Basal Ganglia Dynamics During Spontaneous Behavior

Abstract

Animal behavior is composed of modular actions that are concatenated into sequences by the brain. The dorsolateral striatum (DLS), an integral component of the input nucleus to the basal ganglia, has been implicated in action selection and reinforcement. However, the specific striatal mechanisms underlying the expression and reinforcement of these actions, particularly during spontaneous, self-motivated behavior, remain unknown. By recording both bulk and cellular neural activity from the predominant cell types in the DLS, the direct and indirect pathway spiny projection neurons (SPNs), as mice spontaneously express action sequences, we discovered a systematic encoding of sub-second actions based on their identity and ordering. Notably, similar actions share overlapping neural populations whereas dissimilar actions show minimal neural overlap. The combined dynamics of the direct and indirect pathway SPNs offer superior decoding of moment-to-moment actions than either cell type individually. In a complementary set of experiments, we show that dopamine systematically fluctuates within the DLS as mice express action sequences. Photometric recordings and calibrated closed-loop optogenetic manipulations demonstrate that dopamine modulates the direct and indirect pathways to reinforce specific actions over minutes, increase sequence variability over seconds, and modulate the vigor with which actions are expressed without influencing moment-to-moment kinematics. Interestingly, both endogenous and optogenetically evoked dopamine release appears to reinforce spontaneously expressed actions, with the magnitude of reinforcement varying among individual mice. Notably, the effects of endogenous and evoked dopamine release are correlated across mice, suggesting differential sensitivity to dopamine dynamics among individuals. In summary, we identify a role for the DLS in systematically encoding actions and sequences and discover a role for dopamine in sculpting spontaneously expressed behavior via its interaction with SPNs in the DLS.