Dynamic adaptation of sequential action benefits from cortico-basal ganglia-related temporal variability

Performing several actions in swift succession is often necessary to exploit known contingencies in the environment. However, in order to remain successful when contingency rules change, streamlined action sequences must be adaptable. Here, by combining analyses of behavioural microstructure with circuit-specific manipulation in mice, we report on a relationship between action timing variability and successful adaptation that relies on post-synaptic targets of primary motor cortical (M1) projections to dorsolateral striatum (DLS). Using a two-lever instrumental task, we found that mice build successful action sequences by first establishing action scaffolds, from which they dynamically elongate as task requirements extend. Specific interruption of the M1→DLS circuit altered these dynamics, prompting actions that were less variable in their timing, overall reducing opportunities for success. Our results reveal a role for M1→DLS circuitry in setting the exploration/exploitation balance that is required for adaptively guiding the timing and success of instrumental action. Based on evidence from transsynaptic tracing experiments, we propose that such function may involve additional downstream subcortical processing relating to collateralisation of descending motor pathways to multiple basal ganglia centres.