Distinct sensorimotor encoding in tuft dendrites and somata associated with action, correction, and learning

Frontal cortex plays critical roles in action control and motor skill learning. Within the layer 1 apical tuft dendrites of layer 5 (L5) neurons in the frontal cortex, precise input patterns and back-propagating action potentials can trigger powerful regenerative events that may be essential for flexible computation and learning. However, it remains unclear whether tuft activity in frontal cortical L5 circuits encodes sensorimotor information that differs from the information conveyed by their outputs to downstream targets. Using longitudinal two-photon calcium imaging, we investigated sensorimotor encoding in the apical tuft dendrites and somata of L5 extratelencephalic neurons in the frontal cortex of mice during learning of a discrete change to a cued dexterous action. During learning, movement errors either triggered corrective action or did not, allowing us to dissociate error signals from signals selective for corrective action. Somatic activity tracked both instructional cues and action, whereas tuft activity predominantly tracked instructional cues. Movement errors during learning revealed additional distinct tuft activity that was selectively associated with corrective actions. Furthermore, learning induced divergent changes in the response gain and net selectivity of tuft dendrites compared to somata. Our measurements uncover systematic differences between the tuft dendrites and somata in sensorimotor selectivity, sensitivity to corrective action, and functional plasticity, providing a foundation for investigating the contributions of dendritic computation to motor skill learning.