Somatostatin-excitatory coordination emerges with dexterous motor skill learning

Abstract

Motor skill-learning increases spatio-temporal consistency in neuronal activity in primary motor cortex (M1), and Somatostatin-expressing (SST) interneurons are causally involved in these learning-related activity changes. Yet, how SST-excitatory interactions shape population level activity changes during motor skill acquisition is still unknown. Here, we imaged large populations of excitatory neurons and identified SST or parvalbumin-expressing (PV) interneurons across successive days as mice learned a dexterous, persistently M1-dependent reach-to-grasp task. Sparse, temporally coordinated, trial-resolved, and rate-controlled functional interactions between SST neurons and skill-modulated excitatory neurons emerged with learning and were stronger than those in excitatory-excitatory or PV-excitatory pairs. Interactions strengthened as neurons were recruited to the skill-modulated ensemble and weakened when skill modulation was lost. SST activity also became temporally reliable earlier than excitatory or PV activity, and SST consistency was significantly associated with behavioral performance even after controlling for training session number. Additionally, SST neurons carried more information about movement kinematics than randomly selected subsets of excitatory neurons. Overall, SST neurons became selectively coordinated with behaviorally relevant excitatory populations, revealing a cell-type-specific functional architecture for dexterous motor learning.