Distinct Functions of the Primate Putamen Direct and Indirect Pathways in Adaptive Outcome-Based Action Selection

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 receptormediated
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
Frontiers in Neuroanatomy | www.frontiersin.org 1 August 2017 | Volume 11 | Article 66
Ueda et al. D1, D2 Receptor Blockage
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

書誌情報

Frontiers in neuroanatomy

号 11, p. 66, 発行日 2017-08

PubMed番号

識別子タイプ

PMID

Versions

Ver.1

2023-05-15 23:24:26.261614

Show All versions

Cite as

エクスポート

OAI-PMH

JPCOAR 2.0
JPCOAR 1.0
DublinCore
DDI

Other Formats

JSON
BIBTEX

インデックスリンク

インデックスツリー

アイテム