Abstract
Skillful control of movement is central to our ability to sense and manipulate the world. Dexterous acts depend on cerebral cortex[1⇓⇓⇓⇓⇓⇓⇓⇓-10], and the activity of cortical neurons is correlated with movement[11⇓⇓⇓-15]. By isolating the neural dynamics that command skilled movements from those that reflect other processes (such as planning and deciding to move), we were able to characterize and manipulate the motor commands underlying prehension. We showed that in mice trained to perform a reach / grab / supination / bring-to-mouth sequence (volitional prehension), multiple forms of optogenetic stimuli in sensorimotor cortex resulted in an involuntary, complete movement (opto-prehension). This result suggested that the trained brain could robustly transform a variety of aberrant stimuli into the dynamics sufficient for prehension. We measured the electrical activity of cortical populations and detailed limb kinematics during volitional prehension and optoprehension. During volitional prehension, neurons fired before and during specific stages of the movement, and the population collectively tiled the entire behavioral sequence. During opto-prehension, most neurons recapitulated their volitional prehension activity patterns, but a physiologically distinct subset did not. On trials where the liminal optogenetic stimulus failed to produce these dynamics, movement did not occur, providing further evidence that a specific pattern of neural activity was causally coupled to prehension. Having identified these dynamics, we next tested their robustness to brief, closed-loop perturbation. Regardless of where along the reach we optogenetically halted cortical activity and the movement, relief of suppression resulted in cortical dynamics that immediately recapitulated all steps of the prehension program, and the animal completed the behavior. By combining electrophysiology and optogenetic perturbations, we have identified and characterized the cortical motor program driving a learned, dexterous movement sequence.
