Comprehensive characterization of oscillatory signatures in a model circuit with PV- and SOM-expressing interneurons

Abstract

Neural circuits contain a wide variety of interneuron types, which differ in their biophysical properties and connectivity patterns. The two most common interneuron types, parvalbumin-expressing and somatostatin-expressing cells, have been shown to be differentially involved in many cognitive functions. These cell types also show different relationships with the power and phase of oscillations in local field potentials. The mechanisms that underlie the emergence of different oscillatory rhythms in neural circuits with more than one interneuron subtype, and the roles specific interneurons play in those mechanisms, are not fully understood. Here, we present a comprehensive analysis of all possible circuit motifs and input regimes that can be achieved in circuits comprised of excitatory cells, PV-like fast-spiking interneurons and SOM-like low-threshold spiking interneurons. We identify 18 unique motifs and simulate their dynamics over a range of input strengths. Using several characteristics, such as oscillation frequency, firing rates, phase of firing and burst fraction, we cluster the resulting circuit dynamics across motifs in order to identify patterns of activity and compare these patterns to behaviors that were generated in circuits with one interneuron type. In addition to the well-known PING and ING gamma oscillations and an asynchronous state, our analysis identified three oscillatory behaviors that were generated by the three-cell-type motifs only: theta-nested gamma oscillations, stable beta oscillations and theta-locked bursting behavior, which have also been observed in experiments. Our characterization provides a map to interpret experimental activity patterns and suggests pharmacological manipulations or optogenetics approaches to validate these conclusions.