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Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value

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Abstract

In changing environments, animals must adaptively select actions to achieve their goals. In tasks involving goal-directed action selection, striatal neural activity has been shown to represent the value of competing actions. Striatal representations of action value could potentially bias responses toward actions of higher value. However, no study to date has demonstrated the direct effect of distinct striatal pathways in goal-directed action selection. We found that transient optogenetic stimulation of dorsal striatal dopamine D1 and D2 receptor–expressing neurons during decision-making in mice introduced opposing biases in the distribution of choices. The effect of stimulation on choice was dependent on recent reward history and mimicked an additive change in the action value. Although stimulation before and during movement initiation produced a robust bias in choice behavior, this bias was substantially diminished when stimulation was delayed after response initiation. Together, our data suggest that striatal activity is involved in goal-directed action selection.

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Figure 1: Design of the probabilistic switching task and mouse performance.
Figure 2: Modeling action value and choice.
Figure 3: Optical stimulation induces opposing biases in a mouse's choice.
Figure 4: Dorsal striatal D1R-expressing neuron activation mimics an increase in relative action value for contralateral choice.
Figure 5: Dorsal striatal D2R-expressing neuron activation mimics a decrease in relative action value for contralateral choice.
Figure 6: Comparison of D1R- and D2R-expressing neuron stimulation.
Figure 7: Significant bias was induced by stimulation limited to a 50-ms period before a Go cue.
Figure 8: Bias induced by stimulation diminished when stimulation was delayed 150 ms after a Go cue.

Change history

  • 30 August 2012

    In the version of this article initially published, a reference was not included in Online Methods for the BAC transgenic mice expressing Cre recombinase. The reference is Gong, S. et al. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 27, 9817–9823 (2007). The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank G. Stuber, F. Ambroggi, D. Niell, K. Berger, C. Wu and H. Peckler for assistance with experiments, V. Kharazia for immunostaining and histological quantification, K. Deisseroth (Stanford University) for advice and reagents, and C. Niell for comments on the manuscript. This work was supported by the State of California, the US National Institutes of Health (1RC2NS069350; R01MH087542 and R01DA029150), and the P. Royer and K. Clayton Family.

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L.-H.T., A.M.L. and L.W. designed the study. L.-H.T., A.M.L. and N.B. collected behavioral data. L.-H.T. and A.M.L. analyzed and modeled data. A.M.L. and N.B. processed tissue. L.-H.T., A.M.L., L.W. and A.B. wrote the paper.

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Correspondence to Linda Wilbrecht.

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The authors declare no competing financial interests.

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Tai, LH., Lee, A., Benavidez, N. et al. Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value. Nat Neurosci 15, 1281–1289 (2012). https://doi.org/10.1038/nn.3188

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