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Synapse-specific astrocyte gating of amygdala-related behavior
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The amygdala plays key roles in fear and anxiety. Studies of the amygdala have largely focused on neuronal function and connectivity. Astrocytes functionally interact with neurons, but their role in the amygdala remains largely unknown. We show that astrocytes in the medial subdivision of the central amygdala (CeM) determine the synaptic and behavioral outputs of amygdala circuits. To investigate the role of astrocytes in amygdala-related behavior and identify the underlying synaptic mechanisms, we used exogenous or endogenous signaling to selectively activate CeM astrocytes. Astrocytes depressed excitatory synapses from basolateral amygdala via A 1 adenosine receptor activation and enhanced inhibitory synapses from the lateral subdivision of the central amygdala via A 2A receptor activation. Furthermore, astrocytic activation decreased the firing rate of CeM neurons and reduced fear expression in a fear-conditioning paradigm. Therefore, we conclude that astrocyte activity determines fear responses by selectively regulating specific synapses, which indicates that animal behavior results from the coordinated activity of neurons and astrocytes.
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“chemogenetic activation of astrocytes in relevant circuits can affect memory performance 7, 80 .”
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BackgroundOpioid-Mediated Astrocyte–Neuron Signaling in the Nucleus Accumbens
Corkrum, M., Rothwell, P. E., Thomas, M. J., Kofuji, P., & Araque, A. (2019) · Cells · doi:10.3390/cells8060586 · Cited by 69
Self-citationRole of astrocytes in synapse formation and maturation
Tan, C. X., Burrus, C. J., & Eroğlu, Ç. (2021) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.12.010 · Cited by 66
Astrocytic IP3Rs: Beyond IP3R2
Sherwood, M. W., Arizono, M., Panatier, A., Mikoshiba, K., & Oliet, S. H. R. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.695817 · Cited by 65
Transient Astrocytic Gq Signaling Underlies Remote Memory Enhancement
Iwai, Y., Ozawa, K., Yahagi, K., Mishima, T., Akther, S., Vo, C. T., Lee, A. B., Tanaka, M., Itohara, S., & Hirase, H. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.658343 · Cited by 57
Ou, L., Przybilla, M. J., Ahlat, O., Kim, S., Overn, P., Jarnes, J., O’Sullivan, M. G., & Whitley, C. B. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.03.018 · Cited by 56
“Fear conditioning was performed according to an established protocol.(64) Briefly, on the first day, the mice were put in an enclosed container and given stimuli, followed by electric shock.”
MethodThe Astrocytic cAMP Pathway in Health and Disease
Zhou, Z., Ikegaya, Y., & Koyama, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030779 · Cited by 66
Endocannabinoid signaling in the central nervous system
Ramirez, C. E. M., Ruiz‐Pérez, G., Stollenwerk, T. M., Behlke, C., Doherty, A., & Hillard, C. J. (2022) · Glia · doi:10.1002/glia.24280 · Cited by 54
A novel gene editing system to treat both Tay–Sachs and sandhoff diseases
Ou, L., Przybilla, M. J., Tăbăran, A.-F., Overn, P., O’Sullivan, M. G., Jiang, X., Sidhu, R., Kell, P. J., Ory, D. S., & Whitley, C. B. (2020) · Gene Therapy · doi:10.1038/s41434-019-0120-5 · Cited by 52
Herrewegen, Y. V. D., Sanderson, T. M., Sahu, S., Bundel, D. D., Bortolotto, Z. A., & Smolders, I. J. (2021) · Molecular Brain · doi:10.1186/s13041-021-00856-w · Cited by 51
Chipman, P. H., Fung, C. C. A., Fernández, A. P., Sawant, A., Tedoldi, A., Kawai, A., Gautam, S. G., Kurosawa, M., Abe, M., Sakimura, K., et al. (2021) · eLife · doi:10.7554/elife.70818 · Cited by 55
Astrocytes mediate long-lasting synaptic regulation of ventral tegmental area dopamine neurons
Requie, L. M., Gómez‐Gonzalo, M., Speggiorin, M., Managò, F., Melone, M., Congiu, M., Chiavegato, A., Lia, A., Zonta, M., Losi, G., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01193-4 · Cited by 50
Self-citationEmerging technologies to study glial cells
Hirbec, H., Déglon, N., Foo, L. C., Goshen, I., Grutzendler, J., Hangen, E., Kreisel, T., Linck, N., Muffat, J., Regio, S., et al. (2020) · Glia · doi:10.1002/glia.23780 · Cited by 51
“Expression of this DREADD in centromedial amygdala astrocytes selectively increased inhibitory synaptic transmission, depressed excitatory transmission, and reduced fear perception (Martin-Fernandez et al., 2017).”
