Opponent and bidirectional control of movement velocity in the basal ganglia

Activity in the direct and indirect basal ganglia pathways can bidirectionally control the speed of movements that underlie reward-seeking actions in mice without affecting motivation. Selection and modification of reward-seeking actions Activity in the direct and indirect basal ganglia pathways, respectively, promotes actions associated with reward and suppresses actions that do not lead to reward. Eric Yttri and Joshua Dudman now show that in addition to their role in selecting the action that will lead to reward, these pathways are also involved in the modification of the velocity of movements required to obtain the reward. Through optogenetic stimulation of the direct or indirect pathway during voluntary movement, the authors show that each pathway can produce both a learned increase and a learned decrease in the speed of specific movements, without affecting motivation, and in a dopamine-dependent manner. These findings demonstrate that each pathway can reinforce the speed of movements that underlie reward-seeking actions. For goal-directed behaviour it is critical that we can both select the appropriate action and learn to modify the underlying movements (for example, the pitch of a note or velocity of a reach) to improve outcomes. The basal ganglia are a critical nexus where circuits necessary for the production of behaviour, such as the neocortex and thalamus, are integrated with reward signalling 1 to reinforce successful, purposive actions 2 . The dorsal striatum, a major input structure of basal ganglia, is composed of two opponent pathways, direct and indirect, thought to select actions that elicit positive outcomes and suppress actions that do not, respectively 3 , 4 . Activity-dependent plasticity modulated by reward is thought to be sufficient for selecting actions in the striatum 5 , 6 . Although perturbations of basal ganglia function produce profound changes in movement 7 , it remains unknown whether activity-dependent plasticity is sufficient to produce learned changes in movement kinematics, such as velocity. Here we use cell-type-specific stimulation in mice delivered in closed loop during movement to demonstrate that activity in either the direct or indirect pathway is sufficient to produce specific and sustained increases or decreases in velocity, without affecting action selection or motivation. These behavioural changes were a form of learning that accumulated over trials, persisted after the cessation of stimulation, and were abol