Microglia: Activity‐dependent regulators of neural circuits
Open accessAbstract
It has been more than a century since Pío del Río‐Hortega first characterized microglia in histological stains of brain tissue. Since then, significant advances have been made in understanding the role of these resident central nervous system (CNS) macrophages. In particular, it is now known that microglia can sense neural activity and modulate neuronal circuits accordingly. We review the mechanisms by which microglia detect changes in neural activity to then modulate synapse numbers in the developing and mature CNS. This includes responses to both spontaneous and experience‐driven neural activity. We further discuss activity‐dependent mechanisms by which microglia regulate synaptic function and neural circuit excitability. Together, our discussion provides a comprehensive review of the activity‐dependent functions of microglia within neural circuits in the healthy CNS, and highlights exciting new open questions related to understanding more fully microglia as key components and regulators of neural circuits.
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Microglia sense neural activity and modulate neuronal circuits, releasing factors like BDNF to induce new synapse formation or TNFα to regulate synaptic scaling.
“Microglia also sense neural activity and modulate neuronal circuits, releasing factors like BDNF to induce new synapse formation or TNFα to regulate synaptic scaling [84].”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [84]
The Introduction and Conclusions say microglia sense changes in neural activity and influence circuits; the activity-dependent functional connectivity section says microglia-derived TNFα contributes to synaptic scaling. The Conclusions describe BDNF release as proposed, and the activity-dependent synaptogenesis section leaves open whether BDNF acts through release or through signaling within microglia. The claim presents BDNF release as established. (LLM, conf=0.86)
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“Although it is less clear if neural activity is involved, another important consideration is that in a developmental context, astrocyte-derived IL-33 appears to induce microglial phagocytic transcriptional programs via IL1RL1/ST2 to facilitate microglial elimination of synapses 26–28 (Figure 1B).”
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“86,87 These data raise the possibilitythatmicrogliaarerespondingtolargechangesinneuralnet-work activity by releasing TNF α to modulate synaptic plasticity and function.”
BackgroundAstrocyte-secreted IL-33 mediates homeostatic synaptic plasticity in the adult hippocampus
Wang, Y., Fu, W., Cheung, K., Hung, K.-W., Chen, C., Geng, H.-Y., Yung, W., Qu, J. Y., Fu, A. K. Y., & Ip, N. Y. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020810118 · Cited by 133 · see citing works
Microglial depletion aggravates the severity of acute and chronic seizures in mice
Wu, W., Li, Y., Wei, Y., Bosco, D. B., Xie, M., Zhao, M., Richardson, J. R., & Wu, L. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.06.028 · Cited by 133 · see citing works
Phagocytic elimination of synapses by microglia during sleep
Choudhury, M. E., Miyanishi, K., Takeda, H., Islam, A., Matsuoka, N., Kubo, M., Matsumoto, S., Kunieda, T., Nomoto, M., Yano, H., et al. (2019) · Glia · doi:10.1002/glia.23698 · Cited by 123 · see citing works
Microglia regulate sleep through calcium-dependent modulation of norepinephrine transmission
Ma, C., Li, B., Silverman, D., Ding, X., Li, A., Xiao, C., Huang, G., Worden, K., Muroy, S. E., Chen, W., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01548-5 · Cited by 122 · cited 1× · see citing works
“79 One important open question is whether adenosine is acting directly on neurons or rather on astrocytes, which also express adenosine receptors and have key roles in regulating synaptic activity.”
BackgroundEyo, U. B., Peng, J., Murugan, M., Mo, M., Lalani, A., Xie, P., Xu, P., Margolis, D. J., & Wu, L. (2016) · eNeuro · doi:10.1523/eneuro.0209-16.2016 · Cited by 114 · cited 1× · see citing works
“88 It remains to be determined how CX3CR1 is mediating this effect, but it is intriguing to consider that previously discussed activity-dependent developmental mechanisms that engage CX3CR1–CX3CL1 signaling to regulate synapse numbers 6,31 may be involved.”
