Aversive stimulus differentially triggers subsecond dopamine release in reward regions
Open accessAbstract
Aversive stimuli have a powerful impact on behavior and are considered to be the opposite valence of pleasure. Recent studies have determined some populations of ventral tegmental area (VTA) dopaminergic neurons are activated by several types of aversive stimuli, whereas other distinct populations are either inhibited or unresponsive. However, it is not clear where these aversion-responsive neurons project, and whether alterations in their activity translate into dopamine release in the terminal field. Here we show unequivocally that the neurochemical and anatomical substrates responsible for the perception and processing of pleasurable stimuli within the striatum are also activated by tail pinch, a classical painful and aversive stimulus. Dopamine release is triggered in the dorsal striatum and nucleus accumbens (NAc) core by tail pinch and is time locked to the duration of the stimulus, indicating that the dorsal striatum and NAc core are neural substrates, which are involved in the perception of aversive stimuli. However, dopamine is released in the NAc shell only when tail pinch is removed, indicating that the alleviation of aversive condition could be perceived as a rewarding event.
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Aversive stimuli induce delayed, post-stimulus dopamine release in the shell of the nucleus accumbens, the magnitude of which predicts successful punishment avoidance.
“Correspondingly, aversive stimuli induce delayed, post-stimulus dopamine release in the shell of the nucleus accumbens63,133, the magnitude of which predicts successful punishment avoidance136.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [63]
Some studies have reported that aversive stimuli inhibit DA activity of midbrain neurons, whereas others have found that they elicit phasic DA release in the VS.
“whereas some studies have reported that aversive stimuli inhibit the DA activity of midbrain neurons (e.g., [67]), others have found that they elicit phasic DA release in the VS (e.g., [68]).”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [68]
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- Authors
- Budygin, E. A., Park, J., Bass, C. E., Grinevich, V. P., Bonin, K. D., & Wightman, R. M.
- Affiliations
- Wake Forest University Health Sciences (US)
- University of North Carolina at Chapel Hill (US)
- University at Buffalo, State University of New York (US)
- Wake Forest University (US)
- Corresponding author
- Budygin, E.A.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 201
- Pages
- 331-337
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC3258373
- OpenAlex
- W1978660947
- Cited by
- 152
- References
- 37
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 8 · 2023: 7 · 2022: 11 · 2021: 13 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 5 · 2016: 12 · 2015: 12 · 2014: 13 · 2013: 13 · 2012: 14
- FWCI
- 5.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (DA024763, DA-109000, K01DA021634, K01DA024763, R01DA010900, DA021634)
- National Institute of Neurological Disorders and Stroke (R01NS015841)
- 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
- aversive stimuli, dopamine release, tail pinch, dorsal striatum, nucleus accumbens core, nucleus accumbens shell, ventral tegmental area, reward processing, aversion, pain perception
- MeSH terms
- Animals, Behavior, Animal, Corpus Striatum, Dopamine, Electric Stimulation, Evoked Potentials, Male, Neurons, Nucleus Accumbens, Physical Stimulation, Piperazines, Rats, Sprague-Dawley, Dopamine Uptake Inhibitors, Rats
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