The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Synapse-specific astrocyte gating of amygdala-related behavior
Open accessAbstract
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“chemogenetic activation of astrocytes in relevant circuits can affect memory performance 7, 80 .”
From Astrocyte function from information processing to cognition and cognitive impairment (2019) · cites this paper as [80]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
Tripartite synapses: glia, the unacknowledged partner
Araque, A., Parpura, V., Sanzgiri, R. P., & Haydon, P. G. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01349-6 · Cited by 2,529
Self-citationTripartite synapses: astrocytes process and control synaptic information
Perea, G., Navarrete, M., & Araque, A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.001 · Cited by 1,820
Self-citationEndogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,595
LeDoux, J., Iwata, J., Cicchetti, P., & Reis, D. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02517.1988 · Cited by 1,580
Long-term potentiation depends on release of d-serine from astrocytes
Henneberger, C., Papouin, T., Oliet, S. H. R., & Rusakov, D. A. (2010) · Nature · doi:10.1038/nature08673 · Cited by 1,389
Gliotransmitters Travel in Time and Space
Araque, A., Carmignoto, G., Haydon, P. G., Oliet, S. H. R., Robitaille, R., & Volterra, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.007 · Cited by 1,308
Self-citationCortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303
Amygdala circuitry mediating reversible and bidirectional control of anxiety
Tye, K. M., Prakash, R., Kim, S.-Y., Fenno, L. E., Grosenick, L., Zarabi, H., Thompson, K. R., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. (2011) · Nature · doi:10.1038/nature09820 · Cited by 1,289
Astrocytic Purinergic Signaling Coordinates Synaptic Networks
Pascual, O., Casper, K. B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.-Y., Takano, H., Moss, S. J., McCarthy, K., & Haydon, P. G. (2005) · Science · doi:10.1126/science.1116916 · Cited by 1,280
Endocannabinoid Signaling and Synaptic Function
Castillo, P. E., Younts, T. J., Chávez, A. E., & Hashimotodani, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.020 · Cited by 1,191
Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice
Zimmer, A., Zimmer, A. M., Hohmann, A. G., Herkenham, M. A., & Bonner, T. I. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5780 · Cited by 1,078
Glia-Derived d-Serine Controls NMDA Receptor Activity and Synaptic Memory
Panatier, A., Theodosis, D. T., Mothet, J.-P., Touquet, B., Pollegioni, L., Poulain, D. A., & Oliet, S. H. R. (2006) · Cell · doi:10.1016/j.cell.2006.02.051 · Cited by 934
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878
Astrocytic Modulation of Sleep Homeostasis and Cognitive Consequences of Sleep Loss
Halassa, M. M., Florian, C., Fellin, T., Munoz, J. R., Lee, S.-Y., Abel, T. G., Haydon, P. G., & Frank, M. G. (2009) · Neuron · doi:10.1016/j.neuron.2008.11.024 · Cited by 877
Imai, Y., Ibata, I., Ito, D., Ohsawa, K., & Kohsaka, S. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1112 · Cited by 872
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840
Midbrain circuits for defensive behaviour
Tovote, P., Esposito, M. S., Botta, P., Chaudun, F., Fadok, J. P., Marković, M., Wolff, S. B. E., Ramakrishnan, C., Fenno, L. E., Deisseroth, K. A., et al. (2016) · Nature · doi:10.1038/nature17996 · Cited by 766
Amygdala Microcircuits Controlling Learned Fear
Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751
Astrocytes Potentiate Transmitter Release at Single Hippocampal Synapses
Perea, G., & Araque, A. (2007) · Science · doi:10.1126/science.1144640 · Cited by 727
Self-citationAstrocytes Are Endogenous Regulators of Basal Transmission at Central Synapses
Panatier, A., Vallée, J., Haber, M., Murai, K. K., Lacaille, J.-C., & Robitaille, R. (2011) · Cell · doi:10.1016/j.cell.2011.07.022 · Cited by 650
Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation
Parri, H. R., Gould, T. M., & Crunelli, V. (2001) · Nature Neuroscience · doi:10.1038/90507 · Cited by 635
Endocannabinoids Mediate Neuron-Astrocyte Communication
Navarrete, M., & Araque, A. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.029 · Cited by 625
Self-citationToll-like receptors modulate adult hippocampal neurogenesis
