Behavioral Context Shapes Sensory Responses in Vibrissal Motor Cortex

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Abstract

Understanding how motor cortical circuits flexibly transform sensory and contextual information into behavior remains a central challenge. Whether neurons in primary vibrissal motor cortex (M1) multiplex across behaviors or are selectively engaged in context-specific actions is still unclear. To address this question, we trained mice on multiple vibrissal sensorimotor tasks, including a cue-triggered whisking-to-touch task and an air-puff–triggered licking task. Fast-spiking and regular-spiking neurons in layers 2/3 and 5 in vM1 responded robustly within ∼15 ms to air-puff stimulation. In contrast, these same neurons were only weakly modulated during goal-directed whisking-to-touch behavior. Unexpected air-puffs evoked responses in fewer neurons than expected stimuli. Trials in which stimulation elicited whisker movements produced smaller neural responses than trials without whisking. Stimulus-evoked activity in M1 was organized along a spectrum of response profiles with neurons exhibiting varying responses dynamics that cut across laminar and physiological distinctions. This organization of responses is consistent with context-dependent recruitment of M1 neurons. Together, these findings indicate that M1 activity is more closely associated with the selection of specific behavioral responses than with generalized sensory-motor encoding.

Significance

How motor cortex links sensory input to behavior remains a central question in neuroscience. Do neurons that respond to vibrissal stimuli also participate in whisker-based behaviors, or do they reflect distinct functional states? Here, we show that activity in vM1 is context dependent. Across multiple behaviors, sensory inputs recruit different neuronal populations depending on behavioral context: air-puff stimuli evoke rapid and robust responses, whereas the same neurons are only weakly engaged during goal-directed whisking-to-touch. In addition, expected and unexpected stimuli activate partially distinct ensembles, and sensory responses are attenuated when stimuli directly trigger movement. These findings indicate that M1 does not uniformly encode sensory input; instead, activity reflects context-dependent action selection where neuronal populations are engaged according to behavioral demands.

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