How microglia sense and regulate neuronal activity

Umpierre, Anthony D.; Wu, Long‐Jun

doi:10.1002/glia.23961

Cited by 241Neuroinflammation and Neurodegeneration MechanismsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

How microglia sense and regulate neuronal activity

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Umpierre, Anthony D., Wu, Long‐Jun·2021·Glia

DOI 10.1002/glia.23961PMC PMC8113084

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Abstract

Microglia are innate immune cells of the central nervous system that sense extracellular cues. Brain injuries, inflammation, and pathology evoke dynamic structural responses in microglia, altering their morphology and motility. The dynamic motility of microglia is hypothesized to be a critical first step in sensing local alterations and engaging in pattern-specific responses. Alongside their pathological responses, microglia also sense and regulate neuronal activity. In this review, we consider the extracellular molecules, receptors, and mechanisms that allow microglia to sense neuronal activity changes under both hypoactivity and hyperactivity. We also highlight emerging in vivo evidence that microglia regulate neuronal activity, ranging from physiological to pathophysiological conditions. In addition, we discuss the emerging role of calcium signaling in microglial responses to the extracellular environment. The dynamic function of microglia in monitoring and influencing neuronal activity may be critical for brain homeostasis and circuit modification in health and disease.

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Ca2+ currents have been implicated in the regulation of microglial motility.
“Ca2+ currents have also been implicated in the regulation of microglial motility (reviewed in [50]).”
From Heterozygous expression of the Alzheimer’s disease-protective PLCγ2 P522R variant enhances Aβ clearance while preserving synapses (2022) · cites this paper as [50]

