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Neuron-type-specific signals for reward and punishment in the ventral tegmental area

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Cohen, Jeremiah Y., Haesler, Sebastian, Vong, Linh, Lowell, Bradford B., Uchida, Naoshige·2012·Nature

DOI 10.1038/nature10754PMC PMC3271183

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Abstract

Dopamine has a central role in motivation and reward. Dopaminergic neurons in the ventral tegmental area (VTA) signal the discrepancy between expected and actual rewards (that is, reward prediction error), but how they compute such signals is unknown. We recorded the activity of VTA neurons while mice associated different odour cues with appetitive and aversive outcomes. We found three types of neuron based on responses to odours and outcomes: approximately half of the neurons (type I, 52%) showed phasic excitation after reward-predicting odours and rewards in a manner consistent with reward prediction error coding; the other half of neurons showed persistent activity during the delay between odour and outcome that was modulated positively (type II, 31%) or negatively (type III, 18%) by the value of outcomes. Whereas the activity of type I neurons was sensitive to actual outcomes (that is, when the reward was delivered as expected compared to when it was unexpectedly omitted), the activity of type II and type III neurons was determined predominantly by reward-predicting odours. We 'tagged' dopaminergic and GABAergic neurons with the light-sensitive protein channelrhodopsin-2 and identified them based on their responses to optical stimulation while recording. All identified dopaminergic neurons were of type I and all GABAergic neurons were of type II. These results show that VTA GABAergic neurons signal expected reward, a key variable for dopaminergic neurons to calculate reward prediction error.

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Authors: Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N.
Affiliations: Harvard University (US)
Beth Israel Deaconess Medical Center (US)
Corresponding author: Uchida, Naoshige
ORCID: Cohen, Jeremiah Y.
Haesler, Sebastian
Vong, Linh
Lowell, Bradford B.
Uchida, Naoshige
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-01-18
Volume: 482
Issue: 7383
Pages: 85-88
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10754
PMC: PMC3271183
OpenAlex: W2022561563
Cited by: 1,318
References: 39
Citations by year: 2026: 52 · 2025: 115 · 2024: 90 · 2023: 78 · 2022: 99 · 2021: 116 · 2020: 113 · 2019: 106 · 2018: 100 · 2017: 83 · 2016: 88 · 2015: 102 · 2014: 69 · 2013: 63 · 2012: 43
FWCI: 36.51
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institute of Mental Health (R01MH095953)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK057521, R01DK075632, R01DK089044, P30DK046200, F32DK078478)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: ventral tegmental area, dopaminergic neurons, GABAergic neurons, reward prediction error, reward anticipation, aversive stimuli, dopamine, channelrhodopsin-2
MeSH terms: Channelrhodopsins, Animals, Cues, Dopamine, gamma-Aminobutyric Acid, Male, Mice, Inbred C57BL, Odorants, Punishment, Reward, Ventral Tegmental Area, Principal Component Analysis, Mice, Dopaminergic Neurons, GABAergic Neurons

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Neuron-type-specific signals for reward and punishment in the ventral tegmental area

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