BackgroundMicroglial MERTK eliminates phosphatidylserine‐displaying inhibitory post‐synapses
Park, J., Choi, Y., Jung, E., Lee, S., Sohn, J., & Chung, W. (2021) · The EMBO Journal · doi:10.15252/embj.2020107121 · Cited by 114 · cited 2× · see citing works
“38”
BackgroundMicroglial trogocytosis and the complement system regulate axonal pruning in vivo
Lim, T. K. Y., & Ruthazer, E. S. (2021) · eLife · doi:10.7554/elife.62167 · Cited by 112 · cited 2× · see citing works
“46,47 These studies provided evidence that microglia preferentially trogocy-tose a presynaptic membranes and axons rather than engulfing whole synaptic compartments or postsynaptic material (Figure 3C).”
Bolós, M., Perea, J. R., Terreros‐Roncal, J., Pallas‐Bazarra, N., Jurado‐Arjona, J., Ávila, J., & Llorens-Martı́n, M. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.10.002 · Cited by 109 · cited 1× · see citing works
“In addition to regulation of synapse numbers in the developing brain, microglia have synaptogenic roles in the adult brain, based on work in the cortex, 17 hippocamus, 18 and olfactory bulb 19,20 (Figure 1A).”
BackgroundLiu, Y., Given, K. S., Dickson, E. L., Owens, G. P., Macklin, W. B., & Bennett, J. L. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.04.011 · Cited by 105 · see citing works
A comparative analysis of microglial inducible Cre lines
Faust, T. E., Feinberg, P. A., O’Connor, C., Kawaguchi, R., Chan, A., Strasburger, H., Frosch, M., Boyle, M. A., Masuda, T., Amann, L., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113031 · Cited by 103 · see citing works
Self-citationLowery, R. L., Tremblay, M., Hopkins, B. E., & Majewska, A. K. (2017) · Glia · doi:10.1002/glia.23192 · Cited by 80 · see citing works
An activity-dependent determinant of synapse elimination in the mammalian brain
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“41 ItispossiblethatJAK2–STAT1transcriptional programs elicit changes in PtdSer exposure in less active neurons, followed by microglial engulfment of synaptic material.”
BackgroundREV-ERBα mediates complement expression and diurnal regulation of microglial synaptic phagocytosis
Griffin, P., Sheehan, P. W., Dimitry, J. M., Guo, C., Kanan, M. F., Lee, J., Zhang, J., & Musiek, E. S. (2020) · eLife · doi:10.7554/elife.58765 · Cited by 73 · cited 1× · see citing works
“68 Interesting, deleting the master clock gene Bmal1 only in CD11b-expressing myeloid cells, including microglia,inagedmiceresultedintheoppositeresult,thatisdecreased complement deposition, decreased microglia engulfment of synapses, and increased immature dendritic spines in the hippocampus.”
BackgroundExperience-Dependent Synaptic Plasticity in V1 Occurs without Microglial CX3CR1
Schecter, R. W., Maher, E. E., Welsh, C. A., Stevens, B., Erişir, A., & Bear, M. F. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2679-16.2017 · Cited by 71 · cited 1× · see citing works
“57,58 One possibility is that neuronal diversity in molecular signatures and activity patterns drives differential expression of factors that drive this region-specific immune-mediated pruning.”
BackgroundOkojie, A. K., Uweru, J. O., Coburn, M., Li, S., Cao-Dao, V. D., & Eyo, U. B. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02924-5 · Cited by 68 · see citing works
Microglia regulate chandelier cell axo-axonic synaptogenesis
Gallo, N. B., Berisha, A., & Aelst, L. V. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114476119 · Cited by 63 · cited 4× · see citing works
“16 These data suggest that microglia respond to GABAergic neurotransmission to modulate their association with the AIS, which subsequently facilitates chandelier cell inhibitory synapse formation.”
