Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks

Oscillatory activity in the gamma frequency range (30–90 Hz) is a hallmark of the function of the hippocampal network. These oscillations are thought to be important for information processing.Gamma oscillations can be replicated in in vitro models, in which the underlying mechanisms can be analysed systematically.In all in vitro models, gamma oscillations are dependent on GABAA (γ-aminobutyric acid type A)-receptor-mediated inhibition, suggesting that these oscillations are primarily generated by networks of inhibitory interneurons.Fast-spiking, parvalbumin-expressing basket cells are key components of the hippocampal interneuron network. They are extensively interconnected and fire action potentials that are phase-locked to the oscillations.Interneuron network models that are based on mutual inhibition, assuming slow, weak and hyperpolarizing synapses, generate synchronized gamma activity if exposed to a tonic excitatory drive. However, these models are highly sensitive to heterogeneity in the drive.Experimental analysis has revealed that basket cell–basket cell synapses are functionally specialized. They mediate fast, strong and shunting inhibition.Realistic interneuron network models generate synchronized gamma activity with increased robustness against heterogeneity in the tonic excitatory drive.Experimental analysis further reveals that basket cells are rapidly excited through gap junctions and fast glutamatergic synapses.Both gap junctions and fast glutamatergic synapses stabilize gamma activity in interneuron networks.Specialized synaptic properties turn the interneuron network into a robust gamma frequency oscillator. Therefore, interneuron networks might provide a precise reference signal for temporal encoding of information in principal neurons.