Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model

TLDR

Fast neuronal oscillations (gamma, 20–80 Hz) have been observed in the neocortex and hippocampus during behavioral arousal. Using computer simulations, we tested whether rhythmic activity can arise in a random network of GABAergic fast‑spiking interneurons. The simulations revealed that synchronized gamma oscillations arise only when the spike afterhyperpolarization exceeds the GABA A reversal potential, the synaptic decay time constant is sufficiently long relative to the oscillation period, heterogeneities are modest, and each neuron receives a critical but size‑independent number of synaptic contacts; varying GABA A conductance, decay time, or excitatory drive shifts firing rates but keeps synchronization confined to the 20–80 Hz band, supporting the view that GABA A transmission enables gamma‑range network synchrony in sparsely connected fast‑spiking interneuron circuits and can entrain principal cells.

Abstract

Fast neuronal oscillations (gamma, 20–80 Hz) have been observed in the neocortex and hippocampus during behavioral arousal. Using computer simulations, we investigated the hypothesis that such rhythmic activity can emerge in a random network of interconnected GABAergic fast-spiking interneurons. Specific conditions for the population synchronization, on properties of single cells and the circuit, were identified. These include the following: (1) that the amplitude of spike afterhyperpolarization be above the GABA A synaptic reversal potential; (2) that the ratio between the synaptic decay time constant and the oscillation period be sufficiently large; (3) that the effects of heterogeneities be modest because of a steep frequency–current relationship of fast-spiking neurons. Furthermore, using a population coherence measure, based on coincident firings of neural pairs, it is demonstrated that large-scale network synchronization requires a critical (minimal) average number of synaptic contacts per cell, which is not sensitive to the network size. By changing the GABA A synaptic maximal conductance, synaptic decay time constant, or the mean external excitatory drive to the network, the neuronal firing frequencies were gradually and monotonically varied. By contrast, the network synchronization was found to be high only within a frequency band coinciding with the gamma (20–80 Hz) range. We conclude that the GABA A synaptic transmission provides a suitable mechanism for synchronized gamma oscillations in a sparsely connected network of fast-spiking interneurons. In turn, the interneuronal network can presumably maintain subthreshold oscillations in principal cell populations and serve to synchronize discharges of spatially distributed neurons.