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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Endocrinology and the brain: corticotropin-releasing hormone signaling
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Social isolation stress in adolescence, but not adulthood, produces hypersocial behavior in adult male and female C57BL/6J mice
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The role of dopamine in overcoming aversion with exercise
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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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“Chemogenetic inhibition of the CRF neurons in the BNSTOV prevents this effect (Marcinkiewcz et al., 2016).”
Background
Obligatory roles of dopamine D1 receptors in the dentate gyrus in antidepressant actions of a selective serotonin reuptake inhibitor, fluoxetine
Shuto, 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 64
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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…”
Background
Delineation of an insula-BNST circuit engaged by struggling behavior that regulates avoidance in mice
Luchsinger, 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 64
Risk of Suicidal Behaviors and Antidepressant Exposure Among Children and Adolescents: A Meta-Analysis of Observational Studies
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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).”
Background
Melatonin 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 70
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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).”
Background
From 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 65
“What role do neuromodulators play in changing the molecular and physiological properties of engram cells (Marcinkiewcz et al., 2016)?”
Background
Oxytocin facilitates adaptive fear and attenuates anxiety responses in animal models and human studies—potential interaction with the corticotropin-releasing factor (CRF) system in the bed nucleus of the stria terminalis (BNST)
Janeček, M., & Dabrowska, J. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2889-8 · Cited by 63
“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
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Chronic intermittent ethanol exposure dysregulates a GABAergic microcircuit in the bed nucleus of the stria terminalis
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
Self-citation
Overcoming Resistance to Selective Serotonin Reuptake Inhibitors: Targeting Serotonin, Serotonin-1A Receptors and Adult Neuroplasticity
Vahid-Ansari, F., Zhang, M., Zahrai, A., & Albert, P. R. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00404 · Cited by 59
“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
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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 59
“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.”
Background
Circuit-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 56
“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].”
BackgroundInfluential
Early-life stress alters affective behaviors in adult mice through persistent activation of CRH-BDNF signaling in the oval bed nucleus of the stria terminalis
Hu, 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
“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…”
Background
Anteroventral bed nuclei of the stria terminalis neurocircuitry: Towards an integration of HPA axis modulation with coping behaviors - Curt Richter Award Paper 2017
Radley, J. J., & Johnson, S. B. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.12.005 · Cited by 57
“…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…”
Background
Neurobiology 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
Human loss-of-function variants in the serotonin 2C receptor associated with obesity and maladaptive behavior
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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.”
Early life stress and the programming of eating behavior and anxiety: Sex-specific relationships with serotonergic activity and hypothalamic neuropeptides
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
Pituitary Adenylate Cyclase-Activating Peptide in the Bed Nucleus of the Stria Terminalis Mediates Stress-Induced Reinstatement of Cocaine Seeking in Rats
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 47
“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).”
Background
α2A-Adrenergic Receptor Activation Decreases Parabrachial Nucleus Excitatory Drive onto BNST CRF Neurons and Reduces Their ActivityIn Vivo
Fetterly, 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 50
“Serotonin is known to play a role in promoting anxiety and can activate CRF neurons (Marcinkiewcz et al., 2016).”
Background
Chronic Intermittent Ethanol Exposure Selectively Increases Synaptic Excitability in the Ventral Domain of the Rat Hippocampus
Ewin, 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
Overview on brain function enhancement of Internet addicts through exercise intervention: based on reward-execution-decision cycle
Chen, H., Dong, G., & Li, K. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1094583 · Cited by 47
A neural circuit associated with anxiety‐like behaviors induced by chronic inflammatory pain and the anxiolytic effects of electroacupuncture
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Inhibitory transmission in the bed nucleus of the stria terminalis in male and female mice following morphine withdrawal
Luster, B. R., Cogan, E. S., Schmidt, K. T., Pati, D., Pina, M. M., Dange, K., & McElligott, Z. A. (2019) · Addiction Biology · doi:10.1111/adb.12748 · Cited by 45
“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.”
Background
Detection of a High-Turnover Serotonin Circuit in the Mouse Brain Using Mass Spectrometry Imaging
Sugiyama, E., Guerrini, M. M., Honda, K., Hattori, Y., Abe, M., Källback, P., Andrén, P. E., Tanaka, K. F., Setou, M., Fagarasan, S., et al. (2019) · iScience · doi:10.1016/j.isci.2019.09.036 · Cited by 45
Extended Amygdala Neuropeptide Circuitry of Emotional Arousal: Waking Up on the Wrong Side of the Bed Nuclei of Stria Terminalis
Giardino, W. J., & Pomrenze, M. B. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.613025 · Cited by 48
Agomelatine for the treatment of generalized anxiety disorder: focus on its distinctive mechanism of action
Millan, M. J. (2022) · Therapeutic Advances in Psychopharmacology · doi:10.1177/20451253221105128 · Cited by 48
Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice
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. (2023) · Nature Communications · doi:10.1038/s41467-023-36808-2 · Cited by 50
Oxytocin receptor neurotransmission in the dorsolateral bed nucleus of the stria terminalis facilitates the acquisition of cued fear in the fear-potentiated startle paradigm in rats
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Median and Dorsal Raphe Serotonergic Neurons Control Moderate Versus Compulsive Cocaine Intake
Verheij, M. M. M., Contet, C., Karel, P., Latour, J., van der Doelen, R. H. A., Geenen, B., van Hulten, J. A., Meyer, F., Kozicz, T., George, O., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.031 · Cited by 44
“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).”
Background
TMEM16A expression in cholinergic neurons of the medial habenula mediates anxiety‐related behaviors
Cho, C., Lee, S.-J., Kim, A., Yarishkin, O. V., Ryoo, K., Lee, Y., Jung, H., Yang, E., Lee, D. Y., Lee, B., et al. (2019) · EMBO Reports · doi:10.15252/embr.201948097 · Cited by 43
“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].”
The altered sensitivity of acute stress induced anxiety-related behaviors by modulating insular cortex-paraventricular thalamus-bed nucleus of the stria terminalis neural circuit
Zhao, D., Wang, D., Wang, W., Dai, J., Cui, M., Wu, M., Liu, C., Liu, J., Meng, F., Wang, K., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105890 · Cited by 44
Forced Abstinence From Alcohol Induces Sex-Specific Depression-Like Behavioral and Neural Adaptations in Somatostatin Neurons in Cortical and Amygdalar Regions
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“area and the lateral hypothalamus (Marcinkiewcz et al., 2016; Pati et al., 2019).”
Distinct circuits in rat central amygdala for defensive behaviors evoked by socially signaled imminent versus remote danger
Andraka, K., Kondrakiewicz, K., Rojek-Sito, K., Ziegart-Sadowska, K., Meyza, K. Z., Nikolaev, T., Hamed, A., Kursa, M. B., Wójcik, M., Danielewski, K., et al. (2021) · Current Biology · doi:10.1016/j.cub.2021.03.047 · Cited by 46
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: 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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