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Parsing dopamine's learning and motor functions

Periodic Reporting for period 1 - RegionalDopamine (Parsing dopamine's learning and motor functions)

Reporting period: 2023-01-01 to 2024-12-31

Appropriate selection of situation-appropriate behavior in our everyday life requires both learning and motor control. A key neuromodulator involved in these processes is dopamine, particularly in the basal ganglia. Here, dopamine is thought to reflect the difference between an expected and obtained outcome, also referred to as a reward-prediction error signal. On the other hand, dopamine is vital for movement, making it difficult to disentangle its role in learning and from its role in action control. The overlap is especially apparent in disorders such as Parkinson’s disease, which is characterized by the degeneration of dopaminergic neurons. People with Parkinson’s disease often exhibit difficulty initiating or suppressing movements and learning through rewards.

Our project investigates how dopamine in the ventromedial striatum (VMS) contributes to both reward processing and movement. The goal is to clarify how dopamine supports behavior, by identifying whether its signals are driven by the reward itself or by the actions taken to obtain it or both.
We successfully implanted microelectrodes into the VMS and chronically measured dopamine release during behavior over a period of several months. We replicate previous findings by others showing that dopamine release is elevated when subjects had to engage in action initiation but not the suppression or continuation of the same action.

By innovating design and complexity of such behavioral experiments, we show that dopamine signals in VMS are involved in both the anticipation of future rewards and movement. This increase in dopamine release is primarily driven by the movement towards the reward location. On the other hand, delivery of the reward itself nor the temporal proximity of reward delivery (i.e. how soon the reward is expected) did not affect the dopamine signal.

Together, our data suggests that VMS dopamine not only promotes the execution of actions, but continuously estimates spatial, but not temporal, distance to rewards. Importantly, after satisfying response requirements for rewards, the VMS dopamine signal appears to predominantly encode reward approach. Our findings have implications for understanding the role of dopamine in motivation and goal-directed action, and disorders where these processes may be disrupted.
Our project delivers a novel understanding of how dopamine is involved in learning and movement, particularly its role in motivated behavior and goal-directed action. Previous research has established that dopamine is involved in reward learning and motor control. However, our findings go beyond that and demonstrate that VMS dopamine release is primarily driven by movement toward a reward, rather than by the reward itself or its timing.

The present work facilitates our understanding of dopamine's role in encoding reward prediction errors by showing the importance of behavioral context—specifically, movement toward a reward, and not just reward outcome.
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