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Regulation of synaptic connectivity by glia.
Open accessAbstract
The human brain contains more than 100 trillion (10(14)) synaptic connections, which form all of its neural circuits. Neuroscientists have long been interested in how this complex synaptic web is weaved during development and remodelled during learning and disease. Recent studies have uncovered that glial cells are important regulators of synaptic connectivity. These cells are far more active than was previously thought and are powerful controllers of synapse formation, function, plasticity and elimination, both in health and disease. Understanding how signalling between glia and neurons regulates synaptic development will offer new insight into how the nervous system works and provide new targets for the treatment of neurological diseases.
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“Evidence now shows that astrocytes are directly involved in synaptic connections and control, ranging from ionic balance to the genesis and behavior of synapses”
From Interlaminar and varicose-projection astrocytes: toward a new understanding of the primate brain (2024) · cites this paper as Eroglu and Barres, 2010
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“In mammals, secreted and cell-surface signals, for example, thrombospondin (TSP) family members and integrin-like proteins from glia, control synaptogenesis and synaptic activities (Christopherson et al. 2005; Eroglu & Barres 2010).”
BackgroundVariation in hippocampal glial cell numbers in food‐caching birds from different climates
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“On the other hand, a tripartite model that includes glia has recently been proposed to revise the classical view of synaptic structure([6-8]).”
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Probing Astrocyte Function in Fragile X Syndrome
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BackgroundSpinal astrocyte dysfunction drives motor neuron loss in late-onset spinal muscular atrophy
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“(1998a,b) served to later coin the term ‘‘tripartite synapse’’, which describes how astrocytic processes together with pre- and postsynaptic terminals constitute a functional structure that sustain the activity of neural circuits (Eroglu and Barres, 2010).”
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“Glial cells in the central nervous system may monitor, respond to, and participate in synaptic activity by releasing neuroactive substances in a process known as ‘gliotransmission’ (Eroglu and Barres 2010 ; Parpura et al. 2012 ).”
BackgroundAstrocyte-neuron metabolic crosstalk in ischaemic stroke
Ren, Z., Lan, X., Zheng, Y., Zheng, Y.-X., Chen, C.-A., Liu, Y., He, Y.-H., Han, J.-H., Wang, Q.-G., Cheng, F., et al. (2025) · Neurochemistry International · doi:10.1016/j.neuint.2025.105954 · Cited by 12
Selective regulation of corticostriatal synapses by astrocytic phagocytosis
Kim, J. S., Kim, H., Chung, W., & Park, H. (2025) · Nature Communications · doi:10.1038/s41467-025-57577-0 · Cited by 14
Neural Stem Cells in Adult Mammals are not Astrocytes
Velloso, F. J., Shankar, S., Parpura, V., RAKIC, P. T., & Levison, S. W. (2022) · ASN NEURO · doi:10.1177/17590914221134739 · Cited by 14
“Indeed, the secretion of factors such as thrombospondins, cholesterol, and neuregulins is important for synaptogenesis, synaptic maturation, and myelination (Camargo et al., 2017; Christopherson et al., 2005; Eroglu and Barres, 2010; Eroglu et al., 2009; Kucukdereli et al., 2011).”
BackgroundLeo, M., Schmitt, L.-I., Steffen, R., Kutritz, A., Kleinschnitz, C., & Hagenacker, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126300 · Cited by 13
Yu, D., Zarate, N., White, A., Coates, D., Tsai, W., Nanclares, C., Cuccu, F., Yue, J. S., Brown, T. G., Mansky, R., et al. (2020) · bioRxiv · doi:10.1101/2020.10.29.359380 · Cited by 12
The role of gut-immune-brain signaling in substance use disorders
Lucerne, K. E., & Kiraly, D. D. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.09.005 · Cited by 17
Tedoldi, A., Argent, L. P., & Montgomery, J. M. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00363.2020 · Cited by 19
Overexpression of Swedish mutant APP in aged astrocytes attenuates excitatory synaptic transmission
Katsurabayashi, S., Kawano, H., Ii, M., Nakano, S., Tatsumi, C., Kubota, K., Takasaki, K., 三島, 健., Fujiwara, M., & Iwasaki, K. (2016) · Physiological Reports · doi:10.14814/phy2.12665 · Cited by 13
“Because astrocytes have an important role in the information processing by synapses of the central nervous system (Allen and Barres 2009; Eroglu and Barres 2010), we speculated that the synaptic transmission may be attenuated by chronic exposure to Ab 1–40 and 1–42 released from the Tg astrocytes.”