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Modulation of Microglial Process Convergence Toward Neuronal Dendrites by Extracellular Calcium
Eyo, U. B., Gu, N., De, S., Dong, H., Richardson, J. R., & Wu, L.-J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3279-14.2015 · Cited by 154 · see citing works
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Microglial calcium signal acts as a rapid sensor of single neuron damage in vivo
Eichhoff, G., Brawek, B., & Garaschuk, O. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.10.018 · Cited by 148 · see citing works
Astrocyte-microglia interaction drives evolving neuromyelitis optica lesion
Chen, T., Lennon, V. A., Liu, Y., Bosco, D. B., Li, Y., Yi, M., Zhu, J., Wei, S., & Wu, L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci134816 · Cited by 147 · see citing works
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Inhibition of UDP/P2Y6 purinergic signaling prevents phagocytosis of viable neurons by activated microglia in vitro and in vivo
Neher, J. J., Neniškytė, U., Hornik, T. C., & Brown, G. C. (2014) · Glia · doi:10.1002/glia.22693 · Cited by 143 · see citing works
REM sleep promotes experience-dependent dendritic spine elimination in the mouse cortex
Zhou, Y., Lai, C. S. W., Bai, Y., Li, W., Zhao, R., Yang, G., Frank, M. G., & Gan, W. (2020) · Nature Communications · doi:10.1038/s41467-020-18592-5 · Cited by 137 · 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
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P2Y12R-Dependent Translocation Mechanisms Gate the Changing Microglial Landscape
Eyo, U. B., Mo, M., Yi, M., Murugan, M., Liu, J., Yarlagadda, R., Margolis, D. J., Xu, P., & Wu, L. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.04.001 · Cited by 130 · see citing works
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Microglial Contact Prevents Excess Depolarization and Rescues Neurons from Excitotoxicity
Kato, G., Inada, H., Wake, H., Akiyoshi, R., Miyamoto, A., Eto, K., Ishikawa, T., Moorhouse, A. J., Strassman, A. M., & Nabekura, J. (2016) · eNeuro · doi:10.1523/eneuro.0004-16.2016 · Cited by 128 · see citing works
Microglial P2Y12 receptor regulates ventral hippocampal CA1 neuronal excitability and innate fear in mice
Peng, J., Liu, Y., Umpierre, A. D., Xie, M., Tian, D., Richardson, J. R., & Wu, L. (2019) · Molecular Brain · doi:10.1186/s13041-019-0492-x · Cited by 124 · see citing works
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Activation of mouse microglial cells affects P2 receptor signaling
Möller, T., Kann, O., Verkhratsky, A., & Kettenmann, H. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02244-1 · Cited by 123 · see citing works
Astrocyte IP3R2-dependent Ca2+ signaling is not a major modulator of neuronal pathways governing behavior
Petravicz, J., Boyt, K. M., & McCarthy, K. D. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00384 · Cited by 116 · see citing works
Bulk Loading of Calcium Indicator Dyes to Study Astrocyte Physiology: Key Limitations and Improvements Using Morphological Maps
Reeves, A. M. B., Shigetomi, E., & Khakh, B. S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0127-11.2011 · Cited by 115 · see citing works
Regulation of Physical Microglia–Neuron Interactions by Fractalkine Signaling after Status Epilepticus
Eyo, 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 · see citing works
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Receptors, Ion Channels, and Signaling Mechanisms Underlying Microglial Dynamics
Madry, C., & Attwell, D. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.637157 · Cited by 109 · cited 1× · see citing works
“However, there are additional mechanisms that also influence microglial motility (Madry & Attwell, 2015).”
Background
In vivo dynamics of innate immune sentinels in the CNS
Nayak, D., Zinselmeyer, B. H., Corps, K. N., & McGavern, D. B. (2012) · IntraVital · doi:10.4161/intv.22823 · Cited by 109 · see citing works
Impairment of in vivo calcium signaling in amyloid plaque-associated microglia
Brawek, B., Schwendele, B., Riester, K., Kohsaka, S., Lerdkrai, C., Liang, Y., & Garaschuk, O. (2014) · Acta Neuropathologica · doi:10.1007/s00401-013-1242-2 · Cited by 106 · see citing works
Neuronal and glial purinergic receptors functions in neuron development and brain disease
del Puerto, A., Wandosell, F. G., & Garrido, J. J. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00197 · Cited by 101 · see citing works
Intracellular calcium dynamics in cortical microglia responding to focal laser injury in the PC::G5-tdT reporter mouse
Pozner, A., Xu, B., Palumbos, S. D., Gee, J. M., Tvrdík, P., & Capecchi, M. R. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00012 · Cited by 94 · see citing works
Microglial P2Y12 Receptor Regulates Seizure-Induced Neurogenesis and Immature Neuronal Projections
