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Basal Ganglia Opponent and Bidirectional Control of Movement Velocity
Nature volume 533, pages 402–406 (19 May 2016) Opponent and bidirectional control of movement velocity in the basal ganglia Eric A. Yttri & Joshua T. Dudman Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA [paraphrase] 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 to reinforce successful, purposive actions. 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. Activity-dependent plasticity modulated by reward is thought to be sufficient for selecting actions in the striatum. Although perturbations of basal ganglia function produce profound changes in movement, 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 abolished in the presence of dopamine antagonists. Our results reveal that the direct and indirect pathways can each bidirectionally control movement velocity, demonstrating unprecedented specificity and flexibility in the control of volition by the basal ganglia. Purposive action requires selection of a goal (for example, go left) and execution parameters (for example, how fast to go). For example, in bird song selection of both discrete, sequential actions (syllables) as well as the pitch can be controlled by reinforcement in cortico-basal ganglia pathways8. The striatum is a major input nucleus in basal ganglia and the direct and indirect pathway are primarily composed of two molecularly distinct populations of medium spiny projection neurons (MSNs): direct striatonigral (dMSN) and indirect striatopallidal (iMSN) neurons. Sustained activation of dMSNs increases movement, whereas sustained activation of iMSNs reduces movement. As a result, the balance of activity-dependent plasticity at cortical synapses onto dMSNs and iMSNs is thought to underlie the selection of successful goal-directed actions. While it is known that stimulation of direct pathway neurons can support self-stimulation and bias concomitant choice behaviour, there is little direct evidence that MSN activity is sufficient to produce persistent, specific changes in subsequent actions. Here we proposed a circuit implementation by which a continuous parameter defining a purposive movement can be selectively reinforced by a stimulation-dependent enhancement of bidirectional synaptic plasticity. Importantly, it has been shown that striatal neurons are capable of bidirectional synaptic plasticity; however, plasticity is mediated by distinct signalling events in the two populations. Resolving the roles played by the intersection of these different cellular and circuit factors that govern bidirectional plasticity will be critical to understand the role of dopamine in instrumental learning. In addition to kinematic parameters of movement, other aspects of reinforcement learning are governed by continuous parameters such as rates or value. The circuit implementation we propose could provide a general mechanism by which activity-dependent plasticity in striatum produces learned changes in continuous parameters with monotonic representations in neural activity. [end of paraphrase]
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