BackgroundConnectivity and circuitry in a dish versus in a brain
Chinchalongporn, V., Koppensteiner, P., Prè, D., Thangnipon, W., Bilo, L., & Arancio, O. (2015) · Alzheimer s Research & Therapy · doi:10.1186/s13195-015-0129-y · Cited by 15
Interlaminar and varicose-projection astrocytes: toward a new understanding of the primate brain
Ciani, C., & Falcone, C. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1477753 · Cited by 11
Choi, J. S., Ayupe, A. C., Beckedorff, F., Catanuto, P., McCartan, R., Levay, K., & Park, K. K. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113037 · Cited by 20
“50 Supporting this notion, our data showed dynamic changes in astrocytic expression of various guidance molecules across time points; while genes encoding Eph receptor and ephrin molecules showed decreased expression over time, subsets of genes from the semaphorin-plexin signaling pathway, such as…”
Photons Induce Vesicular Exocytotic Release of Glutamate in a Power-Dependent Way
Cervetto, C., Amaroli, A., Amato, S., Gatta, E., Diaspro, A., Maura, G., Signore, A., Benedicenti, S., & Marcoli, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310977 · Cited by 11
“Electron microscopy also indicated that the isolated nerve terminals retained the hallmarks of mammalian presynaptic nerve terminals in situ [29,30] or in cultured neurons [31] as they were filled with vesicles exhibiting the typical appearance of the small clear synaptic vesicles for storage of the classical neurotra…”
BackgroundNishi, K., Izumi, H., Tomonaga, T., Nagano, C., Morimoto, Y., & Horie, S. (2023) · Biomolecules · doi:10.3390/biom13050718 · Cited by 10
“Among glial cells, astrocytes (ACs) form contacts with many synapses and regulate neuronal activity through the release of glial transmitters such as adenosine triphosphate [6].”
BackgroundIn vivo neuronal and astrocytic activation in somatosensory cortex by acupuncture stimuli
Zhang, L., So, K., Yang, E., Chang, X., Chen, K., Cheng, T., & Lai, P. T. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.339003 · Cited by 13
“…a finding that indicates complementary neuronal contributions and possible glial control, which is consistent with the current knowledge of astrocytes as the regulator and architect of neuronal processing (Eroglu and Barres, 2010; Panatier et al., 2011; Allen and Lyons, 2018; Mederos et al., 2018).”
ResultMurasawa, H., Kobayashi, H., Imai, J., Nagase, T., Soumiya, H., & Fukumitsu, H. (2021) · PLoS ONE · doi:10.1371/journal.pone.0258830 · Cited by 10
“Astrocytes regulate neuronal functions through production and secretion of growth factors, nutrients, and cytokines and by the uptake of transmitters and metabolites [74, 75], while IGF is involved in the differentiation and functional maintenance of neurons as a blood–brain barrier permeable neurotrophic factor [76,…”
BackgroundAdvanced Bio-Based Polymers for Astrocyte Cell Models
Gradišnik, L., Bošnjak, R., Maver, T., & Velnar, T. (2021) · Materials · doi:10.3390/ma14133664 · Cited by 13
“Much of our knowledge of astrocytes, synaptogenesis, and their role in neuronal survival comes from studies of these cells [74,75].”
BackgroundUsing Zebrafish to Elucidate Glial-Vascular Interactions During CNS Development
Umans, R. A., Pollock, C., Mills, W. A., Clark, K. C., Pan, Y. A., & Sontheimer, H. W. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.654338 · Cited by 16
“Glia perform a variety of vital functions including supporting synaptogenesis (Eroglu and Barres, 2010), neurotransmitter and ion homeostasis (Murphy-Royal et al.”
BackgroundAdvances in the Pathophysiology and Management of Cancer Pain: A Scoping Review
Varrassi, G., Paladini, A., Tran, Y. V., Pham, P. V., Al-Alwany, A. A., Farì, G., Caruso, A., Mercieri, M., Pergolizzi, J. V., Kaye, A. D., et al. (2026) · Cancers · doi:10.3390/cancers18020259 · Cited by 15
“Furthermore, astrocytes release thrombospondin-1 and https://doi.org/10.3390/cancers18020259 D-serine, which promote excitatory synapse formation and potentiate NMDA receptor function, respectively [32].”
