Abstract

Cortico-basal ganglia circuits are critical regulators of reward-based decision making. Reinforcement learning models posit that action reward value is encoded by the firing activity of striatal medium spiny neurons (MSNs) and updated upon changing reinforcement contingencies by dopamine (DA) signaling to these neurons. However, it remains unclear how the anatomically distinct direct and indirect pathways through the basal ganglia are involved in updating action reward value under changing contingencies. MSNs of the direct pathway predominantly express DA D1 receptors and those of the indirect pathway predominantly D2 receptors, so we tested for distinct functions in behavioral adaptation by injecting D1 and D2 receptor antagonists into the putamen of two macaque monkeys performing a free choice task for probabilistic reward. In this task, monkeys turned a handle toward either a left or right target depending on an asymmetrically assigned probability of large reward. Reward probabilities of left and right targets changed after 30–150 trials, so the monkeys were required to learn the higher-value target choice based on action–outcome history. In the control condition, the monkeys showed stable selection of the higher-value target (that more likely to yield large reward) and kept choosing the higher-value target regardless of less frequent small reward outcomes. The monkeys also made flexible changes of selection away from the high-value target when two or three small reward outcomes occurred randomly in succession. DA D1 antagonist injection significantly increased the probability of the monkey switching to the alternate target in response to successive small reward outcomes. Conversely, D2 antagonist injection significantly decreased the switching probability. These results suggest distinct functions of D1 and D2 receptor-mediated signaling processes in action selection based on action–outcome history, with D1 receptor-mediated signaling promoting the stable choice of higher-value targets and D2 receptor-mediated signaling promoting a switch in action away from small reward outcomes. Therefore, direct and indirect pathways appear to have complementary functions in maintaining optimal goal-directed action selection and updating action value, which are dependent on D1 and D2 DA receptor signaling.

Highlights

  • Humans and non-human animals adapt behavior based on previous experience, choosing actions followed by rewards and avoiding those followed by unfavorable outcomes

  • To assess possible contributions of the direct and indirect pathways to action selection based on action–outcome history, we examined the responses of monkeys during a rewardbased probabilistic learning paradigm (Samejima et al, 2005) under control conditions, D1 antagonist local infusion, and D2 antagonist local infusion into putamen

  • The large reward probability for the left target remained 50% while the large reward probability for the right target was changed to 90% (L50%–R90% condition), and the monkey quickly switched to the right target on most trials (Figure 1B)

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Summary

INTRODUCTION

Humans and non-human animals adapt behavior based on previous experience, choosing actions followed by rewards and avoiding those followed by unfavorable outcomes. To assess possible contributions of the direct and indirect pathways to action selection based on action–outcome history, we examined the responses of monkeys during a rewardbased probabilistic learning paradigm (Samejima et al, 2005) under control conditions, D1 antagonist local infusion, and D2 antagonist local infusion into putamen. In this task, two alternative choices, lever turn to a left or right target, were associated with predetermined probabilities of large and small reward. We found that D1 and D2 receptor-mediated signaling mechanisms regulate the balance between stable and flexible action selection to optimize reward

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