BackgroundInfluentialVisual Experience-Dependent Expression of Fn14 Is Required for Retinogeniculate Refinement
Cheadle, L., Tzeng, C. P., Kalish, B. T., Harmin, D. A., Rivera, S. A., Ling, E., Nagy, M. A., Hrvatin, S., Hu, L. S., Stroud, H., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.036 · Cited by 59 · cited 1× · see citing works
“49,50 The authors further found that synapse density was higher around microglia that did not express TWEAK in the LGN, and mice deficient in TWEAK had a defect in retinogeniculate synapse elimination in juvenile mice.”
BackgroundOkada, Y., Hosoi, N., Matsuzaki, Y., Fukai, Y., Hiraga, A., Nakai, J., Nitta, K., Shinohara, Y., Konno, A., & Hirai, H. (2022) · Communications Biology · doi:10.1038/s42003-022-04200-3 · Cited by 58 · see citing works
Kemp, G. M., Altimimi, H. F., Nho, Y., Heir, R., Klyczek, A., & Stellwagen, D. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01737-x · Cited by 57 · cited 1× · see citing works
“81 82-85 It was further shown that seizures could be exacerbated by microglia-derived TNF α , and that blocking brain-derived TNF α reduced seizure severity.”
BackgroundWallace, J. L., Lord, J. S., Dissing‐Olesen, L., Stevens, B., & Murthy, V. N. (2020) · eLife · doi:10.7554/elife.50531 · Cited by 52 · cited 1× · see citing works
“In addition to regulation of synapse numbers in the developing brain, microglia have synaptogenic roles in the adult brain, based on work in the cortex, 17 hippocamus, 18 and olfactory bulb 19,20 (Figure 1A).”
BackgroundHan, R. T., Vainchtein, I. D., Schlachetzki, J. C. M., Cho, F. S., Dorman, L. C., Ahn, E., Kim, D. K., Barron, J. J., Nakao-Inoue, H., Molofsky, A. B., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220605 · Cited by 51 · see citing works
Ocular Dominance Plasticity in Binocular Primary Visual Cortex Does Not Require C1q
Welsh, C. A., Stephany, C.-É., Sapp, R. W., & Stevens, B. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1011-19.2019 · Cited by 49 · cited 2× · see citing works
“53 In contrast, C1q and matrix metalloprotease 9 (MMP9) have been implicated in monocular deprivation–induced synapse engulfment and remodeling in the secondary visual cortex to regulate cross-modal plasticity in developing mice.”
BackgroundCong, Q., Soteros, B. M., Huo, A., Li, Y., Tenner, A. J., & Sia, G.-M. (2021) · Glia · doi:10.1002/glia.24114 · Cited by 47 · cited 2× · see citing works
“16”
Li, T., Yu, D., Oak, H. C., Zhu, B., Wang, L., Jiang, X., Molday, R. S., Kriegstein, A. R., & Piao, X. (2021) · The EMBO Journal · doi:10.15252/embj.2021107915 · Cited by 42 · cited 2× · see citing works
“36,37 Briefly,CDC50A(alsoknownasTMEM30A), a chaperone of phospholipid flippases known to negatively regulate PtdSer exposure, 36 is decreased when neuronal activity decreases in cultured neurons.”
BackgroundIweka, C., Seigneur, E., Hernandez, A., Paredes, S., Cabrera, M., Blacher, E., Pasternak, C. T., Longo, F., de Lecea, L., & Andreasson, K. (2022) · bioRxiv · doi:10.1186/s12974-023-02727-8 · Cited by 39 · cited 1× · see citing works
“69 These seemingly opposing results may be a consequence of differences in global versus cell-specific (CD11b + cell) deletion.”
BackgroundSynapse development is regulated by microglial THIK-1 K + channels
Izquierdo, P., Shiina, H., Hirunpattarasilp, C., Gillis, G., & Attwell, D. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2106294118 · Cited by 37 · cited 2× · see citing works
“43,44 Previous work showed that microglial surveillance of the brain parenchyma was dependent on expression of THIK-1 44 (Figure 2A).”