Mo, M., Eyo, U. B., Xie, M., Peng, J., Bosco, D. B., Umpierre, A. D., Zhu, X., Tian, D., Xu, P., & Wu, L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0487-19.2019 · Cited by 93 · see citing works
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How does calcium interact with the cytoskeleton to regulate growth cone motility during axon pathfinding?
Gasperini, R., Pavez, M., Thompson, A. C., Mitchell, C. B., Hardy, H., Young, K. M., Chilton, J. K., & Foa, L. C. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.07.006 · Cited by 88 · see citing works
Resting Microglial Motility Is Independent of Synaptic Plasticity in Mammalian Brain
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The adenosine generating enzymes CD39/CD73 control microglial processes ramification in the mouse brain
Matyash, M., Zabiegalov, O., Wendt, S., Matyash, V., & Kettenmann, H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175012 · Cited by 80 · see citing works
Role of norepinephrine in the regulation of rapid eye movement sleep
Mallick, B. N., Majumdar, S., Faisal, M., Yadav, V., Madan, V., & Pal, D. (2002) · Journal of Biosciences · doi:10.1007/bf02705052 · Cited by 80 · see citing works
Induction of hippocampal long-term potentiation increases the morphological dynamics of microglial processes and prolongs their contacts with dendritic spines
Pfeiffer, T., Avignone, E., & Nägerl, U. V. (2016) · Scientific Reports · doi:10.1038/srep32422 · Cited by 79 · see citing works
Altered Expression of CX3CL1 in Patients with Epilepsy and in a Rat Model
Xu, Y., Zeng, K., Han, Y., Wang, L., Chen, D., Xi, Z., Wang, H., Wang, X., & Chen, G. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.01.024 · Cited by 78 · see citing works
The mysterious origins of microglia
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Activation of microglial P2Y12 receptor is required for outward potassium currents in response to neuronal injury
Swiatkowski, P., Murugan, M., Eyo, U. B., Wāng, Y., Rangaraju, S., Oh, S. B., & Wu, L. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.008 · Cited by 75 · see citing works
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P2X7 receptor activation regulates microglial cell death during oxygen-glucose deprivation
Eyo, U. B., Miner, S. A., Ahlers‐Dannen, K. E., Wu, L., & Dailey, M. E. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.032 · Cited by 75 · see citing works
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Microglial Displacement of GABAergic Synapses Is a Protective Event during Complex Febrile Seizures
Wan, Y., Feng, B., You, Y., Yu, J., Xu, C., Dai, H., Trapp, B. D., Shi, P. D., Chen, Z., & Hu, W. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108346 · Cited by 70 · see citing works
P2Y13 receptors regulate microglial morphology, surveillance, and resting levels of interleukin 1β release
Kyrargyri, V., Madry, C., Rifat, A., Arancibia‐Cárcamo, I. L., Jones, S. P., Chan, V. T. T., Xu, Y., Robaye, B., & Attwell, D. (2019) · Glia · doi:10.1002/glia.23719 · Cited by 69 · see citing works
Transcranial Direct Current Stimulation (tDCS) Induces Adrenergic Receptor-Dependent Microglial Morphological Changes in Mice
Mishima, T., Nagai, T., Yahagi, K., Akther, S., Oe, Y., Monai, H., Kohsaka, S., & Hirase, H. (2019) · eNeuro · doi:10.1523/eneuro.0204-19.2019 · Cited by 65 · see citing works
Selective Activation of KCa3.1 and CRAC Channels by P2Y2 Receptors Promotes Ca2+ Signaling, Store Refilling and Migration of Rat Microglial Cells
Ferreira, R., & Schlichter, L. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062345 · Cited by 62 · see citing works
Healthy Brain Aging Modifies Microglial Calcium Signaling In Vivo
Olmedillas, M., Asavapanumas, N., Uzcategui, N. L., & Garaschuk, O. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030589 · Cited by 60 · see citing works
In vivo characterization of functional states of cortical microglia during peripheral inflammation
Riester, K., Brawek, B., Savitska, D., Fröhlich, N. T., Zirdum, E., Mojtahedi, N., Heneka, M. T., & Garaschuk, O. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.12.007 · Cited by 59 · see citing works
Effects of the ecto-ATPase apyrase on microglial ramification and surveillance reflect cell depolarization, not ATP depletion
Madry, C., Arancibia‐Cárcamo, I. L., Kyrargyri, V., Chan, V. T. T., Hamilton, N. B., & Attwell, D. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1715354115 · Cited by 58 · see citing works
The GluN2A Subunit Regulates Neuronal NMDA receptor-Induced Microglia-Neuron Physical Interactions
Eyo, U. B., Bispo, A., Liu, J., Sabu, S., Wu, R., DiBona, V. L., Zheng, J., Murugan, M., Zhang, H., Tang, Y., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-19205-4 · Cited by 57 · see citing works
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Brain microdialysate monoamines in relation to circadian rhythms, sleep, and sleep deprivation - a systematic review, network meta-analysis, and new primary data
