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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These drugs affect multiple 5-HT pathways with distinct and contrasting effects on behavior.
“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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Role of the bed nucleus of the stria terminalis in aversive learning and memoryPreprint
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“Further, it is now understood that different populations of neurons within the BNST can bidirectionally regulate various unlearned anxiety-like responses (Jennings et al. 2013; Kim et al. 2013; Crowley et al. 2016; Marcinkiewcz et al. 2016; Mazzone et al. 2016).”
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“…population of CRF neurons are present within the BNST. Data suggest that these CRF BNST neurons are exclusively GABAergic, and these GABAergic CRF neurons are highly interconnected with CRF negative neurons within the BNST (Marcinkiewcz et al., 2016, Mazzone et al., 2016; Partridge et al., 2016).”
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“o, Average traces (left; mean ± 95% CI; shading, opto-activation) and statistics (right; n = 6 mice; two-sided RM two-way ANOVA, F(2, 15) = 319.”
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“DRN-BNST ? ? Anxiogenic when activated [84]”
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“Emerging data suggest that amygdala abnormalities, particularly within the central nucleus of the amygdala and the BNST, are important substrates of anxiety (Kim et al., 2013; Tovote et al., 2015; Marcinkiewcz et al., 2016; Shackman and Fox, 2016).”
BackgroundEndocrinology and the brain: corticotropin-releasing hormone signaling
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Serotonin inputs to the dorsal BNST modulate anxiety in a 5-HT1A receptor-dependent manner
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“…optogenetic stimulation of serotonergic neurons in the DRN in this study contrast with the results from an earlier study showing that optogenetic stimulation of BNST-projecting serotonergic neurons in the DRN modulates anxiety levels, and does not affect locomotion (Marcinkiewcz et al., 2016).”
The central amygdala recruits mesocorticolimbic circuitry for pursuit of reward or pain
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Neuronal diversity of the amygdala and the bed nucleus of the stria terminalis
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“Chemogenetic inhibition of the CRF neurons in the BNSTOV prevents this effect (Marcinkiewcz et al., 2016).”
BackgroundShuto, T., Kuroiwa, M., Sotogaku, N., Kawahara, Y., Oh, Y., Jang, J.-H., Shin, C.-H., Ohnishi, Y. N., Hanada, Y., Miyakawa, T., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0316-x · Cited by 66 · see citing works
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Transient and sustained effects of dopamine and serotonin signaling in motivation‐related behavior
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“In the bed nucleus of the stria terminalis, non-projecting and corticotropin-releasing-factorexpressing neurons exhibited transient depolarization following serotonin application and reverted to the baseline following the discontinuation of the application within a few minutes.(56) Activation of Gscoupled receptors al…”
BackgroundLuchsinger, J. R., Fetterly, T. L., Williford, K. M., Salimando, G. J., Doyle, M. A., Maldonado, J. A., Simerly, R. B., Winder, D. G., & Centanni, S. W. (2021) · Nature Communications · doi:10.1038/s41467-021-23674-z · Cited by 61 · see citing works
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“The inhibitory circuit of corticotropin-releasing factor neurons in the bed nucleus of the stria terminalis may contribute to the aversive behavior following acute exposure to SSRIs (58).”
BackgroundMelatonin as a Potential Approach to Anxiety Treatment
Repova, K., Baka, T., Krajcirovicova, K., Stanko, P., Aziriova, S., Reiter, R. J., & Šimko, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232416187 · Cited by 66 · see citing works
“, the sleep–wake cycle, emotions, stress reaction) [86].”
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“We focused in particular on those cells expressing the stress-related peptide CRF, as this population has been previously implicated in the regulation of emotional behaviors (Sink et al., 2013; Silberman and Winder, 2013; Pleil et al., 2015; Marcinkiewcz et al., 2016; Fetterly et al., 2019).”
BackgroundFrom Engrams to Pathologies of the Brain
Denny, C. A., Lebois, E. P., & Ramirez, S. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00023 · Cited by 64 · see citing works
“What role do neuromodulators play in changing the molecular and physiological properties of engram cells (Marcinkiewcz et al., 2016)?”
BackgroundJaneček, M., & Dabrowska, J. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2889-8 · Cited by 61 · see citing works
“Similarly, selective serotonin reuptake inhibitors enhance cued fear, an effect mediated by BNST neurons expressing serotonin 5-HT2C receptors (Ravinder et al. 2013; Marcinkiewcz et al. 2016; Pelrine et al. 2016).”
A discrete serotonergic circuit regulates vulnerability to social stress
Zou, W.-J., Song, Y., Wu, M., Chen, X.-T., You, Q.-L., Yang, Q., Luo, Z.-Y., Huang, L., Kong, Y., Feng, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18010-w · Cited by 57 · see citing works
Pati, D., Marcinkiewcz, C. A., DiBerto, J. F., Cogan, E. S., McElligott, Z. A., & Kash, T. L. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107759 · Cited by 59 · see citing works
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“Oppositely, optogenetic activation at higher power of a DR projection to the ventral BNST activates (via excitatory 5-HT2C receptors) an anxiogenic CRH neurons that silence anxiolytic BNST output neurons (Marcinkiewcz et al., 2016).”