BackgroundEngram stability and maturation during systems consolidation
Refaeli, R., Kreisel, T., Groysman, M., Adamsky, A., & Goshen, I. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.042 · Cited by 46
Prefrontal cortex astroglia modulate anhedonia-like behavior
Codeluppi-Arrowsmith, S. A., Xu, M., Bansal, Y., Lepack, A. E., Duric, V., Chow, M., Muir, J., Bagot, R. C., Licznerski, P., Wilber, S. L., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02246-1 · Cited by 45
“We also conducted a control study assessing the behavioral effects of CNO in control, non-surgerized mice subjected to or not to CRS (C57Bl/6 mice, n = 10/group, 4 groups, 50% female) (Supplementary Method).”
MethodBossuyt, J., Herrewegen, Y. V. D., Nestor, L., Buckinx, A., Bundel, D. D., & Smolders, I. J. (2023) · Glia · doi:10.1002/glia.24390 · Cited by 44
“, 2016) Central amygdala: " Ca events (Martin-Fernandez et al., 2017) Hippocampus: " Ca events (Durkee et al.”
BackgroundMiguel‐Quesada, C., Zaforas, M., Herrera-Pérez, S., Lines, J., Fernández‐López, E., Alonso‐Calviño, E., Ardaya, M., Soria, F. N., Araque, A., Aguilar, J., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112950 · Cited by 45
Self-citationChen, Y., Lin, S., Jin, S., & Gao, T. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.04.013 · Cited by 42
Assessment of astrocytes as a mediator of memory and learning in rodents
Akther, S., & Hirase, H. (2021) · Glia · doi:10.1002/glia.24099 · Cited by 38
“Astrocytic A1 and A3 receptors are coupled to the Gi family of GPCRs, A2A receptors are coupled to the Gs family of proteins, and A2B couples to both Gs and Gq (Boison et al., 2010).”
BackgroundInfluentialPatton, A. P., Smyllie, N. J., Chesham, J. E., & Hastings, M. H. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2337-21.2022 · Cited by 44
Suthard, R. L., Senne, R. A., Buzharsky, M. D., Pyo, A. Y., Dorst, K. E., Diep, A. H., Cole, R. H., & Ramirez, S. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1775-22.2023 · Cited by 39
Essential Role of Astrocytes in Learning and Memory
Escalada, P., Ezkurdia, A., Ramírez, M. J., & Solas, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031899 · Cited by 46
Astrocytic microRNAs and transcription factors in Alzheimer’s disease and therapeutic interventions
Nassar, A., Kodi, T., Satarker, S., Chowdari Gurram, P., Upadhya, D., SM, F., Mudgal, J., & Nampoothiri, M. (2022) · Cells · doi:10.3390/cells11244111 · Cited by 38
The endocannabinoid system in the amygdala and modulation of fear
Gunduz‐Cinar, O. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110116 · Cited by 40
Sensing and Regulating Synaptic Activity by Astrocytes at Tripartite Synapse
Noriega‐Prieto, J. A., & Araque, A. (2021) · Neurochemical Research · doi:10.1007/s11064-021-03317-x · Cited by 45
Self-citationRapid GFAP and Iba1 expression changes in the female rat brain following spinal cord injury
Mandwie, M., Piper, J., Gorrie, C. A., Keay, K. A., Musumeci, G., Al‐Badri, G., & Castorina, A. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.317982 · Cited by 38
“…the amygdala and PAG, two regions pivotal in mediating emotional coping behaviours and that play important roles in the development of the behavioural dysfunction comorbid with injury and trauma (Keay and Bandler, 2001; Phelps and LeDoux, 2005; Mor et al., 2015; Motta et al., 2017), were evaluated.”
