Abstract:

Animals must execute appropriate actions for survival. In the brain, the striatum is a critical center for movement and learning and striatal activity correlates with vigor and kinematics of overt movements. However, the exact details of striatum control are less clear. A classical view has been that the striatum controls when and how vigorously to move through two opponent pathways. Specifically, the two populations of spiny projection neurons (D1-SPNs heading the striato-nigral pathway and D2-SPNs heading the striato-pallidal pathway) are thought to have opposing effects on movement. Other work indicates D1- and D2-SPNs may control specific actions in concert. Here, we performed 2-photon imaging and stimulation in the dorsolateral striatum as mice performed two forelimb actions in a self-paced manner, consisting of a push or pull isometric force on an immobile joystick.  Both D1- and D2-SPNs populations equally predicted the preparation and execution of specific actions, irrespective of what action was reinforced. Further, we developed a closed-loop system to model and manipulate action-specific neural ensembles using holographic optogenetics through a GRIN lens. Stimulation of action-specific ensembles of both D1- and D2-SPNs increased the force of action, but only for their congruent action. These results show that D1- and D2-SPNs can control specific ongoing actions concurrently, with specific ensembles controlling actions as granular as forces exerted by the same body part.