Rolls, A., Shechter, R., London, A., Ziv, Y., Ronen, A., Levy, R., & Schwartz, M. (2007) · Nature Cell Biology · doi:10.1038/ncb1629 · Cited by 620
Topographic organization of neurons in the acoustic thalamus that project to the amygdala
LeDoux, J., Farb, C. R., & Ruggiero, D. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01043.1990 · Cited by 564
Local Ca2+ detection and modulation of synaptic release by astrocytes
Di Castro, M. A., Chuquet, J., Liaudet, N., Bhaukaurally, K., Santello, M., Bouvier, D., Tiret, P., & Volterra, A. (2011) · Nature Neuroscience · doi:10.1038/nn.2929 · Cited by 529
Han, J., Kesner, P., Metna-Laurent, M., Duan, T., Xu, L., Georges, F., Koehl, M., Abrous, D. N., Mendizabal-Zubiaga, J., Grandes, P., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.037 · Cited by 514
Self-citationThe paraventricular thalamus controls a central amygdala fear circuit
Penzo, M. A., Robert, V., Tucciarone, J., De Bundel, D., Wang, M., Van Aelst, L., Darvas, M., Parada, L. F., Palmiter, R. D., He, M., et al. (2015) · Nature · doi:10.1038/nature13978 · Cited by 506
Experience-dependent modification of a central amygdala fear circuit
Li, H., Penzo, M. A., Taniguchi, H., Kopec, C. D., Huang, Z. J., & Li, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3322 · Cited by 497
Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes.
Navarrete, M., & Araque, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.043 · Cited by 480
Self-citationAstrocyte Ca2+ signalling: an unexpected complexity
Volterra, A., Liaudet, N., & Savtchouk, I. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3725 · Cited by 446
Hippocampal Short- and Long-Term Plasticity Are Not Modulated by Astrocyte Ca 2+ Signaling
Agulhon, C., Fiacco, T. A., & McCarthy, K. D. (2010) · Science · doi:10.1126/science.1184821 · Cited by 409
GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression
Serrano, A., Haddjeri, N., Lacaille, J.-C., & Robitaille, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5255-05.2006 · Cited by 398
Kim, K. K., Adelstein, R. S., & Kawamoto, S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.052969 · Cited by 398
Synaptic correlates of fear extinction in the amygdala
Amano, T., Ünal, Ç. T., & Paré, D. (2010) · Nature Neuroscience · doi:10.1038/nn.2499 · Cited by 384
Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala
Viviani, D., Charlet, A., van den Burg, E., Robinet, C., Hurni, N., Abatis, M., Magara, F., & Stoop, R. (2011) · Science · doi:10.1126/science.1201043 · Cited by 381
Astrocytes regulate cortical state switching in vivo
Poskanzer, K. E., & Yuste, R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520759113 · Cited by 377
Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat
McDonald, A. J. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902120307 · Cited by 371
Astrocyte signaling controls spike timing–dependent depression at neocortical synapses
Min, R., & Nevian, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3075 · Cited by 361
Cytoarchitecture of the central amygdaloid nucleus of the rat
McDonald, A. J. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902080409 · Cited by 338
Li, X., Zima, A. V., Sheikh, F., Blatter, L. A., & Chen, J. (2005) · Circulation Research · doi:10.1161/01.res.0000172556.05576.4c · Cited by 333
Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways
Martín, R., Bajo-Grañeras, R., Moratalla, R., Perea, G., & Araque, A. (2015) · Science · doi:10.1126/science.aaa7945 · Cited by 312
Self-citationSynaptically Released Acetylcholine Evokes Ca2+Elevations in Astrocytes in Hippocampal Slices
Araque, A., Martı́n, E. D., Perea, G., Arellano, J. I., & Buño, W. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02443.2002 · Cited by 283
Self-citationStructural and Functional Plasticity of Astrocyte Processes and Dendritic Spine Interactions
Perez-Alvarez, A., Navarrete, M., Covelo, A., Martin, E. D., & Araque, A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2401-14.2014 · Cited by 280
Self-citationRaastad, M., Storm, J. F., & Andersen, P. N. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00114.x · Cited by 250
Glial Biology in Learning and Cognition
Fields, R. D., Araque, A., Johansen-Berg, H., Lim, S.-S., Lynch, G., Nave, K.-A., Nedergaard, M., Perez, R., Sejnowski, T., & Wake, H. (2014) · The Neuroscientist · doi:10.1177/1073858413504465 · Cited by 232
