Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models

Networks of compartmental model neurons were used to investigate the biophysical basis of the synchronization observed between sparsely-connected neurons in neocortex. A model of a single column in layer 5 consisted of 100 model neurons: 80 pyramidal and 20 inhibitory. The pyramidal cells had conductances that caused intrinsic repetitive bursting at different frequencies when driven with the same input. When connected randomly with a connection density of 10%, a single model column displayed synchronous oscillatory action potentials in response to stationary, uncorrelated Poisson spike-train inputs. Synchrony required a high ratio of inhibitory to excitatory synaptic strength; the optimal ratio was 4∶1, within the range observed in cortex. The synchrony was insensitive to variation in amplitudes of postsynaptic potentials and synaptic delay times, even when the mean synaptic delay times were varied over the range 1 to 7 ms. Synchrony was found to be sensitive to the strength of reciprocal inhibition between the inhibitory neurons in one column: Too weak or too strong reciprocal inhibition degraded intra-columnar synchrony. The only parameter that affected the oscillation frequency of the network was the strength of the external driving input which could shift the frequency between 35 to 60 Hz. The same results were obtained using a model column of 1000 neurons with a connection density of 5%, except that the oscillation became more regular.Synchronization between cortical columns was studied in a model consisting of two columns with 100 model neurons each. When connections were made with a density of 3% between the pyramidal cells of each column there was no inter-columnar synchrony and in some cases the columns oscillated 180° out of phase with each other. Only when connections from the pyramidal cells in each column to the inhibitory cells in the other column were added was synchrony between the columns observed. This synchrony was established within one or two cycles of the oscillation and there was on average less than 1 ms phase difference between the two columns. Unlike the intra-columnar synchronization, the inter-columnar synchronization was found to be sensitive to the synaptic delay: A mean delay of greater than 5 ms virtually abolished synchronization between columns.

[1]  U. Eysel,et al.  Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17) , 1992, Neuroscience.

[2]  P König,et al.  Direct physiological evidence for scene segmentation by temporal coding. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E. White.  Cortical Circuits , 1989, Birkhäuser Boston.

[4]  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10-to 50-Hz frequency range , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Henry,et al.  Properties of area 17/18 border neurons contributing to the visual transcallosal pathway in the cat , 1990, Visual Neuroscience.

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

[7]  Colin Blakemore,et al.  Patterns of Local Connectivity in the Neocortex , 1993, Neural Computation.

[8]  W. Singer,et al.  Relation between oscillatory activity and long-range synchronization in cat visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Matthew A. Wilson,et al.  A Computer Simulation of Oscillatory Behavior in Primary Visual Cortex , 1991, Neural Computation.

[10]  H. Schuster,et al.  Mutual Entrainment of Two Limit Cycle Oscillators with Time Delayed Coupling , 1989 .

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

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

[13]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[14]  V. Bringuier,et al.  Synaptic origin of rhythmic visually evoked activity in kitten area 17 neurones. , 1992, Neuroreport.

[15]  N. Kopell,et al.  Rhythmogenesis, amplitude modulation, and multiplexing in a cortical architecture. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Thomson,et al.  Voltage-dependent currents prolong single-axon postsynaptic potentials in layer III pyramidal neurons in rat neocortical slices. , 1988, Journal of neurophysiology.

[17]  C. Gray,et al.  Visually evoked oscillations of membrane potential in cells of cat visual cortex. , 1992, Science.

[18]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[19]  B. Connors,et al.  Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor‐mediated responses in neocortex of rat and cat. , 1988, The Journal of physiology.

[20]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

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

[22]  T. Wiesel,et al.  Lateral interactions in visual cortex. , 1990, Cold Spring Harbor symposia on quantitative biology.

[23]  E. Azmitia.  Microcultures of Dissociated Primary Central Nervous System Neurons , 1990 .

[24]  W. Singer,et al.  Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey , 1992, The European journal of neuroscience.

[25]  Peter König,et al.  Stimulus-Dependent Assembly Formation of Oscillatory Responses: I. Synchronization , 1991, Neural Computation.

[26]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[27]  C. Koch,et al.  Visibility of synaptically induced conductance changes: theory and simulations of anatomically characterized cortical pyramidal cells , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Pettet,et al.  Dynamic changes in receptive-field size in cat primary visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[29]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Inter‐Columnar Interaction as Determined by Cross‐Correlation Analysis , 1990, The European journal of neuroscience.

[30]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[31]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[32]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[34]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[35]  R. Llinás,et al.  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[36]  C. Koch,et al.  Synaptic Background Activity Influences Spatiotemporal Integration in Single Pyramidal Cells. , 1991, The Biological bulletin.

[37]  D. Whitteridge,et al.  Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17) , 1987, The Journal of comparative neurology.

[38]  H. Schuster,et al.  A model for neuronal oscillations in the visual cortex , 1990, Biological Cybernetics.

[39]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[40]  T. Sejnowski,et al.  Effects of inhibition and dendritic saturation in simulated neocortical pyramidal cells. , 1994, Journal of neurophysiology.

[41]  T. Sejnowski,et al.  Reduced compartmental models of neocortical pyramidal cells , 1993, Journal of Neuroscience Methods.

[42]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[43]  E. Fetz,et al.  Intracortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex , 1988, Brain Research.

[44]  G. Edelman,et al.  Reentrant signaling among simulated neuronal groups leads to coherency in their oscillatory activity. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[45]  A. Winfree.  Biological rhythms and the behavior of populations of coupled oscillators. , 1967, Journal of theoretical biology.

[46]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[47]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[48]  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.

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

[50]  H. Swadlow,et al.  Efferent neurons and suspected interneurons in second somatosensory cortex of the awake rabbit: receptive fields and axonal properties. , 1991, Journal of neurophysiology.

[51]  W. Singer,et al.  Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties , 1992, Visual Neuroscience.

[52]  H Sompolinsky,et al.  Global processing of visual stimuli in a neural network of coupled oscillators. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[53]  G Tononi,et al.  Modeling perceptual grouping and figure-ground segregation by means of active reentrant connections. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[54]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[55]  C. Koch,et al.  Towards a neurobiological theory of consciousness , 1990 .

[56]  T. Williams.  Phase coupling by synaptic spread in chains of coupled neuronal oscillators. , 1992, Science.