BackgroundMicroglia Enable Cross-Modal Plasticity by Removing Inhibitory Synapses
Hashimoto, A., Kawamura, N., Tarusawa, E., Takeda, I., Aoyama, Y., Ohno, N., Inoue, M., Kagamiuchi, M., Kato, D., Matsumoto, M., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112383 · Cited by 36 · cited 2× · see citing works
“54 Cross-modal plasticity occurs when brain circuits reorganize to integrate functions of two or more sensory modalities, usually as a result of a decrease in a specific sensory input.”
BackgroundBosch, A. J. T., Keller, L., Steiger, L., Rohm, T. V., Wiedemann, S. J., Low, A. J. Y., Stawiski, M., Rachid, L., Roux, J., Konrad, D., et al. (2023) · Diabetologia · doi:10.1007/s00125-023-06007-1 · Cited by 31 · see citing works
Elevated TNF-α Leads to Neural Circuit Instability in the Absence of Interferon Regulatory Factor 8
Feinberg, P. A., Becker, S. C., Chung, L., Ferrari, L. L., Stellwagen, D., Anaclet, C., Durán‐Laforet, V., Faust, T. E., Sumbria, R. K., & Schafer, D. P. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0601-22.2022 · Cited by 28 · see citing works
Self-citationGABA-receptive microglia selectively sculpt developing inhibitory circuits
Favuzzi, E., Huang, S.-H., Saldi, G.-A., Binan, L., Ibrahim, L., Fernandez-Otero, M., Cao, Y., Zeine, A., Sefah, A., Zheng, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.10.009 · Cited by 13 · see citing works
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Glioblastoma microenvironment—from biology to therapyPreprint
Read, R. D., Tapp, Z. M., Rajappa, P., & Hambardzumyan, D. (2024) · Genes & Development · doi:10.1101/gad.351427.123 · Cited by 46 · see citing works
“For example, synaptic plasticity is regulated by microglia (Duran Laforet and Schafer 2024), but their role in malignant synaptic networks is not yet known.”
BackgroundMicroglia-astrocyte crosstalk regulates synapse remodeling via Wnt signaling
Faust, T. E., Lee, Y., O’Connor, C. D., Boyle, M. A., Gunner, G., Durán‐Laforet, V., Ferrari, L. L., Murphy, R. E., Badimon, A., Sakers, K., et al. (2025) · Cell · doi:10.1016/j.cell.2025.08.023 · Cited by 81 · see citing works
Self-citationHow microglia contribute to the induction and maintenance of neuropathic pain
Malcangio, M., & Sideris-Lampretsas, G. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00914-5 · Cited by 66 · see citing works
Modulation of host immunity by sensory neurons.
Saraiva-Santos, T., Zaninelli, T. H., & Pinho-Ribeiro, F. A. (2024) · Trends in immunology · doi:10.1016/j.it.2024.03.005 · Cited by 34 · see citing works
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Tryptophan Metabolism Through the Kynurenine Pathway in Glial Cells
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“CX3CL1 release by neurons is activity-dependent and inflammatory stimuli drive CX3CL1 release, which consequently regulates microglia activation and exerts neuroprotective effects [89,90].”
BackgroundBaumann, N. S., Sears, J. C., & Broadie, K. (2024) · Cellular Signalling · doi:10.1016/j.cellsig.2024.111224 · Cited by 10 · see citing works
Bridlance, C., Viguier, S., Olivié, N., Dupont, E., Thobois, D., Mathieu, B., Jiang, J. X., López‐Bendito, G., Greter, M., Becher, B., et al. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00625-8 · Cited by 6 · see citing works
“1 (floxed stop), Emx1Cre/+ ; Csf1fl/fl , and Cx3cr1Cre/+ ; Csf1fl/fl mice the authors interrogate the roles of neural activity, neural Csf1, and microglial Csf1 on microglial colonization.”
