Decomposed frontal corticostriatal ensemble activity changes across trials, revealing distinct features relevant to outcome-based decision making

The frontal cortex-striatum circuit plays a pivotal role in adaptive goal-directed behaviours. However, the mediation of decision-related signals through cross-regional transmission between the medial frontal cortex and the striatum by neuronal ensembles remains unclear. We analysed neuronal ensemble activity obtained through simultaneous multiunit recordings in the secondary motor cortex (M2) and dorsal striatum (DS) while the rats performed an outcome-based choice task. Tensor component analysis (TCA), an unsupervised dimensionality reduction approach at the single-trial level, was adopted for concatenated ensembles of M2 and DS neurons. We identified distinct three spatiotemporal neural dynamics (TCA components) at the single-trial level specific to task-relevant variables. Choice-position selective neural dynamics was correlated with the trial-to-trial fluctuation of behavioural variables. This analytical approach unveiled choice-pattern selective neural dynamics distinguishing whether the incoming choice was a repetition or switch from the previous choice. Other neural dynamics was selective to outcome. Choice-pattern selective within-trial activity increased before response choice, whereas outcome selective within-trial activity increased following response. These results suggest that the concatenated ensembles of M2 and DS process distinct features of decision-related signals at various points in time. The M2 and DS may collaboratively monitor action outcomes and determine the subsequent choice, whether to repeat or switch, for coordinated action selection.