Desire and dread from the nucleus accumbens: cortical glutamate and subcortical GABA differentially generate motivation and hedonic impact in the rat.
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BACKGROUND: GABAergic signals to the nucleus accumbens (NAc) shell arise from predominantly subcortical sources whereas glutamatergic signals arise mainly from cortical-related sources. Here we contrasted GABAergic and glutamatergic generation of hedonics versus motivation processes, as a proxy for comparing subcortical and cortical controls of emotion. Local disruptions of either signals in medial shell of NAc generate intense motivated behaviors corresponding to desire and/or dread, along a rostrocaudal gradient. GABA or glutamate disruptions in rostral shell generate appetitive motivation whereas disruptions in caudal shell elicit fearful motivation. However, GABA and glutamate signals in NAc differ in important ways, despite the similarity of their rostrocaudal motivation gradients. METHODOLOGY/PRINCIPAL FINDINGS: Microinjections of a GABA(A) agonist (muscimol), or of a glutamate AMPA antagonist (DNQX) in medial shell of rats were assessed for generation of hedonic "liking" or "disliking" by measuring orofacial affective reactions to sucrose-quinine taste. Motivation generation was independently assessed measuring effects on eating versus natural defensive behaviors. For GABAergic microinjections, we found that the desire-dread motivation gradient was mirrored by an equivalent hedonic gradient that amplified affective taste "liking" (at rostral sites) versus "disliking" (at caudal sites). However, manipulation of glutamatergic signals completely failed to alter pleasure-displeasure reactions to sensory hedonic impact, despite producing a strong rostrocaudal gradient of motivation. CONCLUSIONS/SIGNIFICANCE: We conclude that the nucleus accumbens contains two functional affective keyboards for amino-acid signals: a motivation-generating keyboard and a hedonic-generating keyboard. Corticolimbic glutamate signals and subcortical GABA signals equivalently engage the motivation keyboard to generate desire and-or dread. Only subcortical GABA signals additionally engage the hedonic keyboard to amplify affective "liking" and "disliking" reactions. We thus suggest that top-down cortical glutamate signals powerfully regulate motivation components, but are relatively unable to penetrate core hedonic components of emotion. That may carry implications of limits to therapeutic regulation of pathological emotions.
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Neural mechanisms that generate 'disgust' and 'fear' reactions are mostly distinct, though they do partly overlap in the posterior shell of nucleus accumbens.
“However, neural mechanisms that generate ‘disgust’ and ‘fear’ reactions are mostly distinct, though they do partly overlap in the posterior shell of nucleus accumbens (Faure et al., 2010; Maren et al., 2013; Ho and Berridge, 2014; Perusini and Fanselow, 2015; Paré and Quirk, 2017).”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Faure et al., 2010
In this GABA-related mode, the normally 'liked' taste of sucrose instead elicits 'disgust' gapes and headshakes from rats, as though the taste were bitter quinine.
“In this GABA-related mode, the normally ‘liked’ taste of sucrose instead elicits ‘disgust’ gapes and headshakes from rats, as though the taste were bitter quinine.”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Faure et al., 2010
Animal brain-manipulation studies show one interesting overlap in neural generators for intense 'disgust' and 'fear' reactions in nucleus accumbens, involving a shift in neural mode of function at the same brain location.
“Yet our animal brain-manipulation studies show one interesting overlap in neural generators for intense ‘disgust’ and ‘fear’ reactions in nucleus accumbens, involving a shift in neural mode of function at the same brain location.”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Faure et al., 2010
This 'disgust-plus-fear' mode is produced when the posterior shell zone receives microinjections of a drug that activates GABA receptors, such as muscimol.
“This ‘disgust-plus-fear’ mode is produced when the posterior shell zone receives microinjections of a drug that activates GABA receptors, such as muscimol (Faure et al., 2010; Ho and Berridge, 2014).”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Faure et al., 2010
The posterior portion of the medial shell has two 'fear' generating neurochemical modes (glutamate AMPA receptor blockade versus GABA receptor activation), and only the GABA mode also generates excessive 'disgust'.
“The posterior portion of its medial shell has two ‘fear’ generating neurochemical modes (glutamate AMPA receptor blockade versus GABA receptor activation), and only the GABA mode also generates excessive ‘disgust’.”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Faure et al., 2010
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- Authors
- Faure, A., Richard, J. M., & Berridge, K. C.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Faure, Alexis
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-06-18
- Volume
- 5
- Issue
- 6
- Pages
- e11223
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2887893
- OpenAlex
- W2084903850
- Cited by
- 114
- References
- 81
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 3 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 10 · 2019: 10 · 2018: 8 · 2017: 5 · 2016: 6 · 2015: 11 · 2014: 11 · 2013: 7 · 2012: 9
- FWCI
- 3.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH-63649, R01MH063649)
- National Institute on Drug Abuse (DA015188, R01DA015188)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- nucleus accumbens shell, GABAergic neurotransmission, glutamatergic signaling, motivation, desire, dread, appetitive motivation, muscimol, DNQX, rostrocaudal gradient, emotion regulation
- MeSH terms
- Animals, Fear, Feeding Behavior, gamma-Aminobutyric Acid, Motivation, Muscimol, Nucleus Accumbens, Quinoxalines, Glutamic Acid, Rats
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