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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Background
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Background
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Background
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“The elevated plus maze test has been performed as described by Marcinkiewcz et al., 2016.”
Method
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Influential
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Background
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Background
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“30 Moreover, serotonin activates the HPA axis and contributes to anxiety.(31)”
Background
The Relationship Between 5-Hydroxytryptamine and Its Metabolite Changes With Post-stroke Depression
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“…have reported that ovBNST CRF neurons are involved in distress-related circuits and could produce aversive effects in both female and male mice ( 37 , 38 ), it has not been demonstrated whether there are preexisting differences in ovBNST CRF neural activities driving sex differential…”
Background
Crh receptor priming in the bed nucleus of the stria terminalis (BNST) induces tph2 gene expression in the dorsomedial dorsal raphe nucleus and chronic anxiety
Donner, N. C., Davies, S. M., Fitz, S. D., Kienzle, D. M., Shekhar, A., & Lowry, C. A. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109730 · Cited by 28
“Conversely, serotonergic projections from the DR to BNST Crh-expressing neurons, through activation of 5-HT2C receptors, promote development of an anxiety-like state (Marcinkiewcz et al., 2016).”
Background
Mu Opioid Receptor–Expressing Neurons in the Dorsal Raphe Nucleus Are Involved in Reward Processing and Affective Behaviors
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“…physiology, and function in mice revealed two functionally heterogenous DRN 5-HT subgroups with one projecting to amygdala promoting anxiety-like behavior 17,26 and the other projecting to frontal cortex innervating neurons responsible for locomotor restriction in the face of challenges 17 .”
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“For example, while chemogenetic activation of DRN neurons projecting to the orbitofrontal cortex (OFC) or CeA decreases locomotion, photoactivation of BNST-projecting DRN neurons does not affect locomotion, and photoactivation of the overlapping DRN neurons in both normal-weight and obese mice increases locomotion [23…”
Background
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“…combined transgenic and retrograde virus delivery of recombinases to target neurons based on genetic and topological characteristics; in this case (Marcinkiewcz et al., 2016) Con/FoffChR2-YFP was used, thereby excluding expression of ChR2-YFP from cells expressing a certain gene AND projecting to…”
Method
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“These studies suggest that one of the serotonin receptors, probably receptor 2C (5-HTR2C) is the pSAg of anxiety (129).”
Background
CRF modulation of central monoaminergic function: Implications for sex differences in alcohol drinking and anxiety
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Background
Cooperative CRF and α1 Adrenergic Signaling in the VTA Promotes NMDA Plasticity and Drives Social Stress Enhancement of Cocaine Conditioning
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“The VTA receives several CRF inputs, some of which originate in the bed nucleus of the stria terminalis, central amygdala, and hypothalamus (Marcinkiewcz et al., 2016; Rinker et al., 2017; Rodaros et al., 2007).”
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Self-citation
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“In rodents, decades of fear-conditioning and threat-related studies have built a foundation for investigating threat processing and have been instrumental to the formulation, testing, and refinement of hypotheses regarding individual responses of the Ce and BST to phasic and sustained threats (Davis et al., 2010; Walk…”
Background
Serotonin and Depression: Scrutiny of New Targets for Future Anti- Depressant Drug Development
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“The negative glucocorticoid response element (nGRE) on the human CRF promoter [38, 39] is located between nt − 278 to − 249, whose deletion resulted in complete loss of dexamethasone (DEX)-mediated CRF repression [13].”
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Luo, P. X., Manning, C., Fass, J. N., Williams, A. V., Hao, R., Campi, K. L., & Trainor, B. C. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113084 · Cited by 24
Control of Emotion and Wakefulness by Neurotensinergic Neurons in the Parabrachial Nucleus
Chen, J., Gannot, N., Li, X., Zhu, R., Zhang, C., & Li, P. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00994-8 · Cited by 24
“Activation of NtsPBN neurons by optogenetics and chemogenetics is sufficient to induce freezing and anxiety-like behaviors, which is consistent with their robust projection to the limbic system, including the CeA and the BNST, which are essential in the control of fear and anxiety [4, 42, 44, 47, 48].”
