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Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala
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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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“As 5-HT in the Amy has been linked to anxiety and depression (Bocchio et al. 2016; Marcinkiewcz et al. 2016), disruptions in this system may also account for the changes in 5-HT levels observed in the 20 L:4D rats and the likely rise in NA of the 4 L:20D rats.”
Amidfar, M., & Kim, Y. (2022) · Neuromethods · doi:10.1007/978-1-0716-2083-0_9 · Cited by 1
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Anatomical and functional characterization of serotonergic neurocircuitry
Dorocic, I. P. (2016) · Figshare · Cited by 1
A BNST-Centered Microcircuit Regulating Inflammation-Associated Anorexia and FeedingPreprint
Wang, Y., Kim, J., Schmit, M. B., Cho, T., Fang, C., & Cai, H. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3236485 · Cited by 2
Flanigan, M. E., Hon, O. J., D’Ambrosio, S., Boyt, K. M., Hassanein, L. A., Castle, M. Z. D., Haun, H. L., Pina, M. M., & Kash, T. L. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.28.478036 · Cited by 1
“…animal models report that manipulations of 5-HT signaling can both increase and decrease alcohol consumption and associated negative affect (Campbell et al., 2021; Filip et al., 2012; Fu et al., 2020; Marcinkiewcz et al., 2015; Marcinkiewcz et al., 2016a; Tabbara et al., 2021; Umhau et al., 2011).”
BackgroundResultInfluentialThe Central Extended Amygdala Guides Survival-Relevant Tradeoffs for Action SelectionPreprint
Holley, D., & Fox, A. S. (2022) · doi:10.31234/osf.io/z9w3t · Cited by 1
Hamada, H. T., Abe, Y., Takata, N., Taira, M., Tanaka, K. F., & Doya, K. (2022) · Research Square · doi:10.21203/rs.3.rs-1958666/v1 · Cited by 1
Serotonin shapes the temporal window for associative fear learningPreprint
Zhao, Y., Li, X., Chang, T., Xie, S., Wu, Y., Li, S., Cao, J., Wang, D., Deng, F., Feng, J., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.06.669013 · Cited by 1
“The serotonergic system has been implicated in fear learning efficiency, particularly in delay fear conditioning 19,20 .”
Hyperexcitability of female serotonin neurons underlies sex-specific anxiety responsesPreprint
Pizzoccaro, L., van der Veldt, S., Henderson, F. J., Simard, A.-S., Perreault, F., Fortin‐Houde, J., Lalot, E., Ducharme, G., & Amilhon, B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.17.670715 · Cited by 3
Serotonergic modulation of motor subspace dynamics drives a sleep-independent quiescent statePreprint
Qi, K., Chai, Y., Tan, G., Li, D., & Wen, Q. (2026) · eLife · doi:10.7554/elife.110370 · Cited by 2
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“A second arm that is likely also contributing to this comorbidity involves the role of serotonin in neuronal functions and psychiatric disorders, including fear conditioning [44, 53] as well as in platelet homeostasis [45].”
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“Furthermore, the BNST is known to regulate feeding, fear, anxiety- and rewardlike behaviors via projections to the VTA and LH (Jennings et al., 2013a,b; Marcinkiewcz et al., 2016).”
BackgroundInfluentialHypothalamic-extended amygdala circuit regulates temporal discountingPreprint
Rossi, M. A., Li, H. E., Watson, G. D. R., Moore, H. G., Cai, M. T., Kim, N., Vokt, K. A., Lu, D., Bartholomew, R. A., & Yin, H. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/577973
“11 The BNST has been implicated in stress, anxiety, and other aversive motivational states (Marcinkiewcz et al., 2016; Sahuque et al., 2006).”
BackgroundContributions of Genetically Defined Cell Populations in the Extended Amygdala to Emotional Behavior
Mazzone, C. M. (2017) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/mn8w-xr58
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“…coping during protracted withdrawal from alcohol complement established 15 research characterizing the extended amygdala to BNST anxiolytic-like circuitry using chemoand optogenetics in mice (Kim et al. 2013, Jennings et al. 2013, Marcinkiewcz et al. 2016, Mazzone et al. 2018, Crowley et al. 2016).”
Genetic Dissection of Neuropeptide Circuits Mediating Psychosocial Stress
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How Do Abnormalities in the Cerebrospinal Fluid Impact Neuropsychology with Progressing Age?
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CRF neurons of the BNST promote resilience by blunting the internal experience of aversionPreprint
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“5-HT is implicated in a variety of physiological functions, including the regulation of sensory and motor responses [2–5], brain states [6–8], learning and reward processing [9–11], fear responses [12] and social interactions [13,14].”
BackgroundHon, O. J., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D’Ambrosio, S., Lee, S., Simpson, Y., Buccini, M. C., Machinski, S. N., et al. (2023) · eLife · doi:10.7554/elife.89189.1 · Cited by 1
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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