Molecular Physiology of the Neuronal Synapse
Ramírez-Expósito, M. J., Cueto-Ureña, C., & Martínez-Martos, J. M. (2026) · Current Issues in Molecular Biology · doi:10.3390/cimb48010088 · Cited by 6 · see citing works
Jäntti, H., Michels, S., Cherubini, E., Giniatullin, R. A., & Malm, T. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106275 · Cited by 9 · see citing works
Role of Neural Circuits in Cognitive Impairment
Zhang, L., Liu, G., Peng, Y., Gao, J., & Tian, M. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04309-3 · Cited by 6 · see citing works
Potential roles for microglia in drug addiction: Adolescent neurodevelopment and beyond
Martinez, M. X., & Mahler, S. V. (2025) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2025.578600 · Cited by 5 · see citing works
The Microbiota Shapes Central Nervous System Myelination in Early Life
Lynch, C. M. K., Knox, E. G., Soong, D. Y. H., Bastiaanssen, T. F. S., Trontti, K., Tofani, G. S. S., Ivaschuk, S., Collins, M., Arafa, D., Nagpal, J. K., et al. (2026) · Advanced Science · doi:10.1002/advs.202515671 · Cited by 4 · see citing works
“Microglia, the innate immune cells of the brain, play a crucial role in sensing neural activity, regulating developmental myelination, and shaping neuronal circuits accordingly [ 38, 39 ].”
The neuronal-like behaviour of macrophages
Giovanni, S. D. (2025) · Trends in Cell Biology · doi:10.1016/j.tcb.2025.04.003 · Cited by 1 · see citing works
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Microglia: Mediators of experience-driven corrective neuroplasticity
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“MGCs, which are yolk sac-derived, colonize brain regions undergoing circuit assembly, engulfing opsonized synapses in an activity-dependent manner (Tremblay et al. 2010; Schafer et al. 2012; Wu et al. 2015; Thion and Garel, 2017; Faust et al. 2021; Laforet and Schafer 2024).”
Trogocytosis: Emerging insights into cellular communication, immunity, and pathogenesis
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Adaptive Immune Signals Shape Neural Circuit Development Through CNS Border-Glia Pathways.
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“Microglia can affect neural activity by modulating synapse formation, neural activity, and immune function [31,32].”
Brain Synapses: Neurons, Astrocytes, and Extracellular Vesicles in Health and Diseases
Meldolesi, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010159
Dysfunction of microglia-mediated synaptic pruning in Autism spectrum disorderPreprint
Yu, C., Zhang, X., & Wang, W. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.20.665801
“Synapse Typically, microglia sense synaptic activity and modulate the synapse numbers 15 .”
Spinal Cord Microglia in the Development of Touch
Eschenbacher, K. M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1200-24.2024
- Authors
- Durán Laforet, V., & Schafer, D. P.
- Affiliations
- Department of Neurobiology, Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School Worcester Massachusetts USA
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Schafer, Dorothy P.
- ORCID
- Schafer, Dorothy P.
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 2024-01-31
- Volume
- 1533
- Issue
- 1
- Pages
- 38-50
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- PMC
- PMC10976428
- OpenAlex
- W4391404951
- Cited by
- 32
- References
- 98
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 7
- FWCI
- 1.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- BrightFocus Foundation (A2022006F)
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (n/a)
- National Institute of Mental Health (NIMH‐R01MH113743)
- Alzheimer's Association (AARF‐22‐923219)
- National Institute on Aging (NIA‐RF1AG068281)
- National Institute of Neurological Disorders and Stroke (NINDS‐R01NS117533)
- Simons Foundation Autism Research Initiative (957585DS)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- microglia, synaptic pruning, synapse number, spontaneous neuronal activity, experience-dependent plasticity, CNS macrophages
- MeSH terms
- Central Nervous System, Humans, Macrophages, Neurons, Synapses, Microglia
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