Subsecond dopamine fluctuations in human striatum encode superposed error signals about actual and counterfactual reward

Author:

Kishida Kenneth T.1,Saez Ignacio1,Lohrenz Terry1,Witcher Mark R.2,Laxton Adrian W.2,Tatter Stephen B.2,White Jason P.1,Ellis Thomas L.2,Phillips Paul E. M.34,Montague P. Read156

Affiliation:

1. Virginia Tech Carilion Research Institute, Virginia Tech, Roanoke, VA 24016;

2. Department of Neurosurgery, Wake Forest Health Sciences, Winston-Salem, NC 27157;

3. Department of Psychiatry & Behavioral Sciences, University of Washington, Seattle, WA 98195;

4. Department of Pharmacology, University of Washington, Seattle, WA 98195;

5. Department of Physics, Virginia Tech, Blacksburg, VA 24060;

6. Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom

Abstract

SignificanceThere is an abundance of circumstantial evidence (primarily work in nonhuman animal models) suggesting that dopamine transients serve as experience-dependent learning signals. This report establishes, to our knowledge, the first direct demonstration that subsecond fluctuations in dopamine concentration in the human striatum combine two distinct prediction error signals: (i) an experience-dependent reward prediction error term and (ii) a counterfactual prediction error term. These data are surprising because there is no prior evidence that fluctuations in dopamine should superpose actual and counterfactual information in humans. The observed compositional encoding of “actual” and “possible” is consistent with how one should “feel” and may be one example of how the human brain translates computations over experience to embodied states of subjective feeling.

Funder

Wellcome Trust Principal Research Fellowship

Virgnia Tech

Kane Family Foundation

Publisher

Proceedings of the National Academy of Sciences

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