Control of amygdala circuits by 5-HT neurons via 5-HT and glutamate cotransmission
Open accessAbstract
The serotonin (5-HT) system and the amygdala are key regulators of emotional behavior. Several lines of evidence suggest that 5-HT transmission in the amygdala is implicated in the susceptibility and drug treatment of mood disorders. Therefore, elucidating the physiological mechanisms through which midbrain 5-HT neurons modulate amygdala circuits could be pivotal in understanding emotional regulation in health and disease. To shed light on these mechanisms, we performed patch-clamp recordings from basal amygdala (BA) neurons in brain slices from mice with channelrhodopsin genetically targeted to 5-HT neurons. Optical stimulation of 5-HT terminals at low frequencies (≤1 Hz) evoked a short-latency excitation of BA interneurons (INs) that was depressed at higher frequencies. Pharmacological analysis revealed that this effect was mediated by glutamate and not 5-HT because it was abolished by ionotropic glutamate receptor antagonists. Optical stimulation of 5-HT terminals at higher frequencies (10–20 Hz) evoked both slow excitation and slow inhibition of INs. These effects were mediated by 5-HT because they were blocked by antagonists of 5-HT2Aand 5-HT1Areceptors, respectively. These fast glutamate- and slow 5-HT-mediated responses often coexisted in the same neuron. Interestingly, fast-spiking and non-fast-spiking INs displayed differential modulation by glutamate and 5-HT. Furthermore, optical stimulation of 5-HT terminals did not evoke glutamate release onto BA principal neurons, but inhibited these cells directly via activation of 5-HT1Areceptors and indirectly via enhanced GABA release. Collectively, these findings suggest that 5-HT neurons exert a frequency-dependent, cell-type-specific control over BA circuitry via 5-HT and glutamate co-release to inhibit the BA output. SIGNIFICANCE STATEMENTThe modulation of the amygdala by serotonin (5-HT) is important for emotional regulation and is implicated in the pathogenesis and treatment of affective disorders. Therefore, it is essential to determine the physiological mechanisms through which 5-HT neurons in the dorsal raphe nuclei modulate amygdala circuits. Here, we combined optogenetic, electrophysiological, and pharmacological approaches to study the effects of activation of 5-HT axons in the basal nucleus of the amygdala (BA). We found that 5-HT neurons co-release 5-HT and glutamate onto BA neurons in a cell-type-specific and frequency-dependent manner. Therefore, we suggest that theories on the contribution of 5-HT neurons to amygdala function should be revised to incorporate the concept of 5-HT/glutamate cotransmission.
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About 60% of DR serotonin neurons co-express the vesicular glutamate transporter Vglut3 in the rat and co-release glutamate in the mouse.
“~60% of DR serotonin neurons co-express the vesicular glutamate transporter Vglut3 in the rat (Gras et al., 2002) and co-release glutamate in the mouse (Liu et al., 2014; Sengupta et al., 2017).”
From Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems (2018) · cites this paper as Sengupta et al., 2017
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Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems
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The Wiring Logic of an Identified Serotonergic Neuron That Spans Sensory Networks
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Endocannabinoid-serotonin systems interaction in health and disease
Colangeli, R., Teskey, G. C., & Giovanni, G. D. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2021.01.003 · Cited by 30 · see citing works
Asim, M., Wang, H., & Waris, A. (2023) · Neuropeptides · doi:10.1016/j.npep.2023.102322 · Cited by 30 · see citing works
Serotonergic neuromodulation of synaptic plasticity
Higa, G. S. V., Viana, F. J. C., Francis-Oliveira, J., Cruvinel, E., Franchin, T. S., Marcourakis, T., Ulrich, H., & De Pasquale, R. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110036 · Cited by 29 · see citing works
A Role for Serotonin in Modulating Opposing Drive and Brake Circuits of Impulsivity
Desrochers, S. S., Spring, M. G., & Nautiyal, K. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.791749 · Cited by 29 · see citing works
“…its core and shell subregions have been extensively studied for their individual roles in impulsive action through reaction time tests, with pharmacological manipulations and deep brain stimulation of the shell subregion causing elevated premature responding (Sesia et al., 2010; Feja et al., 2014).”