Background
A circuit of COCH neurons encodes social-stress-induced anxiety via MTF1 activation of Cacna1h
Jing, W., Zhang, T., Liu, J., Huang, X., Yu, Q., Yu, H., Zhang, Q., Li, H., Deng, M., Zhu, L., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110177 · Cited by 25
Concurrent anxiety in patients with major depression and cerebral serotonin 4 receptor binding. A NeuroPharm-1 study
Köhler‐Forsberg, K., Ozenne, B., Larsen, S. V., Poulsen, A. S., Landman, E. B., Dam, V. H., Ip, C.-T., Jørgensen, A., Svarer, C., Knudsen, G. M., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02034-5 · Cited by 26
“Intriguingly, if 5-HT4R is an inverse proxy for cerebral 5-HT levels [22, 38], our observations suggest that high anxiety levels in depression are associated with higher-thannormal brain 5-HT levels and may correspond to the observation of serotonin-increase caused engagement of anxiety and fearpromoting circuit in th…”
Background
Dorsal raphe serotonergic neurons suppress feeding through redundant forebrain circuits
Aklan, İ., Sayar, N., Deng, F., Kim, H., Yavuz, Y., Rysted, J., Laule, C. F., Davis, D., Li, Y., & Atasoy, D. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101676 · Cited by 24
“Alternatively, DRN / BNST input may promote hypophagia through stimulation of aversive state and anxiety [44].”
Background
Lacticaseibacillus rhamnosus KY16 Improves Depression by Promoting Intestinal Secretion of 5-HTP and Altering the Gut Microbiota
Xie, S., Wang, C., Song, J., Zhang, Y., Wang, H., Chen, X., & Suo, H. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c03870 · Cited by 27
Interactions between Sleep and Emotions in Humans and Animal Models
Lefter, R. M., Cojocariu, R. O., Ciobica, A. S., Balmuș, I.-M., Mavroudis, I. A., & Kis, A. (2022) · Medicina · doi:10.3390/medicina58020274 · Cited by 25
“Several studies showed that due to the fact that the REM stage is characterized by increased cholinergic activity and also lacks aminergic activity, in this stage the processing of emotional memories occurs [12,14,15].”
Background
Serotonin modulates an inhibitory input to the central amygdala from the ventral periaqueductal gray
Hon, O. J., DiBerto, J. F., Mazzone, C. M., Sugam, J. A., Bloodgood, D. W., Hardaway, J. A., Husain, M., Kendra, A. M., McCall, N. M., López, A. J., et al. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01392-4 · Cited by 23
“We showed previously that this concentration of 5HT and RS102221 are sufficient to significantly increase GABAergic transmission and to block 5HT2C-mediated depolarization in the extended amygdala, respectively [25].”
Background
Synaptic Plasticity in the Bed Nucleus of the Stria Terminalis: Underlying Mechanisms and Potential Ramifications for Reinstatement of Drug- and Alcohol-Seeking Behaviors
Harris, N. A., & Winder, D. G. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00169 · Cited by 22
The role of the bed nucleus of the stria terminalis in pain-induced aversive motivation
Minami, M. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.003 · Cited by 25
Characterization of the relaxin family peptide receptor 3 system in the mouse bed nucleus of the stria terminalis
Ch’ng, S. S., Fu, J., Brown, R. M., Smith, C. M., Hossain, M. A., McDougall, S. J., & Lawrence, A. J. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24695 · Cited by 23
“…(VTA); however, these pathways show divergent but complementary roles in drug consumption, conditioned reinforcement, and drug-seeking behavior (Briand et al., 2010; Buffalari & See, 2011; Jennings et al., 2013; Mahler & Aston-Jones, 2012; Marcinkiewcz et al., 2016; Sartor & Aston-Jones, 2012).”
