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A selective role for dopamine in stimulus–reward learning

Nature volume 469, pages 53–57 (2011)Cite this article

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Abstract

Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, becoming attractive and desirable incentive stimuli. However, whether a cue acts solely as a predictor of reward, or also serves as an incentive stimulus, differs between individuals. Thus, individuals vary in the degree to which cues bias choice and potentially promote maladaptive behaviour. Here we use rats that differ in the incentive motivational properties they attribute to food cues to probe the role of the neurotransmitter dopamine in stimulus–reward learning. We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors. Rather, dopamine acts selectively in a form of stimulus–reward learning in which incentive salience is assigned to reward cues. In individuals with a propensity for this form of learning, reward cues come to powerfully motivate and control behaviour. This work provides insight into the neurobiology of a form of stimulus–reward learning that confers increased susceptibility to disorders of impulse control.

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Figure 1: Development of sign-tracking versus goal-tracking CRs in bHR and bLR rats.
Figure 2: Phasic dopamine signalling in response to CS and US presentation during the acquisition of Pavlovian conditional approach behaviour in bHR and bLR rats.
Figure 3: Conditional responses and phasic dopamine signalling in response to CS and US presentation in outbred rats.
Figure 4: Dopamine is necessary for learning CS–US associations that lead to sign-tracking, but not goal-tracking.

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Acknowledgements

This work was supported by National Institutes of Health grants: R01-MH079292 (to P.E.M.P.), R01-DA027858 (to P.E.M.P.), T32-DA07278 (to J.J.C.), F32-DA24540 (to J.J.C.), R37-DA04294 ( to T.E.R.), and 5P01-DA021633-02 (to T.E.R. and H.A.). The selective breeding colony was supported by a grant from the Office of Naval Research to H.A. (N00014-02-1-0879). We thank K. Berridge and J. Morrow for comments on earlier versions of the manuscript, and S. Ng-Evans for technical support.

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Author notes

  1. Shelly B. Flagel and Jeremy J. Clark: These authors contributed equally to this manuscript.

Authors and Affiliations

  1. Molecular and Behavioral Neuroscience Institute, University of Michigan, Michigan, USA

    Shelly B. Flagel, Leah Mayo, Sarah M. Clinton & Huda Akil

  2. Department of Psychiatry and Behavioral Sciences and Department of Pharmacology, University of Washington, Washington, USA

    Jeremy J. Clark, Ingo Willuhn, Christina A. Akers & Paul E. M. Phillips

  3. Department of Psychology, University of Michigan, Michigan, USA

    Terry E. Robinson & Alayna Czuj

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Contributions

S.B.F, J.J.C., T.E.R., P.E.M.P. and H.A. designed the experiments and wrote the manuscript. S.B.F., J.J.C., L.M., A.C., I.W. and C.A.A. conducted the experiments, S.M.C. oversaw the selective breeding colony, and S.B.F. and J.J.C. analysed the data.

Corresponding authors

Correspondence to Paul E. M. Phillips or Huda Akil.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Results, additional references, Supplementary Figures 1-6 with legends and legends for Supplementary Movies 1-2. (PDF 986 kb)

Supplementary Movie 1

The movie shows a single trial of CS-US pairing for a bHR rat during the 6thPavlovian conditioning session (see Supplementary Information file for full legend). This movie file was replaced on 11 January 2011. (MOV 3660 kb)

Supplementary Movie 2

The movie shows a single trial of CS-US pairing for a bLR rat during the 6thPavlovian conditioning session (see Supplementary Information file for full legend). This movie file was replaced on 11 January 2011. (MOV 3544 kb)

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Flagel, S., Clark, J., Robinson, T. et al. A selective role for dopamine in stimulus–reward learning. Nature 469, 53–57 (2011). https://doi.org/10.1038/nature09588

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