BackgroundWelsch, L., Colantonio, E., Frison, M., Johnson, D. A., McClain, S. P., Mathis, V., Banghart, M. R., Hamida, S. B., Darcq, E., & Kieffer, B. L. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.05.019 · Cited by 34 · see citing works
Functional Neurologic Disorder, La Lésion Dynamique
Hallett, M. (2024) · Neurology · doi:10.1212/wnl.0000000000210051 · Cited by 28 · see citing works
Differential Expression of VGLUT2 in Mouse Mesopontine Cholinergic Neurons
Steinkellner, T., Yoo, J. H., & Hnasko, T. S. (2019) · eNeuro · doi:10.1523/eneuro.0161-19.2019 · Cited by 28 · see citing works
“…(Gras et al., 2008; Ren et al., 2011; Frahm et al., 2015; Sakae et al., 2015), ACh and GABA (Saunders et al., 2015a,b); serotonin and glutamate (Amilhon et al., 2010; Voisin et al., 2016; Sengupta et al., 2017); and even glutamate and GABA (Root et al., 2014; Shabel et al., 2014; Yoo et al., 2016).”
BackgroundJi, G., & Neugebauer, V. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184380 · Cited by 28 · see citing works
“5-HT can also decrease BLA output by direct 5-HT1AR-mediated inhibition of glutamatergic principal neurons [58], by HT1BR-mediated inhibition of their glutamatergic drive [59] or by 5-HT2R-mediated activation of BLA interneurons [19,58,60].”
BackgroundPrice, M. E., & McCool, B. A. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.08.001 · Cited by 28 · see citing works
“5-HT2A receptors depolarize (Rainnie, 1999) and excite BA interneurons (Sengupta et al., 2017), including PV+ interneurons (Bocchio et al.”
BackgroundThe dorsal raphe nucleus in the control of energy balance
Bhave, V. M., & Nectow, A. R. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.09.004 · Cited by 25 · see citing works
“Furthermore, some DRN neurons are known to corelease glutamate [74], and VGLUT3 in axon terminals could potentially facilitate increased 5-HT release through vesicular synergy [75].”
BackgroundAdaptation to photoperiod via dynamic neurotransmitter segregation
Maddaloni, G., Chang, Y., Senft, R. A., & Dymecki, S. M. (2024) · Nature · doi:10.1038/s41586-024-07692-7 · Cited by 30 · see citing works
“This finding suggests that mr En1-Pet1 neurons may transmit with glutamate as well as 5-HT; indeed, in other serotonergic neurons such as in the dorsal raphe, VGLUT3 has been demonstrated to be necessary for glutamate neurotransmission 25–27 .”
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“, prefrontal cortex), anxiety, and hence, increase the risk of developing depression (Arnsten, 2009; Bocchio et al., 2016; Hannibal and Bishop, 2014; Sengupta et al., 2017; Tafet et al., 2001).”
Beecher, K., Wang, J., Jacques, A., Chaaya, N., Chehrehasa, F., Belmer, A., & Bartlett, S. E. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.678267 · Cited by 22 · see citing works
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Anxiety and Gene Expression Enhancement in Mice Exposed to Glyphosate-Based Herbicide
Ait-Bali, Y., Kaikai, N.-E., Ba-M’hamed, S., Sassoé‐Pognetto, M., Giustetto, M., & Bennis, M. (2022) · Toxics · doi:10.3390/toxics10050226 · Cited by 20 · see citing works
“Moreover, the expression of the 5-HT3 and 5-HT2 receptor subtypes on the interneurons of the BLA suggest that the inhibition of cell firing may also be facilitated by the direct excitation of GABAergic interneurons in this nucleus [41].”
BackgroundBär, K., Köhler, S., de la Cruz, F., Schumann, A., Zepf, F. D., & Wagner, G. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116362 · Cited by 19 · see citing works
Esaki, H., Sasaki, Y., Nishitani, N., Kamada, H., Mukai, S., Ohshima, Y., Nakada, S., Ni, X., Deyama, S., & Kaneda, K. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.175653 · Cited by 18 · see citing works
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“Moreover, ex vivo electrophysiological recordings with optogenetic methods and pharmacological analysis revealed the existence of the 5-HT and glutamate co-transmission in basal amygdala neurons (Sengupta et al. 2017).”
