Cited by 457Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

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Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala

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Marcinkiewcz, Catherine A., Mazzone, Christopher M., D’Agostino, Giuseppe, Halladay, Lindsay R., Hardaway, J. Andrew, DiBerto, Jeffrey F., Navarro, Montserrat, Burnham, Nathan, Cristiano, Claudia, Dorrier, Cayce E., Tipton, Gregory J., Ramakrishnan, Charu, Kozicz, Tamas, Deisseroth, Karl, Thiele, Todd E., McElligott, Zoe A., Holmes, Andrew, Heisler, Lora K., Kash, Thomas L.·2016·Nature

DOI 10.1038/nature19318PMC PMC5124365

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Abstract

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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MethodInfluential
Retracted
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A BIBLIOMETRIC ANALYSIS OF HUMAN HORMONES IN CONSUMER NEUROSCIENCE AND HUMAN BEHAVIOR RESEARCH: TRENDS AND INSIGHTS WITH IMPLICATIONS FOR MARKETING
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Rooibos (Aspalathus linearis) alters secretome trace amine profile of probiotic and commensal microbes in vitro
Pretorius, L., Staden, A. D. P. V., Kellermann, T. A., Henning, N., & Smith, C. (2022) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2022.115548 · Cited by 10
Sex differences in BNST signaling and BNST CRF in fear processingPreprint
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“BNST CRF neurons project both locally and out of the BNST ( Marcinkiewcz et al., 2016 ; Pati et al., 2020 ), which may indicate that CRF signaling within the BNST versus in target regions of BNST CRF differentially alters acoustic startle reflex.”
Influential
Prefrontal–bed nucleus of the stria terminalis physiological and neuropsychological biomarkers predict therapeutic outcomes in depression
Wang, L., Zhang, Y., Wang, Y., Ding, Q., Dai, L., Hu, K., Ye, K., lv, X., Zhang, X., Mandali, A., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65179-z · Cited by 11
“The BNST acts as an integrated station to orchestrate divergent motivational, arousal, and emotional states 16,17,20 .”
Amygdalar activity measured using FDG-PET/CT at head and neck cancer staging independently predicts survival
Hassan, M. Z. O., Tawakol, A. A., Wang, Y., Alvi, R. M., Awadalla, M., Jones‐O’Connor, M., Bakar, R. B., Banerji, D., Rokicki, A., Zhang, L., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0279235 · Cited by 10
Role of 5-hydroxytryptamine type 3 receptors in the regulation of anxiety reactions
Du, Y., Li, Z., Zhao, Y., Han, J., Hu, W., & Liu, Z. (2024) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2200642 · Cited by 9
“…nucleus (MRN) using optogenetic methods has induced obvi ‐ ous anxiety reactions, including novelty suppressed feeding (NSF), marble-burying behavior (MBB), and elevated-plus maze (EPM), in several emotional be ‐ havior tests (Challis et al., 2014; Marcinkiewcz et al., 2016; Abela et al., 2020).”
Neural Circuits for Fear Relapse
Goode, T. D., Jin, J., & Maren, S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00010-1 · Cited by 10
Pharmacological and Physiological Correlates of the Bidirectional Fear Phenotype of the Carioca Rats and Other Bidirectionally Selected Lines
Lages, Y., Balthazar, L., Krahe, T. E., & Landeira-Fernández, J. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666221012121534 · Cited by 9
Serotonin modulates social responses to stressed conspecifics via insular 5-HT 2C receptors in rat
Ng, A. J., Vincelette, L. K., Li, J., Brady, B. H., & Christianson, J. P. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109598 · Cited by 9
“Most of 5-HT’s anxiety-producing effects can be attributed to 5-HT2C receptors (Drago & Serretti, 2009; Heisler et al., 2007; Marcinkiewcz et al., 2016), which are found throughout the forebrain (Clemett et al.”
Background
Serotonin neurons in mating female mice are activated by male ejaculation
Troconis, E. L., Seo, C., Guru, A., & Warden, M. R. (2023) · Current Biology · doi:10.1016/j.cub.2023.09.071 · Cited by 10
Bed Nucleus of the Stria Terminalis (BNST) neurons containing the serotonin 5HT2c receptor modulate operant alcohol self-administration behavior in mice
