Shunting Inhibition Improves Synchronization in Heterogeneous Inhibitory Interneuronal Networks with Type 1 Excitability Whereas Hyperpolarizing Inhibition Is Better for Type 2 Excitability

Abstract

All-to-all homogeneous networks of inhibitory neurons synchronize completely under the right conditions; however, many modeling studies have shown that biological levels of heterogeneity disrupt synchrony. Our fundamental scientific question is “how can neurons maintain partial synchrony in the presence of heterogeneity and noise?” A particular subset of strongly interconnected interneurons, the PV+ fast-spiking (FS) basket neurons, are strongly implicated in γ oscillations and in phase locking of nested γ oscillations to theta. Their excitability type apparently varies between brain regions: in CA1 and the dentate gyrus they have type 1 excitability, meaning that they can fire arbitrarily slowly, whereas in the striatum and cortex they have type 2 excitability, meaning that there is a frequency thresh old below which they cannot sustain repetitive firing. We constrained the models to study the effect of excitability type (more precisely bifurcation type) in isolation from all other factors. We use sparsely connected, heterogeneous, noisy networks with synaptic delays to show that synchronization properties, namely the resistance to suppression and the strength of theta phase to γ amplitude coupling, are strongly dependent on the pairing of excitability type with the type of inhibition. Shunting inhibition performs better for type 1 and hyperpolarizing inhibition for type 2. γ Oscillations and their nesting within theta oscillations are thought to subserve cognitive functions like memory encoding and recall; therefore, it is important to understand the contribution of intrinsic properties to these rhythms.