurobiology.

[28]  Michael Weliky,et al.  Relationship of Correlated Spontaneous Activity to Functional Ocular Dominance Columns in the Developing Visual Cortex , 2002, Neuron.

[29]  Gang Wang,et al.  Difference in the representation of cardinal and oblique contours in cat visual cortex , 2003, Neuroscience Letters.

[30]  R. Freeman,et al.  Oblique effect: a neural basis in the visual cortex. , 2003, Journal of neurophysiology.

[31]  A. Grinvald,et al.  Spatiotemporal Dynamics of Sensory Responses in Layer 2/3 of Rat Barrel Cortex Measured In Vivo by Voltage-Sensitive Dye Imaging Combined with Whole-Cell Voltage Recordings and Neuron Reconstructions , 2003, The Journal of Neuroscience.