Flanigan, M. E., Gianessi, C. A., Castle, M., Dorlean, W., Sides, T. R., & Kash, T. L. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01753-7 · Cited by 8
“5HT circuitry is extensive throughout the brain, posing a challenge with isolating the contributions of speci ﬁ c brain regions to alcohol-related behaviors (Marcinkiewcz et al., 2016).”
Identification of a novel perifornical-hypothalamic-area-projecting serotonergic system that inhibits innate panic and conditioned fear responses
Bernabe, C., Caliman, I., de Abreu, A. D., Molosh, A., Truitt, W., Shekhar, A., & Johnson, P. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02769-3 · Cited by 8
“The stimulation parameters (470nm, 20 Hz, 10 mW, 5-ms pulses, 5 min) were chosen based on in vitro and in vivo DR neuronal ﬁ ring patterns and serotonin release in rodents [45, 46].”
Method
Disentangling the effects of corticotrophin releasing factor and GABA release from the bed nucleus of the stria terminalis on ethanol self-administration in mice
Gianessi, C. A., Haun, H. L., Pati, D., Sides, T. R., D’Ambrosio, S., Kelson, W. P., Hernandez, R., Gereau, G. B., Boyt, K. M., Hodge, C. W., et al. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02192-2 · Cited by 12
“…lever responding across days for effects of sex and virus, there was a signi ﬁ cant main effect of virus (Wald χ 2 (1) = 22.0, p 0.0001), a signi ﬁ cant sex-by-virus interaction (Wald χ 2 (1) = 9.0, p = 0.003), and a signi ﬁ cant sex-by-virus-by-day interaction (Wald χ 2 (8) = 15.3, p = 0.05).”
Influential
CRH Neurons in the Laterodorsal Tegmentum Mediate Acute Stress-induced Anxiety
Tang, W., Zhou, D., Wang, S., Hao, S., Wang, X., Helmy, M., Zhu, J., & Wang, H. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00684-x · Cited by 10
Exercise reduces the anxiogenic effects of meta-chlorophenylpiperazine: The role of 5-HT2C receptors in the bed nucleus of the stria terminalis
Fox, J. H., Boucher, M. N., Abedrabbo, K. S., Hare, B. D., Grimmig, B. A., Falls, W. A., & Hammack, S. E. (2023) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.1067420 · Cited by 9
“Moreover, we have observed significant enhancement in baseline startle responding following both systemic and intra-BNST mCPP administration (Fox et al., 2008; Marcinkiewcz et al., 2016); hence, acoustic startle responding was implemented as the primary behavioral measure in the present report.”
BackgroundMethodInfluential
Coordinated excitatory and inhibitory circuits governing unpredictable threat-induced anxiety
Teng, S.-W., Wang, X., Yao, Z.-X., He, T., Gao, M.-Y., Che, Y.-Y., Wei, X.-Y., Chen, X.-L., Liu, C., & Chen, Z.-Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115146 · Cited by 9
S1PR3 in hippocampal neurons improves synaptic plasticity and decreases depressive behavior via downregulation of RhoA/ROCK1
Liu, H., Chen, S., Hong, X., Xiao, J., Zhao, S., Zhang, X., Shu, Z., Zhang, J., Ouyang, J., Liu, Q., et al. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111256 · Cited by 8
Salient safety conditioning improves novel discrimination learning
Nahmoud, I., Vasquez, J. G., Cho, H., Dennis‐Tiwary, T. A., & Likhtik, E. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112907 · Cited by 10
The Role of Dorsal Raphe Nucleus Serotonergic Systems in Emotional Learning and Memory in Male BALB/c Mice
Payet, J. M., Stevens, L., Russo, A. M., Jaehne, E. J., van den Buuse, M., Kent, S., Lowry, C. A., Baratta, M. V., & Hale, M. W. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.10.003 · Cited by 9
Amygdalostriatal transition zone neurons encode sustained cue responses to guide defensive behaviors
Mills, F., Lee, C. R., Howe, J. R., Li, H., Keisler, M. N., Shao, S., Taschbach, F., Lemieux, M., Aloboudi, F., White, J., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.012 · Cited by 10
Cisplatin Inhibits Neurotransmitter Release during Exocytosis from Single Chromaffin Cells Monitored with Single Cell Amperometry
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Involvement of DR→mPFC 5-HTergic neural projections in changes of social exploration behaviors caused by adult chronic social isolation in mice
Lv, Z., Zhang, Y., Zhang, L., Hou, W., Lin, M., Xun, Y., Ma, H., Li, Y., Li, Y., Tai, F., et al. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.04.016 · Cited by 8