Background
Bed nuclei of the stria terminalis modulate memory consolidation via glucocorticoid-dependent and -independent circuits
Lingg, R. T., Johnson, S. B., Emmons, E. B., Anderson, R. M., Romig‐Martin, S. A., Narayanan, N. S., McGaugh, J. L., LaLumiere, R. T., & Radley, J. J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915501117 · Cited by 26
Effect of 5-HT2C receptor agonist and antagonist on chronic unpredictable stress (CUS) - Mediated anxiety and depression in adolescent Wistar albino rat: Implicating serotonin and mitochondrial ETC-I function in serotonergic neurotransmission
Wankhar, W., Syiem, D., Pakyntein, C. L., Thabah, D., & Sunn, S. E. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112780 · Cited by 22
Phasic signaling in the bed nucleus of the stria terminalis during fear learning predicts within- and across-session cued fear expressionPreprint
Bjorni, M., Rovero, N. G., Yang, E. R., Holmes, A., & Halladay, L. R. (2020) · Learning & Memory · doi:10.1101/lm.050807.119 · Cited by 25
An in vitro screening method for probiotics with antidepressant-like effect using the enterochromaffin cell model
Tian, P., Zhu, H., Zou, R., Kong, Q., Xu, M., Zhao, J., Zhang, H., Chen, W., & Wang, G. (2021) · Food & Function · doi:10.1039/d0fo02307h · Cited by 22
Corticotropin releasing factor and norepinephrine related circuitry changes in the bed nucleus of the stria terminalis in stress and alcohol and substance use disorders
Snyder, A. E., & Silberman, Y. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108814 · Cited by 22
A Distinct Metabolically Defined Central Nucleus Circuit Bidirectionally Controls Anxiety-Related Behaviors
Ren, J., Lu, C.-L., Huang, J., Fan, J., Guo, F., Mo, J.-W., Huang, W.-Y., Kong, P.-L., Li, X.-W., Sun, L.-R., et al. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1578-21.2022 · Cited by 22
Flexible B, N co-doped graphene electrodes for electrochemical detection of serotonin in bodily fluids
Liu, Y., Li, M., Zhou, B., Xuan, X., & Li, H. (2023) · Electrochimica Acta · doi:10.1016/j.electacta.2023.142494 · Cited by 22
Tau pathology in the dorsal raphe may be a prodromal indicator of Alzheimer’s disease
Pierson, S. R., Fiock, K. L., Wang, R., Balasubramanian, N., Reinhardt, J., Khan, K. M., James, T. D., Hunter, M. L., Cooper, B. J., Williamsen, H. R., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02664-9 · Cited by 27
Projections from subfornical organ to bed nucleus of the stria terminalis modulate inflammation-induced anxiety-like behaviors in mice
Zhang, J., Xie, C., Xu, P., Tong, Q., Xiao, L., & Zhong, J. (2024) · Science Advances · doi:10.1126/sciadv.adp9413 · Cited by 21
“Using neural circuit tracing and chemogenetic techniques, we observed that SFO exerts its anxiolytic effect through glutamatergic projections to the bed nucleus of the stria terminalis (BNST), a well-known anxiety-related brain region ( 19 – 21 ).”
Comparison of neurotransmitter levels, physiological conditions, and emotional behavior between isolation‐housed rats with group‐housed rats
Kaneda, Y., Kawata, A., Suzuki, K., Matsunaga, D., Yasumatsu, M., & Ishiwata, T. (2020) · Developmental Psychobiology · doi:10.1002/dev.22036 · Cited by 21
Early response to trazodone once-a-day in major depressive disorder: review of the clinical data and putative mechanism for faster onset of action
Albert, U., Lamba, P., & Stahl, S. M. (2021) · CNS Spectrums · doi:10.1017/s1092852921000304 · Cited by 19
“It has been shown that serotonin release from the dorsal raphe nucleus enhances fear and anxiety through activation of 5-HT2C receptors on a subpopulation of corticotropin-releasing factor neurons.(76,77) Therefore, antagonism at 5-HT2C receptors along with trazodone’s action at other serotonergic receptors may potent…”
Background
Serotonin in panic and anxiety disorders
Zangrossi, H., Del‐Ben, C. M., Graeff, F. G., & Guimarães, F. S. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-444-64125-0.00036-0 · Cited by 25
Strategies for Targeting Neural Circuits: How to Manipulate Neurons Using Virus Vehicles
Hui, Y., Zheng, X., Zhang, H., Li, F., Yu, G., Li, J., Zhang, J., Gong, X., & Guo, G. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.882366 · Cited by 25
Chronic stress-induced synaptic changes to corticotropin-releasing factor-signaling in the bed nucleus of the stria terminalis
Maita, I., Roepke, T. A., & Samuels, B. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.903782 · Cited by 21
Chemogenetic manipulation of the bed nucleus of the stria terminalis counteracts social behavioral deficits induced by early life stress in C57BL/6J mice
Emmons, R., Sadok, T., Rovero, N. G., Belnap, M. A., Henderson, H. J. M., Quan, A., Toro, N. J. D., & Halladay, L. R. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24644 · Cited by 21
“…are activated in response to acute stressors (for review see Daniel & Rainnie, 2016), and activation or inhibition of BNST CRF neurons induces anxiogenic or anxiolytic effects, respectively (Kim et al., 2013; Lee & Davis, 1997; Marcinkiewcz et al., 2016; Pleil et al., 2015; Sahuque et al., 2006).”