InfluentialBenazzato, C., Lojudice, F. H., Pöehlchen, F., Leite, P. E. C., Manucci, A. C., van der Linden, V., Jungmann, P., Sogayar, M. C., Bruni‐Cardoso, A., Russo, F. B., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-65392-8 · Cited by 14
Human iPSC-Derived Cortical Neurons Display Homeostatic Plasticity
Cordella, F., Ferrucci, L., D’Antoni, C., Ghirga, S., Brighi, C., Soloperto, A., Gigante, Y., Ragozzino, D., Bezzi, P., & Angelantonio, S. D. (2022) · Life · doi:10.3390/life12111884 · Cited by 11
Dong, Z., Zhan, T., Sun, H., Wang, J., Duan, G., Zhang, Y., Chen, Y., Huang, Y., & Xu, S. (2022) · Journal of Pain · doi:10.1016/j.jpain.2022.07.006 · Cited by 10
Badia‐Soteras, A., de Vries, J., Dykstra, W., Broersen, L. M., Verkuyl, J. M., Smit, A. B., & Verheijen, M. H. G. (2022) · Cells · doi:10.3390/cells11091428 · Cited by 13
Günther, H., Henne, S., Oehlmann, J., Urban, J., Pleizier, D., Renevier, N., Lohr, C., & Wülfing, C. (2021) · Scientific Reports · doi:10.1038/s41598-021-92364-z · Cited by 10
Ren, B., & Dunaevsky, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041692 · Cited by 12
O’Reilly, K., O’Farrell, K., Midttun, Ø., Rakovets, Y., David‐Bercholz, J., & Harkin, A. (2021) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-020-09976-x · Cited by 12
Wentz, E., Dobrescu, S. R., Dinkler, L., Gillberg, C., Gillberg, C., Blennow, K., Råstam, M., & Zetterberg, H. (2020) · European Child and Adolescent Psychiatry · doi:10.1007/s00787-020-01657-7 · Cited by 10
Simone, U. D., Lonati, D., Ronchi, A., & Coccini, T. (2016) · Toxicology Letters · doi:10.1016/j.toxlet.2016.05.006 · Cited by 8
“…in the CNS. Astrocytes have a variety of important functions such as supplying of metabolic nutrients to neurons and also protecting the brain against oxidative stress and metal toxicity (Eroglu and Barres, 2010; Hirrlinger and Dringen, 2010; Parpura et al., 2012; Tiffany-Castiglioni et al., 2011).”
BackgroundPhysiology of Astroglia: Channels, Receptors, Transporters, Ion Signaling and Gliotransmission
Verkhratsky, A., & Parpura, V. (2015) · Colloquium Series on Neuroglia in Biology and Medicine From Physiology to Disease · doi:10.4199/c00123ed1v01y201501ngl004 · Cited by 12
Jindal, D. A., Leier, H. C., Salazar, G., Foden, A. J., Seitz, E. A., Wilkov, A. J., Coutinho‐Budd, J., & Broihier, H. T. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1166199 · Cited by 16
“Beyond supportive roles in neuronal growth and metabolism (Eroglu and Barres, 2010; Nave, 2010; Kettenmann et al., 2013), glia monitor and modify”
BackgroundGarcía‐Bonilla, M., Ojeda-Pérez, B., Shumilov, K., Rodríguez‐Pérez, L., Domínguez-Pinos, D., Vitórica, J., Jiménez, S., Ramírez‐Lorca, R., Echevarrı́a, M., Cárdenas, C., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065640 · Cited by 13
“As another remarkable effect, BM-MSC treated hyh mice presented an underregulation of complement proteins implicated in synaptic pruning, which involves microglia and astroglia [75].”
BackgroundVoluntary running exercise modifies astrocytic population and features in the peri-infarct cortex
Yamaguchi, N., Sawano, T., Nakatani, J., Nakano‐Doi, A., Nakagomi, T., Matsuyama, T., & Tanaka, H. (2023) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2023.02.004 · Cited by 9
A novel regulator in Alzheimer's disease progression: The astrocyte-derived extracellular vesicles
Li, B., Ma, Z., & Li, Z. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101871 · Cited by 11
Sears, S. M. S., Roberts, S. H., & Hewett, S. J. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24971 · Cited by 9
Development of astrocyte morphology and function in mouse visual thalamus
Somaiya, R. D., Huebschman, N. A., Chaunsali, L., Sabbagh, U., Carrillo, G. L., Tewari, B. P., & Fox, M. A. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25261 · Cited by 12
An, H., Koh, W., Kang, S., Nam, M., & Lee, C. J. (2021) · Experimental Neurobiology · doi:10.5607/en21015 · Cited by 10
“Astrocytes contact multiple synapses through an ultrastructure called microdomain or perisynapse to form tripartite synapses with presynaptic axon terminals and postsynaptic dendritic spines throughout the whole brain [4, 5].”
Background
Metadata
- Authors
- Eroglu, C., & Barres, B. A.
- Affiliations
- Stanford Medicine (US)
- ORCID
- Barres, Ben A.
- Venue
- Nature
- Published
- 2010-11
- Volume
- 468
- Issue
- 7321
- Pages
- 223-231
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4431554
- OpenAlex
- W1973477241
- Cited by
- 813
- References
- 104
- Citations by year
- 2026: 21 · 2025: 46 · 2024: 48 · 2023: 52 · 2022: 54 · 2021: 60 · 2020: 52 · 2019: 52 · 2018: 66 · 2017: 54 · 2016: 50 · 2015: 50 · 2014: 55 · 2013: 58 · 2012: 58
- FWCI
- 4.31
- 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)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Alfred P. Sloan Foundation
- National Institute on Drug Abuse (R01DA015043)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- glial cells, synaptic connectivity, synaptogenesis, synaptic pruning, synaptic plasticity, synaptic development, learning, neurological disorders
- MeSH terms
- Animals, Axons, Central Nervous System Diseases, Drosophila melanogaster, Humans, Synaptic Transmission, Neuroglia, Synapses
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