Abstract
Mammalian cerebral cortex is accepted as being critical for voluntary motor control, but what functions depend on cortex is still unclear. Here we used rapid, reversible optogenetic inhibition to test the role of cortex during a head-fixed task in which mice reach, grab, and eat a food pellet. Sudden cortical inhibition blocked initiation or froze execution of this skilled prehension behavior, but left untrained forelimb movements unaffected. Unexpectedly, kinematically normal prehension occurred immediately after cortical inhibition, even during rest periods lacking cue and pellet. This 'rebound' prehension was only evoked in trained and food-deprived animals, suggesting that a motivation-gated motor engram sufficient to evoke prehension is activated at inhibition's end. These results demonstrate the necessity and sufficiency of cortical activity for enacting a learned skill.
Highlights
Execution of complex voluntary movements depends on many functions including choosing a behavior, specifying each step, enacting the movements, and learning to perform with increasing skill
Motor control is achieved by the coordinated activity of myriad neural structures, including the cerebral cortex, basal ganglia, cerebellum, and spinal cord
To test the role of the cortex for control of skilled motor tasks, we developed a multi-step, cued, prehension task in which head-fixed mice reach for a food pellet, grab it, and bring the pellet to the mouth for consumption (Figure 1A, Video 1). This prehension behavior was broken down into six sequential epochs (Lift, Hand open, Grab, Supinate, At mouth, and Chew; Figure 1B and C) that divide the complex movement into components that involve distinct muscle activations
Summary
Execution of complex voluntary movements depends on many functions including choosing a behavior, specifying each step, enacting the movements, and learning to perform with increasing skill. Motor control is achieved by the coordinated activity of myriad neural structures, including the cerebral cortex, basal ganglia, cerebellum, and spinal cord. Neurophysiological recordings, inactivation experiments, and stimulation studies have been used to describe the role of cortex in motor control. Cortical neurons display dynamic activity patterns during movement planning and execution, but their functional contribution to skilled action cannot be assessed from recordings alone (Lemon, 1993; Scott, 2003; Evarts, 2011). We inhibited cortex with an optogenetic method that minimizes compensation, and selective stimulation of cortical neurons was achieved by the cessation of inhibition
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