Ballanger, B., Bath, K. G., & Mandairon, N. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.06.007 · Cited by 17 · see citing works
Leveraging VGLUT3 Functions to Untangle Brain Dysfunctions
Favier, M., Pietrancosta, N., Mestikawy, S. E., & Gangarossa, G. (2021) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2021.03.003 · Cited by 17 · see citing works
Synthetic surprise as the foundation of the psychedelic experience
Filippo, R. D., & Schmitz, D. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105538 · Cited by 15 · see citing works
Lyon, K. A., Rood, B. D., Wu, L., Senft, R. A., Goodrich, L. V., & Dymecki, S. M. (2020) · eNeuro · doi:10.1523/eneuro.0202-20.2020 · Cited by 16 · see citing works
“Indeed, there is precedent for the differential usage of serotonin and glutamate by raphe serotonergic neurons (Liu et al., 2014; Kapoor et al., 2016; Sengupta et al., 2017; Wang et al., 2019), although GABAergic and serotonergic co-release has not been reported.”
BackgroundModulation of serotonin and noradrenaline in the BLA by pindolol reduces long‐term ethanol intake
Patkar, O. L., Belmer, A., Holgate, J. Y., Klenowski, P. M., & Bartlett, S. E. (2018) · Addiction Biology · doi:10.1111/adb.12630 · Cited by 15 · see citing works
“For instance, enhancement in BLA principal cell excitability has been demonstrated with 5-HT depletion (Tran et al. 2013), 5-HT-mediated inhibition of BLA interneurons (Sengupta et al. 2017) and application of β-AR agonists (Pu et al. 2009).”
BackgroundResilience to fear: The role of individual factors in amygdala response to stressors
Fonseca, R., Madeira, N., & Simões, C. R. B. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103582 · Cited by 16 · see citing works
Fortin‐Houde, J., Henderson, F., Dumas, S., Ducharme, G., & Amilhon, B. (2023) · The Journal of Comparative Neurology · doi:10.1002/cne.25452 · Cited by 15 · see citing works
“…functional inputs from VGLUT3 DR neurons to the VTA (Liu et al., 2014; McDevitt et al., 2014; Qi et al., 2014; H. L. Wang et al., 2019; Zou et al., 2020) and amygdala (Sengupta et al., 2017; Sengupta & Holmes, 2019) and inputs from the MnR to the dorsal HP (He et al., 2022; Varga et al., 2009).”
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Evidence for a Role of 5-HT-glutamate Co-releasing Neurons in Acute Stress Mechanisms
Gullino, L. S., Fuller, C., Dunn, P., Collins, H., Mestikawy, S. E., & Sharp, T. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00758 · Cited by 12 · see citing works
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Serotonergic Input into the Cerebellar Cortex Modulates Anxiety-Like Behavior
Chin, P. W., & Augustine, G. J. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1825-24.2024 · Cited by 12 · see citing works
Chen, P., Chen, G., Tang, G., Yang, Z., Ma, W., Chen, C., Sun, S., Zhang, Y., Zhang, S., Qi, Z., et al. (2025) · Dialogues in Clinical Neuroscience · doi:10.1080/19585969.2025.2503367 · Cited by 11 · see citing works
“…(esaki et al. 2023). in addition, optical stimulation evoked 5-ht-receptor-mediated responses in the neurons of basal nucleus of the amygdala (sengupta et al. 2017). in drug-naive healthy human subjects, light-dependent alteration of the regional postsynaptic 5-ht1a receptor binding was…”
5-HT7 receptors enhance inhibitory synaptic input to principal neurons in the mouse basal amygdala
Kusek, M., Siwiec, M., Sowa, J. E., Bobula, B., Bilecki, W., Ciurej, I., Kaczmarczyk-Jarosz, M., Kowalczyk, T., Maćkowiak, M., Hess, G., et al. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108779 · Cited by 11 · see citing works
Wang, Z., Li, C., Ding, J., Li, Y., Zhou, Z., Huang, Y., Wang, X., Fan, H., Huang, J. A., He, Y., et al. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.627307 · Cited by 11 · see citing works
Upmanyu, N., Jin, J., von der Emde, H., Ganzella, M., Bösche, L., Malviya, V. N., Zhuleku, E., Politi, A. Z., Ninov, M., Silbern, I., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.30.449903 · Cited by 11 · see citing works
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Sex-specific modulation of the medial prefrontal cortex by glutamatergic median raphe neurons
Collins, S. A., Stinson, H. E., Himes, A., Nestor‐Kalinoski, A. L., & Ninan, I. (2023) · Science Advances · doi:10.1126/sciadv.adg4800 · Cited by 9 · see citing works
“…our investigation of the effect of 5-HT is limited to its role in MRN (VGLUT3) neuron – mediated hyperpolarization and GABAergic plasticity in pyramidal neurons, these results strongly suggest the role of 5-HT release from MRN (VGLUT3) neurons on mPFC inhibition ( 10 , 14 , 19 , 28 , 46 – 48 ).”
