Cell type-specific dynamics of prefrontal gamma synchrony during flexible behavior

Abstract

The prefrontal cortex (PFC) is required for many cognitive processes that are disrupted in conditions such as schizophrenia. The PFC is composed of neuronal networks which are organized by both local microcircuitry and inter-regional projections, within which precisely tuned neuronal activity generates appropriate cognitive responses. Parvalbumin-positive interneurons (PVI) play an integral role by synchronizing select networks to oscillations in the gamma frequency range (~30-100 Hz). Synchronized gamma oscillations seem to facilitate information transfer between neurons and across regions. In particular, our lab has previously shown that PVI-generated gamma oscillations in the left and right prefrontal cortices become synchronized during cognitive tasks and this synchronization is necessary for animals to learn rule shifts. Here, we examine how this synchrony propagates through prefrontal circuits using novel genetically encoded voltage indicators (GEVIs) to examine gamma oscillations in specific populations of deep layer projection neurons targeting either the mediodorsal thalamus (PFC-MD) or dorsal striatum (PFC-DS). We first designed a novel analysis which found that PVI exhibit inter-hemispheric gamma synchrony immediately (within seconds) following trial outcomes, during a specific subset of trials associated with the adoption of a new behavioral strategy. PFC-MD neurons did not exhibit gamma synchrony during these outcome periods, but did synchronize during the pre-decision period of the next trial. Furthermore, pre-decision gamma synchrony in PFC-MD neurons was dependent on PVI and did not occur in PFC-DS neurons. Together, our findings suggest that gamma synchrony is transmitted from PVI to PFC-MD neurons during rule shifts in a task-phase and cell type-specific manner to facilitate the updating of behavioral strategies.