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Aversive Stimuli Differentially Modulate Real-Time Dopamine Transmission Dynamics within the Nucleus Accumbens Core and Shell

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Badrinarayan, Aneesha, Wescott, Seth A., Vander Weele, Caitlin M., Saunders, Benjamin T., Couturier, Brenann E., Maren, Stephen, Aragona, Brandon J.·2012·The Journal of Neuroscience

DOI 10.1523/jneurosci.3557-12.2012PMC PMC3752139

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Abstract

Although fear directs adaptive behavioral responses, how aversive cues recruit motivational neural circuitry is poorly understood. Specifically, while it is known that dopamine (DA) transmission within the nucleus accumbens (NAc) is imperative for mediating appetitive motivated behaviors, its role in aversive behavior is controversial. It has been proposed that divergent phasic DA transmission following aversive events may correspond to segregated mesolimbic dopamine pathways; however, this prediction has never been tested. Here, we used fast-scan cyclic voltammetry to examine real-time DA transmission within NAc core and shell projection systems in response to a fear-evoking cue. In male Sprague Dawley rats, we first demonstrate that a fear cue results in decreased DA transmission within the NAc core, but increased transmission within the NAc shell. We examined whether these changes in DA transmission could be attributed to modulation of phasic transmission evoked by cue presentation. We found that cue presentation decreased the probability of phasic DA release in the core, while the same cue enhanced the amplitude of release events in the NAc shell. We further characterized the relationship between freezing and both changes in DA as well as local pH. Although we found that both analytes were significantly correlated with freezing in the NAc across the session, changes in DA were not strictly associated with freezing while basic pH shifts in the core more consistently followed behavioral expression. Together, these results provide the first real-time neurochemical evidence that aversive cues differentially modulate distinct DA projection systems.

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Self-citation
Region-specific nucleus accumbens dopamine signals encode distinct aspects of avoidance learning
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Authors: Badrinarayan, A., Wescott, S. A., Vander Weele, C. M., Saunders, B. T., Couturier, B. E., Maren, S., & Aragona, B. J.
Affiliations: University of Michigan (US)
ORCID: Saunders, Benjamin T.
Maren, Stephen
Aragona, Brandon J.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2012-11-07
Volume: 32
Issue: 45
Pages: 15779-15790
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.3557-12.2012
PMC: PMC3752139
OpenAlex: W1976193796
Cited by: 225
References: 82
Citations by year: 2026: 10 · 2025: 18 · 2024: 26 · 2023: 30 · 2022: 12 · 2021: 11 · 2020: 15 · 2019: 17 · 2018: 21 · 2017: 5 · 2016: 10 · 2015: 14 · 2014: 18 · 2013: 18
FWCI: 6.59
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation (0953106)
National Institutes of Health
National Institute of Mental Health (R01MH065961)
National Institute on Drug Abuse (T32DA007281)
National Institute of General Medical Sciences (T32GM007484)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: dopamine release, nucleus accumbens core, nucleus accumbens shell, aversive stimuli, fear, phasic dopamine release, freezing behavior, local pH, mesolimbic dopamine system, fast-scan cyclic voltammetry
MeSH terms: Animals, Conditioning, Classical, Cues, Dopamine, Electroshock, Fear, Male, Synaptic Transmission, Neurons, Nucleus Accumbens, Rats, Sprague-Dawley, Rats

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Aversive Stimuli Differentially Modulate Real-Time Dopamine Transmission Dynamics within the Nucleus Accumbens Core and Shell

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