Inhibitory synaptic transmissions to the bed nucleus of the stria terminalis neurons projecting to the ventral tegmental area are enhanced in rats exposed to chronic mild stress
Hara, R., Takahashi, D., Takehara, T., Amano, T., & Minami, M. (2020) · Molecular Brain · doi:10.1186/s13041-020-00684-4 · Cited by 8
Pathophysiological and therapeutic implications of neuropeptide S system in neurological disorders
Shirasath, K. R., Patil, V. K., Awathale, S. N., Goyal, S. N., & Nakhate, K. T. (2024) · Peptides · doi:10.1016/j.peptides.2024.171167 · Cited by 9
Behavioral and Neurophysiological Implications of Pathological Human Tau Expression in Serotonin Neurons
Khan, N. S., Isaza, J. U., Rouhi, N., Jamani, N. F., Jabeen, S., Gill, A. K., Tsutsui, M., Visser, F., & Sargin, D. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00626 · Cited by 8
The regulative role and mechanism of BNST in anxiety disorder
Xie, M., Xiong, Y., & Wang, H. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1437476 · Cited by 7
A cell-type-specific circuit of somatostatin neurons in the habenula encodes antidepressant action in male mice
Luo, L., Jing, W., Guo, Y., Liu, D., He, A., & Lu, Y. (2025) · Nature Communications · doi:10.1038/s41467-025-58591-y · Cited by 8
“Dopaminergic neurons in the dorsal raphe nucleus and VTA send out signals that are received by excitatory glutamatergic neurons in the BNST 38,39 , which are known to play crucial roles in the onset and manifestation of depression-like behaviors, and following anti-depressant treatments 40,41 .”
Peri-ictal activation of dorsomedial dorsal raphe serotonin neurons reduces mortality associated with maximal electroshock seizures
Petrucci, A. N., Jones, A. R., Kreitlow, B. L., & Buchanan, G. F. (2024) · Brain Communications · doi:10.1093/braincomms/fcae052 · Cited by 7
“64,75 Our preliminary staining also indicates the presence of the 5-HT 2A receptor on CRH containing neurons within the anterior-dorsal subcom-partment of the BNST, but not in the anterior-ventral region (Fig.”
Background
Deciphering the Functions of Raphe–Hippocampal Serotonergic and Glutamatergic Circuits and Their Deficits in Alzheimer’s Disease
Yu, W., Zhang, R., Zhang, A., & Mei, Y. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031234 · Cited by 7
“It is well established that DRN 5-HT neurons play a pivotal role in regulating anxiety behavior through their projections to emotion-related nuclei, such as amygdala [32,101], bed nucleus of the stria terminals [102], and vHP [69].”
Prior stress and vasopressin promote corticotropin-releasing factor inhibition of serotonin release in the central nucleus of the amygdala
Ronan, P. J., Korzan, W. J., Johnson, P. L., Lowry, C. A., Renner, K. J., & Summers, C. H. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1148292 · Cited by 7
Anatomical, Physiological, and Functional Heterogeneity of the Dorsal Raphe Serotonin SystemPreprint
Ren, J., Friedmann, D., Xiong, J., Liu, C. D., DeLoach, K. E., Chen, R., Pu, A., Sun, Y., Weissbourd, B., Neve, R. L., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/257378 · Cited by 7
“Fos immunoreactivity is significantly elevated in DRSert→BNST neurons after foot-shock, and optogenetic stimulation of serotonergic terminals in BNST promotes anxiety-like behavior and fear learning (Marcinkiewcz et al., 2016).”
BackgroundInfluential
Bed nucleus of the stria terminalis regulates fear to unpredictable threat signalsPreprint
Goode, T. D., Ressler, R. L., Acca, G. M., Miles, O. W., & Maren, S. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/376228 · Cited by 8
“Increases in immediate early gene expression, metabolic activity, and changes in electrophysiological firing patterns have been observed in the BNST in response to direct exposure to conditioned contextual cues (Campeau et al., 1997; Daldrup et al., 2016; Jennings et al., 2013; Lemos et al., 2010; Luyten et al., 2012;…”
Excessive energy expenditure due to acute physical restraint disrupts Drosophila motivational feeding response
Gordon, J., & Masek, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-03575-3 · Cited by 6
Exploring the effects of adolescent social isolation stress on the serotonin system and ethanol-motivated behaviors