Menon, J. M. L., Nolten, C., Achterberg, E. J. M., Joosten, R. N. J. M. A., Dematteis, M., Feenstra, M. G. P., Drinkenburg, W. H. (., & Leenaars, C. H. C. (2019) · Journal of Circadian Rhythms · doi:10.5334/jcr.174 · Cited by 57 · see citing works
Complement factor C5a and epidermal growth factor trigger the activation of outward potassium currents in cultured murine microglia
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Biophysical basis for Kv1.3 regulation of membrane potential changes induced by P2X4 ‐mediated calcium entry in microglia
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In vivo imaging of dendritic spines during electrographic seizures
Rensing, N. R., Ouyang, Y., Yang, X., Yamada, K. A., Rothman, S. M., & Wong, M. L. (2005) · Annals of Neurology · doi:10.1002/ana.20658 · Cited by 51 · see citing works
Imaging P2X4 Receptor Lateral Mobility in Microglia
Toulmé, E., & Khakh, B. S. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.329334 · Cited by 47 · see citing works
Effect of Caloric Restriction on the in vivo Functional Properties of Aging Microglia
Olmedillas, M., Fröhlich, N. T., Figarella, K., Mojtahedi, N., & Garaschuk, O. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00750 · Cited by 45 · see citing works
Neuroprotective effects of microglial P2Y 1 receptors against ischemic neuronal injury
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Spontaneous Ca2+ transients in mouse microglia
Korvers, L., Costa, A. D. A., Mersch, M., Matyash, V., Kettenmann, H., & Semtner, M. (2016) · Cell Calcium · doi:10.1016/j.ceca.2016.09.004 · Cited by 44 · see citing works
CCL5 evokes calcium signals in microglia through a kinase‐, phosphoinositide‐, and nucleotide‐dependent mechanism
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Nucleotide transmitters ATP and ADP mediate intercellular calcium wave communication via P2Y12/13 receptors among BV-2 microglia
Jiang, P., Xing, F., Guo, B., Yang, J., Li, Z., Wei, W., Hu, F. Z., Lee, I., Zhang, X., Pan, L., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183114 · Cited by 42 · see citing works
New P2Y12blockers
Cattaneo, M. (2009) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2009.03382.x · Cited by 42 · see citing works
Cholinergic agonists increase intracellular Ca2+ in cultured human microglia
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Complement 3a receptor in dorsal horn microglia mediates pronociceptive neuropeptide signaling
Doolen, S., Cook, J., Riedl, M. S., Kitto, K. F., Kohsaka, S., Honda, C. N., Fairbanks, C. A., Taylor, B. K., & Vulchanova, L. (2017) · Glia · doi:10.1002/glia.23208 · Cited by 35 · see citing works
Regulation of microglia by neuromodulators: Modulations in major and minor modes
Albertini, G., Etienne, F., & Roumier, A. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135000 · Cited by 35 · see citing works
Resting microglia respond to and regulate neuronal activity in vivo
Li, Y., Du, X.-F., & Du, J. (2013) · Communicative & Integrative Biology · doi:10.4161/cib.24493 · Cited by 31 · see citing works
Extracellular acidosis impairs P2Y receptor-mediated Ca2+ signalling and migration of microglia
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Regulation of the Plasma Membrane Calcium ATPases by the actin cytoskeleton
Dalghi, M. G., Ferreira-Gomes, M., & Rossi, J. P. F. C. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.11.151 · Cited by 26 · see citing works
Augmentation of Ca2+ signaling in astrocytic endfeet in the latent phase of temporal lobe epilepsy
Szokol, K., Heuser, K., Tang, W., Jensen, V., Enger, R., Bedner, P., Steinhäuser, C., TaubÃ¸ll, E., Ottersen, O. P., & Nagelhus, E. A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00049 · Cited by 23 · see citing works
Donepezil suppresses intracellular Ca2+ mobilization through the PI3K pathway in rodent microglia
Haraguchi, Y., Mizoguchi, Y., Ohgidani, M., Imamura, Y., Murakawa‐Hirachi, T., Nabeta, H., Tateishi, H., Kato, T. A., & Monji, A. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-1033-0 · Cited by 22 · see citing works
Phosphoinositide 3-kinase γ ties chemoattractant- and adrenergic control of microglial motility
Schneble, N., Schmidt, C., Bauer, R., Müller, J. P., Monajembashi, S., & Wetzker, R. (2016) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2016.11.002 · Cited by 19 · see citing works
Microglia in Neuronal Circuits
Wu, L., Stevens, B., Duan, S., & MacVicar, B. A. (2013) · Neural Plasticity · doi:10.1155/2013/586426 · Cited by 19 · see citing works
Self-citation
IP3-Mediated Calcium Signaling Is Involved in the Mechanism of Fractalkine-Induced Hyperalgesia Response
Wang, A., Yang, T., Zhang, L., Jia, L., Wu, Q., Yao, S., Xu, J., & Yang, H. (2018) · Medical Science Monitor · doi:10.12659/msm.913787 · Cited by 14 · see citing works

