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Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala
Open accessAbstract
Serotonin (also known as 5-hydroxytryptamine (5-HT)) is a neurotransmitter that has an essential role in the regulation of emotion. However, the precise circuits have not yet been defined through which aversive states are orchestrated by 5-HT. Here we show that 5-HT from the dorsal raphe nucleus (5-HT DRN) enhances fear and anxiety and activates a subpopulation of corticotropin-releasing factor (CRF) neurons in the bed nucleus of the stria terminalis (CRF BNST) in mice. Specifically, 5-HT DRN projections to the BNST, via actions at 5-HT 2C receptors (5-HT 2C Rs), engage a CRF BNST inhibitory microcircuit that silences anxiolytic BNST outputs to the ventral tegmental area and lateral hypothalamus. Furthermore, we demonstrate that this CRF BNST inhibitory circuit underlies aversive behaviour following acute exposure to selective serotonin reuptake inhibitors (SSRIs). This early aversive effect is mediated via the corticotrophin-releasing factor type 1 receptor (CRF 1 R, also known as CRHR1), given that CRF 1 R antagonism is sufficient to prevent acute SSRI-induced enhancements in aversive learning. These results reveal an essential 5-HT DRN→CRF BNST circuit governing fear and anxiety, and provide a potential mechanistic explanation for the clinical observation of early adverse events to SSRI treatment in some patients with anxiety disorders.
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“This suggests these drugs affect multiple 5-HT pathways with distinct and contrasting effects on behavior and highlights the need for new approaches to target specific 5-HT neurons and their outputs (Marcinkiewcz et al., 2016; Urban et al., 2016).”
From Molecular and anatomical organization of the dorsal raphe nucleus (2019) · cites this paper as Marcinkiewcz et al., 2016
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Metadata
- Authors
- Marcinkiewcz, C. A., Mazzone, C. M., D’Agostino, G., Halladay, L. R., Hardaway, J. A., DiBerto, J. F., Navarro, M., Burnham, N., Cristiano, C., Dorrier, C. E., Tipton, G. J., Ramakrishnan, C., Kozicz, T., Deisseroth, K., Thiele, T. E., McElligott, Z. A., Holmes, A., Heisler, L. K., & Kash, T. L.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- University of Aberdeen (GB)
- National Institutes of Health (US)
- Stanford University (US)
- Corresponding author
- Kash, Thomas L.
- ORCID
- Venue
- Nature
- Published
- 2016-08-24
- Volume
- 537
- Issue
- 7618
- Pages
- 97-101
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5124365
- OpenAlex
- W2516878167
- Cited by
- 456
- References
- 25
- Citations by year
- 2026: 45 · 2025: 41 · 2024: 41 · 2023: 48 · 2022: 53 · 2021: 46 · 2020: 51 · 2019: 45 · 2018: 46 · 2017: 35 · 2016: 3
- FWCI
- 24.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Wellcome Trust (098012)
- National Institutes of Health (5f32aa021319-02, AA011605)
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (BB/K001418/1)
- National Institute on Alcohol Abuse and Alcoholism (P50AA011605, AA019454, AA011605, F31AA023440, F32-AA021319, K01AA023555, P60AA011605, R01AA019454)
- National Institute of Mental Health (T32MH076694)
- 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
- serotonin, anxiety, fear, extended amygdala, bed nucleus of the stria terminalis, dorsal raphe nucleus, corticotropin-releasing hormone neurons, 5-HT2C receptor, CRF1 receptor, fluoxetine, selective serotonin reuptake inhibitors, adverse drug reactions, ventral tegmental area, lateral hypothalamus, aversive learning
- MeSH terms
- CRF Receptor, Type 1, Amygdala, Animals, Anxiety, Anxiety Disorders, Corticotropin-Releasing Hormone, Fear, Female, Fluoxetine, Hypothalamus, Male, Neurons, Serotonin, Thalamus, Selective Serotonin Reuptake Inhibitors, Ventral Tegmental Area, Receptors, Corticotropin-Releasing Hormone, Mice, Optogenetics, Dorsal Raphe Nucleus
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