Nicotine inhibits the VTA-to-amygdala dopamine pathway to promote anxiety
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Abstract
Nicotine stimulates dopamine (DA) neurons of the ventral tegmental area (VTA) to establish and maintain reinforcement. Nicotine also induces anxiety through an as yet unknown circuitry. We found that nicotine injection drives opposite functional responses of two distinct populations of VTA DA neurons with anatomically segregated projections: it activates neurons that project to the nucleus accumbens (NAc), whereas it inhibits neurons that project to the amygdala nuclei (Amg). We further show that nicotine mediates anxiety-like behavior by acting on β2-subunit-containing nicotinic acetylcholine receptors of the VTA. Finally, using optogenetics, we bidirectionally manipulate the VTA-NAc and VTA-Amg pathways to dissociate their contributions to anxiety-like behavior. We show that inhibition of VTA-Amg DA neurons mediates anxiety-like behavior, while their activation prevents the anxiogenic effects of nicotine. These distinct subpopulations of VTA DA neurons with opposite responses to nicotine may differentially drive the anxiogenic and the reinforcing effects of nicotine.
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Nicotine in adolescence is poised to alter DA development because it acts directly on VTA DA neurons through their expression of nAChRs, modulating their firing rate in a population-specific manner in adult rodents.
“Nicotine in adolescence is thus poised to alter DA development, as it acts directly on VTA DA neurons through their expression of nAChRs, modulating their firing rate in a population-specific manner in adult rodents [72, 137–139].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [137]
These behavioral outcomes are linked with an electrophysiological signature of hyper-reactivity to nicotine specifically in the VTA-NAc circuit, and not in the VTA-Amygdala circuit.
“These behavioral outcomes were linked with an electrophysiological signature of hyper-reactivity to nicotine specifically in the VTA-NAc circuit, and not in the VTA-Amygdala circuit, despite the clear role of this pathway in the anxiogenic effects of nicotine [137].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [137]
Exposure to nicotine in early adolescence (PND 21-28), but not the same exposure in adulthood (PND 60+), produces enduring alterations in sensitivity to nicotine, notably increased sensitivity to its rewarding effects and decreased sensitivity to its anxiogenic effects.
“Our recent study showed that exposure to nicotine in early adolescence (PND 21–28), but not the same nicotine exposure in adulthood (PND 60 + ), produced enduring alterations in sensitivity to nicotine, notably defined by an increased sensitivity to its rewarding effects and a decreased sensitivity to its anxiogenic effects.”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [137]
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- Authors
- Nguyen, C., Mondoloni, S., Le Borgne, T., Centeno, I., Come, M., Jehl, J., Solié, C., Reynolds, L. M., Durand-de Cuttoli, R., Tolu, S., Valverde, S., Didienne, S., Hannesse, B., Fiancette, J.-F., Pons, S., Maskos, U., Deroche-Gamonet, V., Dalkara, D., Hardelin, J.-P., Mourot, A., Marti, F., & Faure, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Université de Bordeaux (FR)
- Institut Pasteur (FR)
- Corresponding author
- Marti, Fabio
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2021-08
- Volume
- 109
- Issue
- 16
- Pages
- 2604-2615.e9
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W3179632423
- Cited by
- 136
- References
- 64
- Citations by year
- 2026: 21 · 2025: 25 · 2024: 40 · 2023: 30 · 2022: 14 · 2021: 5 · 2020: 1
- FWCI
- 10.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion)
- Funders
- Centre National de la Recherche Scientifique (UMR 8246)
- INCa (TABAC-19-020, TABAC-16-022)
- Fondation pour la Recherche Médicale (SPF202005011922, DEQ2013326488, FDT201904008060, ECO201806006688)
- Institut National de la Santé et de la Recherche Médicale (U1130)
- Peking University
- ANR (ANR-16 Nicostress)
- National Institute on Drug Abuse
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotine, anxiety, ventral tegmental area, amygdala, dopaminergic neurons, nucleus accumbens, nicotinic acetylcholine receptors, beta2 subunit, anxiogenic effects, reinforcement, neuronal subpopulations, optogenetics
- MeSH terms
- Amygdala, Animals, Anxiety, Dopamine, Male, Neural Pathways, Nicotine, Nucleus Accumbens, Receptors, Nicotinic, Reinforcement, Psychology, Ventral Tegmental Area, Nicotinic Agonists, Mice, Dopaminergic Neurons
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