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Neuronal hyperexcitability in Alzheimer's disease: what are the drivers behind this aberrant phenotype?
Targa Dias Anastacio, H., Matosin, N., & Ooi, L. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02024-7 · Cited by 401 · see citing works
YY1 lactylation in microglia promotes angiogenesis through transcription activation-mediated upregulation of FGF2
Wang, X., Fan, W., Li, N., Ma, Y., Yao, M., Wang, G., He, S., Li, W., Tan, J., Lu, Q., et al. (2023) · Genome biology · doi:10.1186/s13059-023-02931-y · Cited by 298 · see citing works
Microglia rescue neurons from aggregate-induced neuronal dysfunction and death through tunneling nanotubes
Scheiblich, H., Eikens, F., Wischhof, L., Opitz, S., Jüngling, K., Cserép, C., Schmidt, S. V., Lambertz, J., Bellande, T., Pósfai, B., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.06.029 · Cited by 207 · see citing works
Regulation of myelination by microglia
Santos, E. N., & Fields, R. D. (2021) · Science Advances · doi:10.1126/sciadv.abk1131 · Cited by 137 · see citing works
Tuning neural circuits and behaviors by microglia in the adult brain
Zhao, S., Umpierre, A. D., & Wu, L. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2023.12.003 · Cited by 116 · see citing works
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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 · see citing works
Microglia in epilepsy
Yu, C. J., Deng, X., & Xu, D. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106249 · Cited by 112 · see citing works
Microglia and astrocytes underlie neuroinflammation and synaptic susceptibility in autism spectrum disorder
Xiong, Y., Chen, J., & Li, Y. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1125428 · Cited by 109 · see citing works
A Richer and More Diverse Future for Microglia Phenotype
Wang, J., He, W., & Zhang, J. (2022) · Heliyon · doi:10.1016/j.heliyon.2023.e14713 · Cited by 105 · see citing works
Microglial over-pruning of synapses during development in autism-associated SCN2A-deficient mice and human cerebral organoids
Wu, J., Zhang, J., Chen, X., Wettschurack, K. W., Que, Z., Deming, B. A., Olivero-Acosta, M. I., Cui, N., Eaton, M., Zhao, Y., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02518-4 · Cited by 85 · see citing works
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Long-term diazepam treatment enhances microglial spine engulfment and impairs cognitive performance via the mitochondrial 18 kDa translocator protein (TSPO)
Shi, Y., Cui, M., Ochs, K., Brendel, M., Strübing, F., Briel, N., Eckenweber, F., Zou, C., Banati, R. B., Liu, G. J., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01013-9 · Cited by 85 · see citing works
Microglia sense neuronal activity via GABA in the early postnatal hippocampus
Logiacco, F., Xia, P., Georgiev, S. V., Franconi, C., Chang, Y.-J., Ugursu, B., Sporbert, A., Kühn, R., Kettenmann, H., & Semtner, M. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110128 · Cited by 72 · see citing works
An inducible genetic tool to track and manipulate specific microglial states reveals their plasticity and roles in remyelination
Barclay, K. M., Abduljawad, N., Cheng, Z., Kim, M. W., Zhou, L., Yang, J., Rustenhoven, J., Mazzitelli, J. A., Smyth, L. C. D., Kapadia, D., et al. (2024) · Immunity · doi:10.1016/j.immuni.2024.05.005 · Cited by 65 · see citing works
Neuronal signal-regulatory protein alpha drives microglial phagocytosis by limiting microglial interaction with CD47 in the retina
Jiang, D., Burger, C. A., Akhanov, V., Liang, J. H., Mackin, R. D., Albrecht, N. E., Andrade, P., Schafer, D. P., & Samuel, M. A. (2022) · Immunity · doi:10.1016/j.immuni.2022.10.018 · Cited by 62 · see citing works
Mechanisms of microglia-mediated synapse turnover and synaptogenesis
Ball, J. B., Green‐Fulgham, S. M., & Watkins, L. R. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102336 · Cited by 63 · see citing works
Calcium and activity-dependent signaling in the developing cerebral cortex
Arjun McKinney, A., Petrova, R., & Panagiotakos, G. (2022) · Development · doi:10.1242/dev.198853 · Cited by 55 · see citing works
