Abstract

Dopaminergic (DA) neurons in the midbrain provide rich topographic innervation of the striatum and are central to learning and to generating actions. Despite the importance of this DA innervation, it remains unclear whether and how DA neurons are specialized on the basis of the location of their striatal target. Thus, we sought to compare the function of subpopulations of DA neurons that target distinct striatal subregions in the context of an instrumental reversal learning task. We identified key differences in the encoding of reward and choice in dopamine terminals in dorsal versus ventral striatum: DA terminals in ventral striatum responded more strongly to reward consumption and reward-predicting cues, whereas DA terminals in dorsomedial striatum responded more strongly to contralateral choices. In both cases the terminals encoded a reward prediction error. Our results suggest that the DA modulation of the striatum is spatially organized to support the specialized function of the targeted subregion.

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Acknowledgements

We thank C. Gregory, M. Applegate and J. Finkelstein for assistance in data collection; J. Pillow and A. Conway for advice with data analysis; M. Murugan and B. Engelhard for comments on the manuscript; and D. Tindall and P. Wallace for administrative support. I.B.W. was supported by the Pew, McKnight, NARSAD and Sloan Foundations, NIH DP2 New Innovator Award and an R01 MH106689-02; N.F.P was supported by an NSF Graduate Research Fellowship; and J.P.T. and I.B.W. were supported by the Essig and Enright '82 Fund.

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Affiliations

  1. Princeton Neuroscience Institute and Department of Psychology, Princeton University, Princeton, New Jersey, USA.

    • Nathan F Parker
    • , Courtney M Cameron
    • , Joshua P Taliaferro
    • , Junuk Lee
    • , Jung Yoon Choi
    • , Nathaniel D Daw
    •  & Ilana B Witten
  2. Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, California, USA.

    • Thomas J Davidson

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Contributions

N.F.P., C.M.C., J.P.T. and J.L. performed the experiments; N.F.P., C.M.C., J.P.T., J.L. and J.Y.C. analyzed the data; T.J.D. provided advice on rig design; N.D.D. and I.B.W. provided advice on statistical analysis; N.F.P., N.D.D. and I.B.W. designed experiments and interpreted the results; and N.F.P. and I.B.W. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ilana B Witten.

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DOI

https://doi.org/10.1038/nn.4287

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