Fazekas, C. L., Szabó, A., Török, B., Bánrévi, K., Correia, P., Chaves, T., Daumas, S., & Zelena, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020790 · Cited by 9 · see citing works
“In the basal amygdala, the axon terminals either release 5-HT or Glu based on the frequency of firing [56].”
BackgroundNeuronal pericellular baskets: neurotransmitter convergence and regulation of network excitability
Senft, R. A., & Dymecki, S. M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.08.006 · Cited by 10 · see citing works
“Indeed, certain serotonergic fibers in the amygdala, though not comprising baskets, showed differential neurotransmitter release depending on stimulation frequency: low-frequency stimulation was sufficient to evoke glutamate release, higher frequencies were needed to elicit 5-HT release [54].”
BackgroundCB1/5-HT/GABA interactions and food intake regulation
Escartín-Pérez, R. E., Díaz, J. M. M., Salazar, F. C., López-Alonso, V. E., & Florán, B. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2021.01.005 · Cited by 9 · see citing works
5-HT neurons of the medullary raphe contribute to respiratory control in toads
Fonseca, E. M., Noronha‐de‐Souza, C. R., Bícego, K. C., Branco, L. G. S., & Gargaglioni, L. H. (2021) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2021.103717 · Cited by 8 · see citing works
Brain Circuits Regulated by the 5-HT2A Receptor: Behavioural Consequences on Anxiety and Fear Memory
Moulédous, L., Roullet, P., & Guiard, B. P. (2018) · Springer eBooks · doi:10.1007/978-3-319-70474-6_10 · Cited by 8 · see citing works
Serotonergic control of GABAergic inhibition in the lateral amygdala
Yamamoto, R., Furuyama, T., Sugai, T., Ono, M., Paré, D., & Kato, N. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00500.2019 · Cited by 8 · see citing works
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 · see citing works
“, 2002), and recent physiology studies suggest that these neurons co-release glutamate in the mouse (Liu et al., 2014; Sengupta et al., 2017).”
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Regulation of stress-induced sleep perturbations by dorsal raphe VGLUT3 neurons in male mice
Henderson, F., Dumas, S., Gangarossa, G., Bernard, V., Pujol, M., Poirel, O., Pietrancosta, N., Mestikawy, S. E., Daumas, S., & Fabre, V. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114411 · Cited by 7 · see citing works
Role of adaptor protein complexes in generating functionally distinct synaptic vesicle pools
Asmerian, H., Alberts, J., Sanetra, A. M., Diaz, A. J., & Silm, K. (2024) · The Journal of Physiology · doi:10.1113/jp286179 · Cited by 5 · see citing works
“Differential regulation of the release of two transmitters from the same neuronal population has also been shown in other systems (Lee et al., 2010; Sengupta et al., 2017; Takács et al., 2018) but the contribution of SV pools has not been directly explored.”
Schweimer, J. V., Brouard, J. T., Li, Y., Sánchez, C., & Sharp, T. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15623 · Cited by 6 · see citing works
“Recently, the co-release of glutamate from 5-HT neurons was reported to induce fast excitatory responses in amygdala mediated by ionotropic glutamate receptors (Sengupta et al., 2017).”
BackgroundKranz, 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 · see citing works
Investigation of the Role of Stimulation and Blockade of 5-HT7 Receptors in Ketamine Anesthesia.
