Regulation of gamma-frequency oscillation by feedforward inhibition: A computational modeling study

Throughout the brain, reciprocally connected excitatory and inhibitory neurons interact to produce gamma-frequency oscillations. The emergent gamma rhythm synchronizes local neural activity and helps to select which cells should fire in each cycle. We previously found that such excitation-inhibition microcircuits, however, have a potentially significant caveat: the frequency of the gamma oscillation and the level of selection (i.e., the percentage of cells that are allowed to fire) vary with the magnitude of the input signal. In networks with varying levels of brain activity, such a feature may produce undesirable instability on the time and spatial structure of the neural signal with a potential for adversely impacting important neural processing mechanisms. Here we propose that feedforward inhibition solves the latter instability problem of the excitation-inhibition microcircuit. Using computer simulations, we show that the feedforward inhibitory signal reduces the dependence of both the frequency of population oscillation and the level of selection on the magnitude of the input excitation. Such a mechanism can produce stable gamma oscillations with its frequency determined only by the properties of the feedforward network, as observed in the hippocampus. As feedforward and feedback inhibition motifs commonly appear together in the brain, we hypothesize that their interaction underlies a robust implementation of general computational principles of neural processing involved in several cognitive tasks, including the formation of cell assemblies and the routing of information between brain areas.