Striatal neurons are recruited dynamically into collective representations of self-initiated and learned actions in freely-moving mice

Abstract

Striatal spiny projection neurons are hyperpolarized-at-rest (HaR) and are driven to spike threshold by a small number of powerful inputs - an input-output configuration that is detrimental to response reliability. Because the striatum is important for habitual behaviors and goal-directed learning, we conducted microendoscopic imaging in freely-moving mice that express a genetically-encoded calcium indicator sparsely in striatal HaR neurons to compare their response reliability during self-initiated movements and operant conditioning. The sparse expression was critical for longitudinal studies of response reliability, and for studying correlations among HaR neurons while minimizing spurious correlations arising from contamination by the background neuropil signal. We found that HaR neurons are recruited dynamically into action representation through a moment-by-moment formation of distinct cell assemblies. While individual neurons respond with little reliability, the population response remained reliable. Moreover, we found evidence for the formation of correlated cell assemblies during conditioned (but not innate) behaviors, but this correlation was independent of the distance between neurons.