BackgroundJi, S., Han, S., Yu, L., Du, L., You, Y., Chen, J., Wang, M., Wu, S., Li, S., Sun, X., et al. (2022) · Phytomedicine · doi:10.1016/j.phymed.2022.153940 · Cited by 39
Glial cells in Parkinson´s disease: protective or deleterious?
Domingues, A. V., Pereira, I. M., Vilaça-Faria, H., Salgado, A. J., Rodrigues, A. J., & Teixeira, F. G. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03584-x · Cited by 38
Lei, Z., Xie, L., Li, C. H., Lam, Y. Y., Ramkrishnan, A. S., Fu, Z., Zeng, X., Liu, S., Iqbal, Z., & Li, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116092 · Cited by 36
“Recent studies have shown that Gq pathway activation in the HPC enhances neuronal activity through NMDA receptors [13,32], while Gq pathway activation in the CeM decreased neuron firing [15].”
BackgroundInfluentialScheyer, A. F., Yasmin, F., Naskar, S., & Patel, S. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01438-7 · Cited by 37
Endocannabinoid signaling in synaptic function
Noriega‐Prieto, J. A., Kofuji, P., & Araque, A. (2022) · Glia · doi:10.1002/glia.24256 · Cited by 36
“that the selective and differential regulation of excitatory and inhibitory synapses exerted by eCB-stimulated astrocytes determines animal fear responses (Martin-Fernandez et al., 2017).”
BackgroundSelf-citationIqbal, Z., Lei, Z., Ramkrishnan, A. S., Liu, S., Hasan, M., Akter, M., Lam, Y. Y., & Li, Y. (2023) · Communications Biology · doi:10.1038/s42003-022-04405-6 · Cited by 33
Delepine, C., Li, K., Shih, J., Gaudeaux, P., & Sur, M. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1982-22.2023 · Cited by 35
“…processing from synaptic (Araque et al., 1999; Haydon, 2001) to network levels (Sasaki et al., 2014 ; Perea et al., 2014a; Mederos et al., 2019; Lines et al., 2020) to drive myriad behavioral outputs (Oliveira et al., 2015; Martin-Fernandez et al., 2017; Yu et al., 2018; Nagai et al., 2019).”
BackgroundEngram reactivation mimics cellular signatures of fear
Suthard, R. L., Senne, R. A., Buzharsky, M. D., Diep, A. H., Pyo, A. Y., & Ramirez, S. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113850 · Cited by 33
Metadata
- Authors
- Martin-Fernandez, M., Jamison, S., Robin, L. M., Zhao, Z., Martin, E. D., Aguilar, J., Benneyworth, M. A., Marsicano, G., & Araque, A.
- Affiliations
- University of Minnesota (US)
- Université de Bordeaux (FR)
- Servicio de Salud de Castilla La Mancha (ES)
- Corresponding author
- Araque, Alfonso
- Venue
- Nature Neuroscience
- Published
- 2017-09-25
- Volume
- 20
- Issue
- 11
- Pages
- 1540-1548
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5903286
- OpenAlex
- W2759821008
- Cited by
- 345
- References
- 64
- Citations by year
- 2026: 28 · 2025: 51 · 2024: 45 · 2023: 48 · 2022: 44 · 2021: 41 · 2020: 37 · 2019: 29 · 2018: 20 · 2017: 1
- FWCI
- 11.65
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS097312)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- astrocytes, central amygdala, fear expression, fear conditioning, adenosine A1 receptor, adenosine A2A receptor, synaptic transmission, excitatory synapses, inhibitory synapses, basolateral amygdala, astrocyte-neuron interaction, neuronal firing rate
- MeSH terms
- Amygdala, Animals, Astrocytes, Fear, Male, Mice, Inbred C57BL, Nerve Net, Organ Culture Techniques, Synapses, Mice, Knockout, 6-Cyano-7-nitroquinoxaline-2,3-dione, Maze Learning, Receptor, Adenosine A2A, Mice, Adenosine A2 Receptor Antagonists
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