Primary motor cortex drives expressive facial movements related to reward processing in mice

Animals exhibit expressive facial movements in a wide range of behavioral contexts. However, the underlying neural mechanisms remain enigmatic. In reward-based learning tasks, mice make expressive movements with their whiskers and nose at the timings of reward expectation and acquisition. Here we show that optogenetic stimulation of midbrain dopamine neurons (oDAS) as a reward is sufficient to induce such expressive movements. Pavlovian conditioning with a sensory cue and oDAS elicited both cue-locked (reward-expecting) and oDAS-aligned (reward-acquiring) orofacial movements. Inhibition or knock-out of dopamine D1 receptors in the nucleus accumbens inhibited oDAS-induced motion but spared cue-locked motion. Silencing the whisker primary motor cortex (wM1) abolished both oDAS-induced and cue-locked orofacial movements. We found specific neuronal populations in wM1 representing either oDAS-aligned or cue-locked whisker movements. Thus, reward-acquiring and reward-expecting facial movements are driven by accumbal D1 receptor-dependent and -independent neuronal mechanisms, respectively, both dominantly regulated by wM1 activity.