NFAT1 Orchestrates Spinal Microglial Transcription and Promotes Microglial Proliferation via c‐MYC Contributing to Nerve Injury‐Induced Neuropathic Pain
Jiang, B., Ding, T., Guo, C., Bai, X., Cao, D., Wu, X., Sha, W., Jiang, M., Wu, L., & Gao, Y. (2022) · Advanced Science · doi:10.1002/advs.202201300 · Cited by 54 · see citing works
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Neurovascular adaptations modulating cognition, mood, and stress responses
Dion‐Albert, L., Dudek, K., Russo, S. J., Campbell, M., & Ménard, C. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.01.005 · Cited by 51 · see citing works
Cognitive Impairments, Neuroinflammation and Blood–Brain Barrier Permeability in Mice Exposed to Chronic Sleep Fragmentation during the Daylight Period
Puech, C., Badran, M., Runion, A. R., Barrow, M. B., Cataldo, K., & Gozal, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129880 · Cited by 56 · see citing works
Sleep restoration by optogenetic targeting of GABAergic neurons reprograms microglia and ameliorates pathological phenotypes in an Alzheimer’s disease model
Zhao, Q., Maci, M., Miller, M. R., Zhou, H., Zhang, F., Algamal, M., Lee, Y. F., Hou, S. S., Perle, S. J., Le, H., et al. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00682-9 · Cited by 52 · see citing works
Chemogenetic and Optogenetic Manipulations of Microglia in Chronic Pain
Parusel, S., Yi, M., Hunt, C., & Wu, L. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00937-3 · Cited by 51 · see citing works
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Microglia efferocytosis: an emerging mechanism for the resolution of neuroinflammation in Alzheimer’s disease
Chen, Y., Kou, Y., Ni, Y., Yang, H., Xu, C., Fan, H., & Liu, H. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03428-0 · Cited by 51 · see citing works
Peripheral nervous system microglia-like cells regulate neuronal soma size throughout evolution
Wu, Z., Wang, Y., Chen, W., Sun, H., Chen, X., Li, X., Wang, Z., Liang, W., Wang, S.-Y., Luan, X., et al. (2025) · Cell · doi:10.1016/j.cell.2025.02.007 · Cited by 53 · see citing works
Microglia in Health and Diseases: Integrative Hubs of the Central Nervous System (CNS)
Sierra, A., Miron, V. E., Paolicelli, R. C., & Ransohoff, R. M. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041366 · Cited by 47 · see citing works
Microglia as integrators of brain-associated molecular patterns
Escoubas, C. C., & Molofsky, A. V. (2024) · Trends in Immunology · doi:10.1016/j.it.2024.03.009 · Cited by 46 · see citing works
The Role of Inflammation in Neurodegenerative Diseases: Parkinson’s Disease, Alzheimer’s Disease, and Multiple Sclerosis
Fołta, J., Rzepka, Z., & Wrześniok, D. M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115177 · Cited by 47 · see citing works
Regulation of cortical hyperexcitability in amyotrophic lateral sclerosis: focusing on glial mechanisms
Xie, M., Pallegar, P. N., Parusel, S., Nguyen, A. T., & Wu, L. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00665-w · Cited by 43 · see citing works
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Authors: Umpierre, A. D., & Wu, L.
Affiliations: Mayo Clinic (US)
Corresponding author: Wu, Long‐Jun
ORCID: Umpierre, Anthony D.
Wu, Long‐Jun
Venue: Glia
Publisher: Wiley
Published: 2020-12-28
Volume: 69
Issue: 7
Pages: 1637-1653
ISSN: 0894-1491 (ISSN-L)
1098-1136
DOI: 10.1002/glia.23961
PMC: PMC8113084
OpenAlex: W3115061260
Cited by: 237
References: 137
Citations by year: 2026: 36 · 2025: 62 · 2024: 52 · 2023: 44 · 2022: 28 · 2021: 14
FWCI: 2.24
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Glia (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS088627, NS110825, NS110949, NS112144, NS114040)
National Institute on Aging (AG064159)
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, microglial motility, microglial morphology, microglial receptors, calcium signaling, neuronal hyperactivity, brain homeostasis, neuroinflammation, circuit modification
MeSH terms: Brain, Central Nervous System, Neurons, Microglia, Calcium Signaling

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How microglia sense and regulate neuronal activity

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