Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste “liking”/“disliking” reactions, place preference/avoidance, and fear
Open accessAbstract
Microinjection of the GABA(A) agonist muscimol in the rostral medial accumbens shell in rats elicits appetitive eating behavior, but in the caudal shell instead elicits fearful defensive treading behavior. To further test the hypothesis that rostral shell muscimol microinjections produce positive motivational states, whereas caudal shell muscimol produces negative states, we measured behavioral place preference/avoidance conditioning and affective hedonic and aversive orofacial expressions of taste-elicited "liking" and "disliking" (gapes, etc.) in addition to fear and feeding behaviors. Farthest rostral muscimol microinjections (75 ng) caused increased eating behavior and also caused positive conditioned place preferences and increased positive hedonic reactions to the taste of sucrose. By contrast, caudal shell microinjections elicited negative defensive treading and caused robust negative conditioned place avoidance and negative aversive reactions to sucrose or quinine tastes. Intermediate rostral microinjections elicited effects of mixed positive/negative valence (positive appetitive eating behavior but negative place avoidance and negative taste reactions at mid-rostral sites, and sometimes positive eating simultaneously with fearful defensive treading more caudally). These results indicate that GABAergic neurotransmission in local microcircuits in nucleus accumbens mediates motivated/affective behavior that is bivalently organized along rostrocaudal gradients.
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Even rats do many things within a single emotion category: in the face of threat, they can freeze, flee, or engage in defensive treading.
“Even rats do many things within a single emotion category: in the face of a threat, rats can freeze (e.g., LeDoux et al. 1990), flee (Vazdarjanova & McGaugh 1998), or engage in “defensive treading,” in which they kick bedding in the direction of a known threat (Reynolds & Berridge 2002; 2003; 2008).”
From The brain basis of emotion: a meta-analytic review (2012) · cites this paper as Reynolds & Berridge 2002
The “GABAergic defensive treading, affect, and fear” section describes rats kicking sand toward targets and building protective mounds, and compares this with natural responses to threats. But it says the treading observed in this study was directed at parts of the chamber in the absence of actual threats, so it does not establish the claim’s specific description of bedding kicked toward a known threat. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIntermediate shell GABAergic activation produces combined positive and negative motivational effects.
“Intermediate shell GABAergic activation produces combined positive and negative motivational effects (Reynolds and Berridge, 2002).”
From Dopaminergic reward sensitivity can promote adolescent health: a new perspective on the mechanism of ventral striatum activation (2016) · cites this paper as Reynolds and Berridge, 2002
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Self-citationMonk, C. S., Klein, R. G., Telzer, E. H., Schroth, E. A., Mannuzza, S., Moulton, J. L., Guardino, M., Masten, C. L., McClure-Tone, E. B., Fromm, S., et al. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.06111917 · Cited by 335 · see citing works
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Discovering imaging endophenotypes for major depression
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Telzer, E. H. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.10.010 · Cited by 274 · see citing works
Li, S., & Kirouac, G. J. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21502 · Cited by 261 · see citing works
Reynolds, S. M., & Berridge, K. C. (2008) · Nature Neuroscience · doi:10.1038/nn2061 · Cited by 244 · see citing works
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Self-citationPeciña, S., & Berridge, K. C. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12174 · Cited by 216 · see citing works
Self-citationStriatal functional alteration in adolescents characterized by early childhood behavioral inhibition
Guyer, A. E., Nelson, E. E., Perez-Edgar, K., Hardin, M. G., Roberson-Nay, R., Monk, C. S., Bjork, J. M., Henderson, H. A., Pine, D. S., Fox, N. A., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0666-06.2006 · Cited by 211 · see citing works
Peciña, S., Schulkin, J., & Berridge, K. C. (2006) · BMC Biology · doi:10.1186/1741-7007-4-8 · Cited by 194 · see citing works
Self-citationActive Avoidance Requires a Serial Basal Amygdala to Nucleus Accumbens Shell Circuit
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Faure, A., Reynolds, S. M., Richard, J. M., & Berridge, K. C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4961-07.2008 · Cited by 193 · see citing works
Self-citationAltered neural reward and loss processing and prediction error signalling in depression
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Two brain sites for cannabinoid reward
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Current perspectives on incentive salience and applications to clinical disorders
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The bivalent side of the nucleus accumbens
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Self-citationGoal-directed control and its antipodes
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The role of dopamine in alcohol self-administration in humans: individual differences
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Stress-Induced Potentiation of Cocaine Reward: A Role for CRFR1 and CREB
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Acute Changes in Striatal Microstructure Predict the Development of Interferon-Alpha Induced Fatigue
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De Matteo, R., Head, G. A., & Mayorov, D. N. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00372.2005 · Cited by 33 · see citing works
- Authors
- Reynolds, S. M., & Berridge, K. C.
- Affiliations
- University of Michigan (US)
- ORCID
- Berridge, Kent C.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-08-15
- Volume
- 22
- Issue
- 16
- Pages
- 7308-7320
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6757899
- OpenAlex
- W2132465696
- Cited by
- 403
- References
- 80
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 5 · 2023: 11 · 2022: 9 · 2021: 14 · 2020: 16 · 2019: 50 · 2018: 13 · 2017: 11 · 2016: 7 · 2015: 28 · 2014: 19 · 2013: 17 · 2012: 25
- FWCI
- 3.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9604408)
- National Institutes of Health (DC00011)
- National Institute on Drug Abuse (F31DA014679)
- National Institute on Deafness and Other Communication Disorders (DC-00011, T32DC00011, T32DC000011)
- 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
- nucleus accumbens shell, rostrocaudal gradient, GABAergic neurotransmission, muscimol microinjection, positive motivation, negative motivation, conditioned place preference, conditioned place avoidance, taste liking, fear, sucrose, quinine, emotional behavior
- MeSH terms
- Animals, Behavior, Animal, Conditioning, Psychological, Eating, Fear, Feeding Behavior, Female, gamma-Aminobutyric Acid, Male, Microinjections, Motivation, Muscimol, Nucleus Accumbens, Spatial Behavior, Taste, Rats, Sprague-Dawley, GABA Agonists, Rats
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