McElroy, B. D., Li, C., McCloskey, N. S., Alberici, A. R., & Kirby, L. G. (2025) · Psychopharmacology · doi:10.1007/s00213-025-06749-3 · Cited by 6
“There is a large body of evidence that consistently shows that both chronic stress and excessive alcohol consumption have an inverse relationship with 5-HT (LeMarquand et al. 1994a, b; Marcinkiewcz 2015; Marcinkiewcz et al. 2016).”
Integrated single-cell atlases unveil the operation principles of whole-brain 5-HT neuronal subsystems
Song, Z., Huang, C.-X., Zhang, H., Ye, C., Guan, N. N., & Song, J. (2025) · Science Advances · doi:10.1126/sciadv.adv8128 · Cited by 9
Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) of the Bed Nucleus of the Stria Terminalis Mediates Heavy Alcohol Drinking in Mice
Lepeak, L., Miracle, S. A., Ferragud, A., Seiglie, M. P., Shafique, S., Öztürk, Z., Minnig, M. A., Medeiros, G., Cottone, P., & Sabino, V. (2023) · eNeuro · doi:10.1523/eneuro.0424-23.2023 · Cited by 6
Structural Conversion of Serotonin into Amyloid-like Nanoassemblies Conceptualizes an Unexplored Neurotoxicity Risk
Prajapati, K. P., Mittal, S., Ansari, M., Mishra, N., Mahato, O. P., Tiku, A. B., Anand, B. G., & Kar, K. (2024) · ACS Nano · doi:10.1021/acsnano.4c09522 · Cited by 6
Dorsal raphe GABA-ergic neurons regulate the susceptibility to social transfer of pain in mice
Ai, L., Han, Y., Ge, T., Sha, S., Zhai, X., Ji, R., Zhou, Y., Chen, D., Xie, A., Zhang, W., et al. (2025) · Acta Pharmacologica Sinica · doi:10.1038/s41401-025-01494-x · Cited by 6
Slow motion
Uchida, N., & Cohen, J. Y. (2017) · eLife · doi:10.7554/elife.24792 · Cited by 6
Effects of Jian-Pi-Zhi-Dong Decoction on the Expression of 5-HT and Its Receptor in a Rat Model of Tourette Syndrome and Comorbid Anxiety
Wang, D., Tian, H., Cui, X., Wang, Q., Guo, F., Zhang, W., & Tang, Q.-S. (2020) · Medical Science Monitor · doi:10.12659/msm.924658 · Cited by 6
“A large number of studies have shown that 5-HT metabolic abnormalities play important role in the pathophysiological mechanism of TS [26], anxiety disorders [27], ADHD [28], OCD [29,30] and other mental behavior disorders.”
Background
Selective serotonin reuptake inhibition increases noise burst-induced unconditioned and context-conditioned freezing
Hagsäter, S. M., Thorén, J., Pettersson, R., & Eriksson, E. (2018) · Acta Neuropsychiatrica · doi:10.1017/neu.2018.26 · Cited by 6
Probing the association between serotonin-1A autoreceptor binding and amygdala reactivity in healthy volunteers
Kranz, G. S., Hahn, A., Kraus, C., Spies, M., Pichler, V., Jungwirth, J., Mitterhauser, M., Wadsak, W., Windischberger, C., Kasper, S. F., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.12.092 · Cited by 6
Serotonin Subsystems Modulate Diverse and Opposite Behavioral Functions
Garcia‐García, Á. L., & Soiza‐Reilly, M. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00534 · Cited by 6
Brain-wide electrical dynamics encode an appetitive socioemotional statePreprint
Mague, S. D., Talbot, A., Blount, C., Duffney, L. J., Walder-Christensen, K. K., Adamson, E., Bey, A. L., Ndubuizu, N., Thomas, G. E., Hughes, D. N., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.01.181347 · Cited by 8
“The time that mice spend in the open arms of the maze is increased by myriad anxiolytic manipulations and decreased by anxiogenic manipulations (Krishnan et al., 2007; Marcinkiewcz et al., 2016; Rodgers et al., 1992).”
Background
Optogenetic activation of dorsal raphe serotonin neurons induces brain-wide activationPreprint
Hamada, H. T., Abe, Y., Takata, N., Taira, M., Tanaka, K. F., & Doya, K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.07.503074 · Cited by 7

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: Marcinkiewcz, Catherine A.
D’Agostino, Giuseppe
Halladay, Lindsay R.
DiBerto, Jeffrey F.
Navarro, Montserrat
Cristiano, Claudia
Ramakrishnan, Charu
Deisseroth, Karl
Thiele, Todd E.
Heisler, Lora K.
Kash, Thomas L.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2016-08-24
Volume: 537
Issue: 7618
Pages: 97-101
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature19318
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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Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala

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