Dinçer, B., Halıcı, Z., & Çadırcı, E. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01732-3 · Cited by 5 · see citing works
Serotonergic current responses of neurons in rat oculomotor neural integrators
Saito, Y., & Sugimura, T. (2023) · Journal of Neurophysiology · doi:10.1152/jn.00452.2022 · Cited by 5 · see citing works
Kiyokawa, Y., Ootaki, M., Kambe, Y., Tanaka, K. D., Kimura, G., Tanikawa, T., & Takeuchi, Y. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.05.003 · Cited by 5 · see citing works
“Taken together, the present study sug-Table jections from the DR (Sengupta et al., 2017).”
BackgroundComplementary roles of serotonin and dopamine in model-based learning
Taira, M., & Sharpe, M. J. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101464 · Cited by 6 · see citing works
Human neuromodulatory assembloids to study serotonin signaling and diseasePreprint
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Serotonin circuits act cooperatively with pathophysiology of opioid use disorder
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“Moreover, Sengupta et al. (2017) emphasized the critical role of the amygdala's serotonin receptors (5-HT 1A and 5-HT 2A ) in the emotion process.”
Neuromodulation of Hippocampal Cells and Circuits
Lawrence, J. J., & Cobb, S. (2018) · Springer series in computational neuroscience · doi:10.1007/978-3-319-99103-0_7 · Cited by 4 · see citing works
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Ultra-high field brain MRI for functional neurological disorder: opportunities and challenges
Myren, S., Jungilligens, J., Diez, I. P., Bøen, E., Elvsåshagen, T., Forstmann, B. U., Ziaei, M., & Doan, T. P. (2026) · NeuroImage Clinical · doi:10.1016/j.nicl.2026.103972 · Cited by 3 · see citing works
“Abnormalities in serotonin synthesis, together with strong serotonergic control of amygdala circuits, suggest a potential role in the emotion dysregulation observed in FND (Hallett, 2024; Sengupta et al., 2017).”
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Serotonin and the CNS - New Developments in Pharmacology and Therapeutics
Olivier, B. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.90962 · Cited by 5 · see citing works
Valipour, H., Jahromi, G. P., Mohammadi, A., & Meftahi, G. H. (2023) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-023-02790-1 · Cited by 3 · see citing works
“The amygdala consists of a high density of 5-HT receptors (Sengupta et al., 2017).”
Hirai, H., Konno, K., Yamasaki, M., Watanabe, M., Sakaba, T., & Hashimotodani, Y. (2024) · eLife · doi:10.7554/elife.99711.3 · Cited by 15 · see citing works
The impact of membrane receptors on modulating empathic pain
Teixeira, G. P., Rocha, L., & Faria, R. X. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110471 · Cited by 3 · see citing works
- Authors
- Sengupta, A., Bocchio, M., Bannerman, D. M., Sharp, T., & Capogna, M.
- Affiliations
- University of Oxford (GB)
- Aarhus University (DK)
- Corresponding author
- Sharp, Trevor
- Capogna, Marco
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2017-01-13
- Volume
- 37
- Issue
- 7
- Pages
- 1785-1796
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5320609
- OpenAlex
- W2573649328
- Cited by
- 136
- References
- 52
- Citations by year
- 2026: 15 · 2025: 9 · 2024: 18 · 2023: 13 · 2022: 9 · 2021: 19 · 2020: 21 · 2019: 18 · 2018: 11 · 2017: 3
- FWCI
- 7.10
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Durham Research Online (Durham University) (submittedVersion, cc-by)
- Scopus (Elsevier) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by)
- Funders
- Wellcome Trust
- University of Oxford
- National Institutes of Health
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- serotonin, glutamate co-release, amygdala, basal amygdala, dorsal raphe nucleus, 5-HT1A receptor, 5-HT2A receptor, interneurons, principal neurons, emotion regulation, mood disorders, GABA release, optogenetics, channelrhodopsin, ionotropic glutamate receptors, fast-spiking interneurons
- MeSH terms
- Channelrhodopsins, Amygdala, Animals, Animals, Newborn, Female, Luminescent Proteins, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Net, Synaptic Transmission, Neurons, Piperazines, Pyridines, Receptors, Serotonin, Serotonin, Serotonin Antagonists, Excitatory Amino Acid Agents, Glutamic Acid, GABA Antagonists, Serotonin Plasma Membrane Transport Proteins, Mice
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