Background
Interactions between maternal fluoxetine exposure, the maternal gut microbiome and fetal neurodevelopment in mice
Vuong, H. E., Coley, E. J. L., Kazantsev, M., Cooke, M. E., Rendon, T. K., Paramo, J., & Hsiao, E. Y. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113353 · Cited by 19
Stress decreases serotonin tone in the nucleus accumbens in male mice to promote aversion and potentiate cocaine preference via decreased stimulation of 5-HT1B receptors
Fontaine, H. M., Silva, P. R., Neiswanger, C., Tran, R., Abraham, A. D., Land, B. B., Neumaier, J. F., & Chavkin, C. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01178-0 · Cited by 24
Prenatal ethanol exposure causes anxiety-like phenotype and alters synaptic nitric oxide and endocannabinoid signaling in dorsal raphe nucleus of adult male rats
Oubraim, S., Wang, R., Hausknecht, K. A., Kaczocha, M., Shen, R., & Haj‐Dahmane, S. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02210-7 · Cited by 21
“In addition, recent optogenetic studies have reported that activation of DRn 5-HT neurons projecting to the bed nucleus of the stria terminalis and central amygdala (CeA) promotes anxiety-like behaviors [53, 54].”
Background
CB1 and CB2 receptors in the bed nucleus of the stria terminalis differently modulate anxiety-like behaviors in rats
Gomes‐de‐Souza, L., Bianchi, P., Ferreira, W. C., Tomeo, R. A., Cruz, F. C., & Crestani, C. C. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110284 · Cited by 21
Serotonin in the orbitofrontal cortex enhances cognitive flexibilityPreprint
Hyun, J. H., Hannan, P., Iwamoto, H., Blakely, R., & Kwon, H. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.09.531880 · Cited by 18
“We monitored neuronal excitability, one of the effects of 5-HT observed in other brain areas 37,38 .”
Voltage imaging reveals circuit computations in the raphe underlying serotonin-mediated motor vigor learning
Kawashima, T., Wei, Z., Haruvi, R., Shainer, I., Narayan, S., Baier, H., & Ahrens, M. B. (2025) · Neuron · doi:10.1016/j.neuron.2025.05.017 · Cited by 21
NMDA receptors in the CeA and BNST differentially regulate fear conditioning to predictable and unpredictable threats
Ressler, R. L., Goode, T. D., Evemy, C. G., & Maren, S. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107281 · Cited by 20
Distinct Circuits From the Central Lateral Amygdala to the Ventral Part of the Bed Nucleus of Stria Terminalis Regulate Different Fear Memory
Zhu, Y., Xie, S., Peng, A.-B., Yu, X., Li, C., Fu, J., Shen, C.-J., Cao, S.-X., Zhang, Y., Chen, J., et al. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.08.022 · Cited by 19
Neural circuits expressing the serotonin 2C receptor regulate memory in mice and humans
Liu, H., He, Y., Liu, H., Brouwers, B., Yin, N., Lawler, K., Keogh, J. M., Henning, E., Lee, D.-K., Yu, M., et al. (2024) · Science Advances · doi:10.1126/sciadv.adl2675 · Cited by 20
Dietary tryptophan supplementation and affective state in pigs
Stracke, J., Otten, W., Tuchscherer, A., Witthahn, M., Metges, C. C., Puppe, B., & Düpjan, S. (2017) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2017.03.009 · Cited by 18
“Of course, serotonergic pathways are complex; not only are the involved brain regions highly connected (Pessoa, 2013), but they interact with other structures regulating affective behavior, like the dopaminergic system (Boureau and Dayan, 2011) or the extended amygdala (Marcinkiewcz et al., 2016).”