Quantitative positron emission tomography in brain research
Heurling, K., Leuzy, A., Jonasson, M., Frick, A., Zimmer, E. R., Nordberg, A. K., & Lubberink, M. (2017) · Brain Research · doi:10.1016/j.brainres.2017.06.022 · Cited by 56 · see citing works
Role of the Bed Nucleus of the Stria Terminalis in PTSD: Insights From Preclinical Models
Miles, O. W., & Maren, S. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00068 · Cited by 57 · see citing works
“Indeed, exposure to an aversive event, in general, has been shown to activate or modify BNST signaling (Daniel and Rainnie, 2016; Marcinkiewcz et al., 2016; Rainnie et al., 2017) but with very little uniformity.”
BackgroundCircuit-Based Biomarkers for Mood and Anxiety Disorders
Xia, F., & Kheirbek, M. A. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.08.004 · Cited by 53 · see citing works
“Inhibition of vHPC–LHA projections in mice increases open arm exploration in the EPM, while modulation of vHPC–amygdala projections has no effect on anxiety, but modulates learned fear [29].”
BackgroundInfluentialHu, P., Maita, I., Phan, M. L., Gu, E., Kwok, C., Dieterich, A., Gergues, M. M., Yohn, C. N., Wang, Y., Zhou, J.-N., et al. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01070-3 · Cited by 49 · see citing works
“Importantly, the BNST is a critical node of the avoidance circuitry 90 , which has mutual projections to the central amygdala 53 , PVN 91 , ventral tegmental area (VTA) 92 and lateral hypothalamus 93 , whereas it further receives input from the ventral subiculum 94 that is involved in HPA-negative…”
BackgroundRadley, J. J., & Johnson, S. B. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.12.005 · Cited by 52 · see citing works
“…from its dorsal counterpart. avBST involvement in anxietylike behaviors has been demonstrated (Glangetas et al., 2017; Jennings et al., 2013; Marcinkiewcz et al., 2016), but both the intrinsic connectivity between dorsal and ventral BST, and comorbidity of anxiety and depression disorders…”
BackgroundNeurobiology of alcohol seeking behavior
Domi, E., Domi, A., Adermark, L., Heilig, M. A., & Augier, E. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15343 · Cited by 53 · see citing works
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“Neural circuits in the amygdala (a prominent site of 5-HT 2C R expression) play a critical role in linking fear processing and defensive responses (freeze/flight) 43,46 , which enable a rapid response to a natural predator, promoting survival.”
de Lima, R. M. S., Bento, L. V. D. S., Lugon, M. D. M. V., Baraúna, V. G., Bittencourt, A. S., Dalmaz, C., & Bittencourt, A. P. S. D. V. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112399 · Cited by 50 · see citing works
Miles, O. W., Thrailkill, E. A., Linden, A. K., May, V., Bouton, M. E., & Hammack, S. E. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.135 · Cited by 46 · see citing works
“Upstream PACAP release could enhance the excitability of BNST CRH neurons to promote CRH release independent of changes in transcript, but it may also be possible that BNST PACAP targets a specific population of CRH neurons (Marcinkiewcz et al, 2016).”
BackgroundFetterly, T. L., Basu, A., Nabit, B. P., Awad, E. K., Williford, K. M., Centanni, S. W., Matthews, R. T., Silberman, Y., & Winder, D. G. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1035-18.2018 · Cited by 48 · see citing works
“Serotonin is known to play a role in promoting anxiety and can activate CRF neurons (Marcinkiewcz et al., 2016).”
BackgroundEwin, S. E., Morgan, J. W., Niere, F., McMullen, N. P., Barth, S. H., Almonte, A. G., Raab‐Graham, K. F., & Weiner, J. L. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.028 · Cited by 45 · see citing works
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In vivo electrophysiological recordings of the effects of antidepressant drugs
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“Furthermore, the BNST is known to regulate feeding, fear, anxiety‐, and reward‐like behaviors via projections to the VTA and LH.(31,32,46) In male rodents, spontaneous and naloxone‐precipitated withdrawal inhibits activity of VTA dopamine neurons(13,20) and hence reduces dopamine release in the nucleus accumbens.”
BackgroundDetection of a High-Turnover Serotonin Circuit in the Mouse Brain Using Mass Spectrometry Imaging
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Median and Dorsal Raphe Serotonergic Neurons Control Moderate Versus Compulsive Cocaine Intake
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“Serotonergic signaling in the BNST activates local CRF-expressing neurons (22) and mediates the anxiety-like state associated with withdrawal from chronic intermittent ethanol exposure (62, 63).”
BackgroundTMEM16A expression in cholinergic neurons of the medial habenula mediates anxiety‐related behaviors
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“The serotonin circuits, including the dorsal raphe nucleus (DRN) and bed nucleus of the stria terminalis, have also been implicated in anxiety-related disorders [3].”
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“area and the lateral hypothalamus (Marcinkiewcz et al., 2016; Pati et al., 2019).”
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Cell-type diversity in the bed nucleus of the stria terminalis to regulate motivated behaviors
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- 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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