Optogenetic mapping of rhythmic phase-dependent excitability in the mouse striatum

The striatum is thought to switch flexibly between multiple converging inputs to support adaptive behavior. The "communication through coherence" (CTC) hypothesis is a potential mechanism to implement such a flexible switching. For CTC to work in the striatum, striatal excitability must show rhythmic fluctuations, such as those related to the phase of the striatal local field potential (LFP). To test this fundamental requirement, we delivered a constant input stimulus to ChR2-expressing striatal fast-spiking PV+ interneurons (FSIs) in head-fixed awake mice (PV-Cre:Ai-32, n = 18, 9 female), and determined whether the response to this stimulus varied with LFP phase. We found that approximately one-third (41.2%) of FSIs exhibited significant phase-dependent excitability in at least one LFP frequency band. Phase-dependent excitability was most prominent in the delta (2-5 Hz) frequency band, both in terms of prevalence (23.5% of FSIs sampled) and magnitude (phase modulation strength: 22% of average response). The most excitable phase tended to align with endogenous phase-locking, again most clearly in the delta band. These results bolster the functional relevance of the striatal field potential and spike-field relationships, and provide proof-of-principle support for the possibility of CTC in the striatum. Significance StatementThe striatum is thought to switch dynamically between multiple converging inputs. A leading idea for how this is accomplished is through communication through coherence (CTC). A fundamental, but previously untested, requirement for CTC to work is that striatum must show changes in excitability that depend on local field potential phase. We find that about one-third of striatal neurons show phase-dependent excitability, providing proof of principle for CTC-like switching in striatum.