Background
The anxiolytic-like effects of puerarin are associated with the changes of monoaminergic neurotransmitters and biosynthesis of allopregnanolone in the brain
Qiu, Z.-K., Zhong, D.-S., He, J.-L., Liu, X., Chen, J., & Nie, H. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0127-9 · Cited by 19
Fear not: recent advances in understanding the neural basis of fear memories and implications for treatment development
Milton, A. L. (2019) · F1000Research · doi:10.12688/f1000research.20053.1 · Cited by 15
Neural serotonergic circuits for controlling long-term voluntary alcohol consumption in mice
Belmer, A., Depoortère, R., Beecher, K., Newman‐Tancredi, A., & Bartlett, S. E. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01789-z · Cited by 18
“Given that the brain serotonin (5Hydroxytryptamine, 5-HT) system is closely involved in the stress responses to social isolation [6, 7], fear [8, 9], anxiety [9, 10] and depression [11], we hypothesized that alterations in brain 5-HT neurotransmission contributes to the reinforcement of alcohol seeking/drinking behavi…”
Background
Tripartite extended amygdala–basal ganglia CRH circuit drives locomotor activation and avoidance behavior
Chang, S., Fermani, F., Lao, C. L., Huang, L., Jakovcevski, M., Giaimo, R. D., Gagliardi, M., Menegaz, D., Hennrich, A. A., Ziller, M. J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo1023 · Cited by 19
“CRH circuits have been shown to play an important role in shaping the activity of various neurotransmitter and modulatory systems ( 9 , 11 , 25 ).”
The Anxiolytic Effect of Polysaccharides from Stellariae Radix through Monoamine Neurotransmitters, HPA Axis, and ECS/ERK/CREB/BDNF Signaling Pathway in Stress-induced Male Rats
Ma, M., Quan, H., Chen, S., Fu, X., Zang, L., & Dong, L. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110768 · Cited by 18
“Over the past decade, researchers have been increasingly drawn to the procurement, profiling, and functionality of plant-derived polysaccharides (Mohammed et al., 2021).”
Background
Activation of the NMDA receptor–neuronal nitric oxide synthase pathway within the ventral bed nucleus of the stria terminalis mediates the negative affective component of pain
Deyama, S., Sugano, Y., Mori, S., Amano, T., Yoshioka, M., Kaneda, K., & Minami, M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.008 · Cited by 18
Molecular hypotheses to explain the shared pathways and underlying pathobiological causes in catatonia and in catatonic presentations in neuropsychiatric disorders
Peter-Ross⁎, E. M. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.02.009 · Cited by 18
Blockade of NOP receptor modulates anxiety-related behaviors in mice exposed to inescapable stress
Silva, A. I., Holanda, V. A. D., Neto, J. A., Silva, E. D., Soares-Rachetti, V. D. P., Calò, G., Ruzza, C., & Gavioli, E. C. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05487-y · Cited by 17
“0.05 vs. non-stressed mice; &P < 0.05 vs. vehicle helpless mice (two-way ANOVA, LSD’s test) generally increase anxiety (Marcinkiewcz et al. 2016).”
Influential
Percutaneous Electrical Nerve Field Stimulation in Children and Adolescents With Functional Dyspepsia—Integrating a Behavioral Intervention
Santucci, N. R., Beigarten, A., Khalid, F. C., El‐Chammas, K. I., Graham, K. D., Sahay, R. D., Fei, L., Rich, K. L., & Mellon, M. W. (2023) · Neuromodulation Technology at the Neural Interface · doi:10.1016/j.neurom.2023.07.005 · Cited by 18
Elucidation of the neural circuits activated by a GABAB receptor positive modulator: Relevance to anxiety
Pizzo, R., O’Leary, O. F., & Cryan, J. F. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.021 · Cited by 19
“Such inhibition of 5-HT DRN cells might represent anxiolytic effects in the anxiety-prone BALB/c mice as optogenetic or chemogenetic activation of either the DRN or specific DRN 5-HT projections to the BNST both induce anxiogenic effects (Marcinkiewcz et al., 2016; Urban et al., 2016).”
ErbB4 knockdown in serotonergic neurons in the dorsal raphe induces anxiety-like behaviors
Zhang, S.-R., Wu, J., Chen, H. H., Luo, R., Chen, W., Tang, L., Li, X., Yang, J., & Gao, T. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0601-7 · Cited by 18
TPH2 in the Dorsal Raphe Nuclei Regulates Energy Balance in a Sex-Dependent Manner
Liu, H., Wang, C., Yu, M., Yang, Y., He, Y., Liu, H., Chen, L., Tu, L., Zhang, N., Wang, L., et al. (2020) · Endocrinology · doi:10.1210/endocr/bqaa183 · Cited by 16
A highly selective electrochemical sensor based on surface molecularly imprinted copolymer for the detection of 5-hydroxytryptamine
Xia, Y., Wang, Y., Zhang, M., Zhao, F., & Zeng, B. (2020) · Microchemical Journal · doi:10.1016/j.microc.2020.105748 · Cited by 17

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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