Chaos and synchrony in a model of a hypercolumn in visual cortex

Neurons in cortical slices emit spikes or bursts of spikes regularly in response to a suprathreshold current injection. This behavior is in marked contrast to the behavior of cortical neurons in vivo, whose response to electrical or sensory input displays a strong degree of irregularity. Correlation measurements show a significant degree of synchrony in the temporal fluctuations of neuronal activities in cortex. We explore the hypothesis that these phenomena are the result of the synchronized chaos generated by the deterministic dynamics of local cortical networks. A model of a “hypercolumn” in the visual cortex is studied. It consists of two populations of neurons, one inhibitory and one excitatory. The dynamics of the neurons is based on a Hodgkin-Huxley type model of excitable voltage-clamped cells with several cellular and synaptic conductances. A slow potassium current is included in the dynamics of the excitatory population to reproduce the observed adaptation of the spike trains emitted by these neurons. The pattern of connectivity has a spatial structure which is correlated with the internal organization of hypercolumns in orientation columns. Numerical simulations of the model show that in an appropriate parameter range, the network settles in a synchronous chaotic state, characterized by a strong temporal variability of the neural activity which is correlated across the hypercolumn. Strong inhibitory feedback is essential for the stabilization of this state. These results show that the cooperative dynamics of large neuronal networks are capable of generating variability and synchrony similar to those observed in cortex. Auto-correlation and cross-correlation functions of neuronal spike trains are computed, and their temporal and spatial features are analyzed. In other parameter regimes, the network exhibits two additional states: synchronized oscillations and an asynchronous state. We use our model to study cortical mechanisms for orientation selectivity. It is shown that in a suitable parameter regime, when the input is not oriented, the network has a continuum of states, each representing an inhomogeneous population activity which is peaked at one of the orientation columns. As a result, when a weakly oriented input stimulates the network, it yields a sharp orientation tuning. The properties of the network in this regime, including the appearance of virtual rotations and broad stimulus-dependent cross-correlations, are investigated. The results agree with the predictions of the mean field theory which was previously derived for a simplified model of stochastic, two-state neurons. The relation between the results of the model and experiments in visual cortex are discussed.

[1]  Marius Usher,et al.  Network Amplification of Local Fluctuations Causes High Spike Rate Variability, Fractal Firing Patterns and Oscillatory Local Field Potentials , 1994, Neural Computation.

[2]  Kevan A. C. Martin,et al.  Hybrid analog-digital architectures for neuromorphic systems , 1994, Proceedings of 1994 IEEE International Conference on Neural Networks (ICNN'94).

[3]  Yves Frégnac,et al.  Oscillatory Neuronal Activity in Visual Cortex: A Critical Re-Evaluation , 1994 .

[4]  Apostolos P. Georgopoulos,et al.  Directional operations in the motor cortex modeled by a neural network of spiking neurons , 1994, Biological Cybernetics.

[5]  A. C. Webb,et al.  The spontaneous activity of neurones in the cat’s cerebral cortex , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[6]  Marius Usher,et al.  The Effect of Synchronized Inputs at the Single Neuron Level , 1994, Neural Computation.

[7]  P. Schwindt,et al.  Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro , 1982, Brain Research.

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

[9]  T. Tsumoto,et al.  Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition , 1979, Experimental Brain Research.

[10]  J. Bullier,et al.  Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. , 1995, Journal of neurophysiology.

[11]  Terrence J. Sejnowski,et al.  RAPID STATE SWITCHING IN BALANCED CORTICAL NETWORK MODELS , 1995 .

[12]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[13]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Sompolinsky,et al.  Theory of correlations in stochastic neural networks. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[15]  S. Thorpe,et al.  Dynamics of orientation coding in area V1 of the awake primate , 1993, Visual Neuroscience.

[16]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[17]  E. Fetz,et al.  Synaptic Interactions between Cortical Neurons , 1991 .

[18]  A. Dean The variability of discharge of simple cells in the cat striate cortex , 2004, Experimental Brain Research.

[19]  R. V. Novikova,et al.  Dynamics of orientation tuning in the cat striate cortex neurons , 1993, Neuroscience.

[20]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

[21]  Y. Pomeau,et al.  Order within chaos , 1986 .

[22]  A. Georgopoulos,et al.  Cognitive neurophysiology of the motor cortex. , 1993, Science.

[23]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

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

[25]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Connor,et al.  Neural repetitive firing: modifications of the Hodgkin-Huxley axon suggested by experimental results from crustacean axons. , 1977, Biophysical journal.

[27]  Johan F. Storm,et al.  Functional diversity of K+ currents in hippocampal pyramidal neurons , 1993 .

[28]  E. K. Miller,et al.  Functional interactions among neurons in inferior temporal cortex of the awake macaque , 2004, Experimental Brain Research.

[29]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[30]  Alan Garfinkel,et al.  Self-organizing systems : the emergence of order , 1987 .

[31]  Maureen E. Rush,et al.  The potassium A-current, low firing rates and rebound excitation in Hodgkin-Huxley models , 1995, Bulletin of Mathematical Biology.

[32]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Pierre Bergé,et al.  Order within chaos : towards a deterministic approach to turbulence , 1984 .

[34]  J. Krüger,et al.  Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. , 1988, Journal of neurophysiology.

[35]  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.

[36]  Rodney J. Douglas,et al.  Synchronization of Bursting Action Potential Discharge in a Model Network of Neocortical Neurons , 1991, Neural Computation.

[37]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[38]  Nicolas Brunel,et al.  Global Spontaneous Activity and Local Structured (learned) Delay Activity in Cortex , 1995 .

[39]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[41]  Germán Mato,et al.  Synchrony in Excitatory Neural Networks , 1995, Neural Computation.

[42]  G. Orban,et al.  The response variability of striate cortical neurons in the behaving monkey , 2004, Experimental Brain Research.

[43]  R. Shepard,et al.  Mental Rotation of Three-Dimensional Objects , 1971, Science.

[44]  Bard Ermentrout,et al.  When inhibition not excitation synchronizes neural firing , 1994, Journal of Computational Neuroscience.

[45]  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.

[46]  W. Singer Topographic organization of orientation columns in the cat visual cortex , 1981, Experimental Brain Research.

[47]  H. Wigström,et al.  A transient outward current in a mammalian central neurone blocked by 4-aminopyridine , 1982, Nature.

[48]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[49]  Reinhard Eckhorn,et al.  Feature Linking via Synchronization among Distributed Assemblies: Simulations of Results from Cat Visual Cortex , 1990, Neural Computation.

[50]  B. Finlay,et al.  Short-term response variability of monkey striate neurons , 1976, Brain Research.

[51]  K. Martin,et al.  The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. , 1988, Quarterly journal of experimental physiology.

[52]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[53]  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.

[54]  Hansel,et al.  Synchronization and computation in a chaotic neural network. , 1992, Physical review letters.

[55]  Pieter R. Roelfsema,et al.  How Precise is Neuronal Synchronization? , 1995, Neural Computation.

[56]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[58]  Ernst,et al.  Synchronization induced by temporal delays in pulse-coupled oscillators. , 1995, Physical review letters.

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

[60]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[61]  Eberhard E. Fetz,et al.  Effects of Input Synchrony on the Firing Rate of a Three-Conductance Cortical Neuron Model , 1994, Neural Computation.