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

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Abstract

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.

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  1. Paul Bush

    Present address: Keck Center for Integrative Neuroscience, University of California, San Francisco, 513 Parnassus Avenue, Box 0444, 94143-0444, San Francisco, CA

Authors and Affiliations

  1. Howard Hughes Medical Institute, Computational Neurobiology Laboratory, Salk Institute, 92037, La Jolla, CA, USA

    Paul Bush

  2. Departments of Biology and Neuroscience, University of California at San Diego, 92093, La Jolla, CA, USA

    Terrence Sejnowski

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Bush, P., Sejnowski, T. Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models. J Comput Neurosci 3, 91–110 (1996). https://doi.org/10.1007/BF00160806

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  • DOI: https://doi.org/10.1007/BF00160806

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