Correlated signatures of social behavior in cerebellum and anterior cingulate cortex

Abstract

The cerebellum has been implicated in the regulation of social behavior. Its influence is thought to arise from communication, via the thalamus, to forebrain regions integral in the expression of social interactions, including the anterior cingulate cortex (ACC). However, the signals encoded or the nature of the communication between the cerebellum and these brain regions remains poorly understood. Here, we describe an approach that overcomes technical challenges in exploring the coordination of distant brain regions at high temporal and spatial resolution during social behavior. We developed the E-Scope, an electrophysiology-integrated miniature microscope, to synchronously measure extracellular electrical activity in the cerebellum along with calcium imaging of the ACC. This single coaxial cable device combined these data streams to provide a powerful tool to monitor the activity of distant brain regions in freely behaving animals. During social behavior, we recorded the spike timing of multiple single units in cerebellar right Crus I (RCrus I) Purkinje cells (PCs) or dentate nucleus (DN) neurons while synchronously imaging calcium transients in contralateral ACC neurons. We find that during social interactions, a significant subpopulation of cerebellar PCs were robustly inhibited, while most modulated neurons in the DN were activated. As expected, we find that there are higher correlations in the activity of cerebellar and ACC neurons that are similarly excited or inhibited by social interaction than in the activity of those modulated in an opposing manner. Surprisingly, these distinctions in correlations largely disappear when only non-social bouts were analyzed, suggesting that cerebellar-cortical interactions were social behavior specific. Our work provides new insights into the complexity of cerebellar activation and co-modulation of the ACC during social behavior, and a valuable open-source tool for simultaneous, multimodal recordings in freely behaving mice.