Self-citationHirrlinger, P. G., Scheller, A., Braun, C., Hirrlinger, J., & Kirchhoff, F. (2006) · Glia · doi:10.1002/glia.20342 · Cited by 200
Gq-DREADD Selectively Initiates Glial Glutamate Release and Inhibits Cue-induced Cocaine Seeking
Scofield, M. D., Boger, H. A., Smith, R. J., Li, H., Haydon, P. G., & Kalivas, P. W. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.016 · Cited by 197
Perea, G., Gómez, R., Mederos, S., Covelo, A., Ballesteros, J. J., Schlosser, L., Hernández-Vivanco, A., Martín-Fernández, M., Quintana, R., Rayan, A., et al. (2016) · eLife · doi:10.7554/elife.20362 · Cited by 194
Self-citationDo stars govern our actions? Astrocyte involvement in rodent behavior
Oliveira, J. F., Sardinha, V. M., Guerra-Gomes, S., Araque, A., & Sousa, N. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.07.006 · Cited by 189
Self-citationDunwiddie, T. V., & Diao, L. (1994) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38968-8 · Cited by 168
Astrocytic IP3Rs: Contribution to Ca2+ signalling and hippocampal LTP
Sherwood, M. W., Arizono, M., Hisatsune, C., Bannai, H., Ebisui, E., Sherwood, J. L., Panatier, A., Oliet, S. H. R., & Mikoshiba, K. (2017) · Glia · doi:10.1002/glia.23107 · Cited by 135
Gómez-Gonzalo, M., Navarrete, M., Perea, G., Covelo, A., Martín-Fernández, M., Shigemoto, R., Luján, R., & Araque, A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu231 · Cited by 126
Self-citationBraga, M. F. M., Aroniadou‐Anderjaska, V., Xie, J., & Li, H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00442.2003 · Cited by 112
Appaix, F., Girod, S., Boisseau, S., Römer, J., Vial, J., Albrieux, M., Maurin, M., Depaulis, A., Guillemain, I., & van der Sanden, B. P. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035169 · Cited by 89
Kamprath, K., Romo-Parra, H., Häring, M., Gaburro, S., Doengi, M., Lutz, B., & Pape, H.-C. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.196 · Cited by 86
Ramikie, T. S., Nyilas, R., Bluett, R. J., Gamble‐George, J., Hartley, N. D., Mackie, K., Watanabe, M., Katona, I., & Patel, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.012 · Cited by 81
Physiological properties of central amygdala neurons: species differences
Dumont, É. C., Martina, M., Samson, R. D., Drolet, G., & Paré, D. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01879.x · Cited by 78
Lateral regulation of synaptic transmission by astrocytes.
Covelo, A., & Araque, A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.02.036 · Cited by 77
Self-citationConfocal microscopy for astrocyte in vivo imaging: Recycle and reuse in microscopy
Pérez‐Alvarez, A., Araque, A., & Martín, E. D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00051 · Cited by 35
Self-citationHagos, L., & Hülsmann, S. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.08.010 · Cited by 27
Flagged first, then by citations
Cited by
Sorted by citations
Astrocyte function from information processing to cognition and cognitive impairment
Santello, M., Toni, N., & Volterra, A. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0325-8 · Cited by 737
Astrocytic Activation Generates De Novo Neuronal Potentiation and Memory Enhancement
Adamsky, A., Kol, A., Kreisel, T., Doron, A., Ozeri-Engelhard, N., Melcer, T., Refaeli, R., Horn, H., Regev, L., Groysman, M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.05.002 · Cited by 631
“importance in neuron-astrocyte communication (Agulhon et al., 2008, 2013; Araque et al., 2014; Bonder and McCarthy, 2014; Bull et al., 2014; Chai et al., 2017; Chen et al., 2016; Martin-Fernandez et al., 2017; Scofield et al., 2015; Yang et al., 2015), we chose to express the Gq-coupled designer receptor hM3Dq (Roth,…”
Function and therapeutic value of astrocytes in neurological diseases
Lee, H.-G., Wheeler, M. A., & Quintana, F. J. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00390-x · Cited by 662
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527
Astrocytes, neurons, synapses: a tripartite view on cortical circuit development
Farhy-Tselnicker, I., & Allen, N. J. (2018) · Neural Development · doi:10.1186/s13064-018-0104-y · Cited by 417
“Increases in astrocyte calcium lead in some cases to the release of transmitter molecules such as glutamate, ATP or GABA, termed gliotransmitters that in turn, modulate astrocyte and neuronal activity [30, 80, 127].”
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
