Thalamic input to motor cortex facilitates goal-directed action initiation

Prompt execution of planned motor action is essential for survival. The interactions between frontal cortical circuits and the basal ganglia are central to goal-oriented action selection and initiation.1–4 In rodents, the ventromedial thalamic nucleus (VM) is one of the critical nodes that conveys the output of the basal ganglia to the frontal cortical areas including the anterior lateral motor cortex (ALM).5–9 Recent studies showed the critical role of ALM and its interplay with the motor thalamus in preparing sensory-cued rewarded movements, specifically licking.10–12 Work in primates suggests that the basal ganglia output to the motor thalamus transmits an urgency or vigor signal,13–15 which leads to shortened reaction times and faster movement initiation. As yet, little is known about what signals are transmitted from the motor thalamus to the cortex during cued movements and how these signals contribute to movement initiation. In the present study, we employed a tactile-cued licking task in mice while monitoring reaction times of the initial lick. We found that inactivation of ALM delayed the initiation of cued licking. Two-photon Ca2+ imaging of VM axons revealed that the majority of the axon terminals in ALM were transiently active during licking. Their activity was predictive of the time of the first lick. Chemogenetic and optogenetic manipulation of VM axons in ALM indicated that VM inputs facilitate the initiation of cue-triggered and impulsive licking in trained mice. Our results suggest that VM thalamocortical inputs increase the probability and vigor of initiating planned motor responses. [Display omitted] •Ventromedial (VM) thalamus targets layer 1 of anterior lateral motor cortex (ALM)•VM axons in ALM are transiently active during initiation of cued licking•Inactivation of VM axons delays initiation of cued licking•Activation of VM axons shortens reaction time and increases impulsive licks The ventromedial thalamus (VM) is a critical node mediating the basal ganglia-cortical interaction. In mice trained in a tactile-cued licking task, Takahashi et al. find a transient activation of VM axons in the premotor cortex preceding lick initiation. VM inputs modulate cortical activity and increase the probability and vigor of licking.