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Midbrain dopamine neurons encode decisions for future action

Abstract

Current models of the basal ganglia and dopamine neurons emphasize their role in reinforcement learning. However, the role of dopamine neurons in decision making is still unclear. We recorded from dopamine neurons in monkeys engaged in two types of trial: reference trials in an instructed-choice task and decision trials in a two-armed bandit decision task. We show that the activity of dopamine neurons in the decision setting is modulated according to the value of the upcoming action. Moreover, analysis of the probability matching strategy in the decision trials revealed that the dopamine population activity and not the reward during reference trials determines choice behavior. Because dopamine neurons do not have spatial or motor properties, we conclude that immediate decisions are likely to be generated elsewhere and conveyed to the dopamine neurons, which play a role in shaping long-term decision policy through dynamic modulation of the efficacy of basal ganglia synapses.

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Figure 1: Behavioral tasks and response parameters.
Figure 2: Contribution to probability matching behavior.
Figure 3: Eye positions in reference and decision trials.
Figure 4: Dopamine neurons code the TD error of action value.
Figure 5: Time course of the responses of dopamine neurons in the reference and decision tasks.

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Acknowledgements

We thank Y. Prut, Y. Engel, Y. Ritov, N. Daw, Y. Niv and R. Paz for fruitful discussions and comments on earlier versions of this manuscript; and G. Goelman and V. Sharkansky for technical assistance. This study was partly supported by a Center of Excellence grant administered by the Israel Science Foundation (ISF) and by a 'Fighting against Parkinson' grant administered by the Netherlands Friends of the Hebrew University (HUNA). G.M. was supported by a Horowitz fellowship.

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Correspondence to Genela Morris.

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Supplementary information

Supplementary Fig. 1

Choice triggered averaging (CTA) functions in decision trials. (PDF 321 kb)

Supplementary Fig. 2

Conditioning stimulus responses according to choice value. (PDF 168 kb)

Supplementary Note (PDF 196 kb)

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Morris, G., Nevet, A., Arkadir, D. et al. Midbrain dopamine neurons encode decisions for future action. Nat Neurosci 9, 1057–1063 (2006). https://doi.org/10.1038/nn1743

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