Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term

Andrew S. Hart, Robb B. Rutledge, Paul Glimcher, Paul E M Phillips

Research output: Contribution to journalArticle

Abstract

Making predictions about the rewards associated with environmental stimuli and updating those predictions through feedback is an essential aspect of adaptive behavior. Theorists have argued that dopamine encodes a reward prediction error (RPE) signal that is used in such a reinforcement learning process. Recent work with fMRI has demonstrated that the BOLD signal in dopaminergic target areas meets both necessary and sufficient conditions of an axiomatic model of the RPE hypothesis. However, there has been no direct evidence that dopamine release itself also meets necessary and sufficient criteria for encoding an RPE signal. Further, the fact that dopamine neurons have low tonic firing rates that yield a limited dynamic range for encoding negative RPEs has led to significant debate about whether positive and negative prediction errors are encoded on a similar scale. To address both of these issues, we used fast-scan cyclic voltammetry to measure reward-evoked dopamine release at carbon fiber electrodes chronically implanted in the nucleus accumbens core of rats trained on a probabilistic decision-making task. Wedemonstrate that dopamine concentrations transmit a bidirectional RPE signal with symmetrical encoding of positive and negative RPEs. Our findings strengthen the case that changes in dopamine concentration alone are sufficient to encode the full range of RPEs necessary for reinforcement learning.

Original languageEnglish (US)
Pages (from-to)698-704
Number of pages7
JournalJournal of Neuroscience
Volume34
Issue number3
DOIs
StatePublished - 2014

Fingerprint

Nucleus Accumbens
Reward
Dopamine
Learning
Implanted Electrodes
Dopaminergic Neurons
Psychological Adaptation
Decision Making
Magnetic Resonance Imaging

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. / Hart, Andrew S.; Rutledge, Robb B.; Glimcher, Paul; Phillips, Paul E M.

In: Journal of Neuroscience, Vol. 34, No. 3, 2014, p. 698-704.

Research output: Contribution to journalArticle

Hart, Andrew S. ; Rutledge, Robb B. ; Glimcher, Paul ; Phillips, Paul E M. / Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 3. pp. 698-704.
@article{7f7b328a849f4d48912c4bb6255ea8e0,
title = "Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term",
abstract = "Making predictions about the rewards associated with environmental stimuli and updating those predictions through feedback is an essential aspect of adaptive behavior. Theorists have argued that dopamine encodes a reward prediction error (RPE) signal that is used in such a reinforcement learning process. Recent work with fMRI has demonstrated that the BOLD signal in dopaminergic target areas meets both necessary and sufficient conditions of an axiomatic model of the RPE hypothesis. However, there has been no direct evidence that dopamine release itself also meets necessary and sufficient criteria for encoding an RPE signal. Further, the fact that dopamine neurons have low tonic firing rates that yield a limited dynamic range for encoding negative RPEs has led to significant debate about whether positive and negative prediction errors are encoded on a similar scale. To address both of these issues, we used fast-scan cyclic voltammetry to measure reward-evoked dopamine release at carbon fiber electrodes chronically implanted in the nucleus accumbens core of rats trained on a probabilistic decision-making task. Wedemonstrate that dopamine concentrations transmit a bidirectional RPE signal with symmetrical encoding of positive and negative RPEs. Our findings strengthen the case that changes in dopamine concentration alone are sufficient to encode the full range of RPEs necessary for reinforcement learning.",
author = "Hart, {Andrew S.} and Rutledge, {Robb B.} and Paul Glimcher and Phillips, {Paul E M}",
year = "2014",
doi = "10.1523/JNEUROSCI.2489-13.2014",
language = "English (US)",
volume = "34",
pages = "698--704",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "3",

}

TY - JOUR

T1 - Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term

AU - Hart, Andrew S.

AU - Rutledge, Robb B.

AU - Glimcher, Paul

AU - Phillips, Paul E M

PY - 2014

Y1 - 2014

N2 - Making predictions about the rewards associated with environmental stimuli and updating those predictions through feedback is an essential aspect of adaptive behavior. Theorists have argued that dopamine encodes a reward prediction error (RPE) signal that is used in such a reinforcement learning process. Recent work with fMRI has demonstrated that the BOLD signal in dopaminergic target areas meets both necessary and sufficient conditions of an axiomatic model of the RPE hypothesis. However, there has been no direct evidence that dopamine release itself also meets necessary and sufficient criteria for encoding an RPE signal. Further, the fact that dopamine neurons have low tonic firing rates that yield a limited dynamic range for encoding negative RPEs has led to significant debate about whether positive and negative prediction errors are encoded on a similar scale. To address both of these issues, we used fast-scan cyclic voltammetry to measure reward-evoked dopamine release at carbon fiber electrodes chronically implanted in the nucleus accumbens core of rats trained on a probabilistic decision-making task. Wedemonstrate that dopamine concentrations transmit a bidirectional RPE signal with symmetrical encoding of positive and negative RPEs. Our findings strengthen the case that changes in dopamine concentration alone are sufficient to encode the full range of RPEs necessary for reinforcement learning.

AB - Making predictions about the rewards associated with environmental stimuli and updating those predictions through feedback is an essential aspect of adaptive behavior. Theorists have argued that dopamine encodes a reward prediction error (RPE) signal that is used in such a reinforcement learning process. Recent work with fMRI has demonstrated that the BOLD signal in dopaminergic target areas meets both necessary and sufficient conditions of an axiomatic model of the RPE hypothesis. However, there has been no direct evidence that dopamine release itself also meets necessary and sufficient criteria for encoding an RPE signal. Further, the fact that dopamine neurons have low tonic firing rates that yield a limited dynamic range for encoding negative RPEs has led to significant debate about whether positive and negative prediction errors are encoded on a similar scale. To address both of these issues, we used fast-scan cyclic voltammetry to measure reward-evoked dopamine release at carbon fiber electrodes chronically implanted in the nucleus accumbens core of rats trained on a probabilistic decision-making task. Wedemonstrate that dopamine concentrations transmit a bidirectional RPE signal with symmetrical encoding of positive and negative RPEs. Our findings strengthen the case that changes in dopamine concentration alone are sufficient to encode the full range of RPEs necessary for reinforcement learning.

UR - http://www.scopus.com/inward/record.url?scp=84892388605&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84892388605&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.2489-13.2014

DO - 10.1523/JNEUROSCI.2489-13.2014

M3 - Article

VL - 34

SP - 698

EP - 704

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 3

ER -