Control of Synapse Number by Glia
Abstract
Although astrocytes constitute nearly half of the cells in our brain, their function is a long-standing neurobiological mystery. Here we show by quantal analyses, FM1-43 imaging, immunostaining, and electron microscopy that few synapses form in the absence of glial cells and that the few synapses that do form are functionally immature. Astrocytes increase the number of mature, functional synapses on central nervous system (CNS) neurons by sevenfold and are required for synaptic maintenance in vitro. We also show that most synapses are generated concurrently with the development of glia in vivo. These data demonstrate a previously unknown function for glia in inducing and stabilizing CNS synapses, show that CNS synapse number can be profoundly regulated by nonneuronal signals, and raise the possibility that glia may actively participate in synaptic plasticity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Many original articles, reviews, and textbooks state that the human brain has 100 billion neurons and 10 times more glial cells, usually without citing references.
“Many original articles, reviews and textbooks affirm that we have 100 billion neurons and 10 times more glial cells (Kandel et al., 2000; Ullian et al., 2001; Doetsch, 2003; Nishiyama et al., 2005; Noctor et al., 2007; Allen and Barres, 2009), usually with no references cited.”
From The human brain in numbers: a linearly scaled-up primate brain (2009) · cites this paper as Ullian et al., 2001
Cites
Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse
Geppert, M., Goda, Y., Hammer, R. E., Li, C., Rosahl, T. W., Stevens, C. F., & Südhof, T. C. (1994) · Cell · doi:10.1016/0092-8674(94)90556-8 · Cited by 1,483 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Astrocytes: Biology and pathology
Sofroniew, M. V., & Vinters, H. V. (2010) · Acta Neuropathologica · doi:10.1007/s00401-009-0619-8 · Cited by 5,196 · see citing works
The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
Self-citationZhang, Y., Sloan, S. A., Clarke, L. E., Caneda, C., Plaza, C. A., Blumenthal, P. D., Vogel, H., Steinberg, G. K., Edwards, M. S. B., Li, G., et al. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.013 · Cited by 2,295 · see citing works
Self-citationAzevedo, F. A. C., Carvalho, L. R. B., Grinberg, L. T., Farfel, J. M., Ferretti, R. E. L., Leite, R. E. P., Filho, W. J., Lent, R., & Herculano‐Houzel, S. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21974 · Cited by 2,337 · see citing works
The human brain in numbers: a linearly scaled-up primate brain
Herculano-Houzel, S. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.031.2009 · Cited by 1,778 · see citing works
“Recent efforts to support this uniqueness have focused on fi nding genetic differences between humans and other primates (reviewed in Vallender, 2008), as well as cellular particularities such as the presence and distribution of Von Economo neurons (Nimchinsky et al., 1999; but see Butti et al.,…”
CNS synaptogenesis promoted by glia-derived cholesterol
Mauch, D. H., Nägler, K., Schumacher, S., Göritz, C., Müller, E.-C., Otto, A., & Pfrieger, F. W. (2001) · Science · doi:10.1126/science.294.5545.1354 · Cited by 1,711 · see citing works
Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis
Christopherson, K. S., Ullian, E. M., Stokes, C. C. A., Mullowney, C. E., Hell, J. W., Agah, A., Lawler, J., Mosher, D. F., Bornstein, P., & Barres, B. A. (2005) · Cell · doi:10.1016/j.cell.2004.12.020 · Cited by 1,688 · see citing works
Self-citationFunctional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture
Paşca, A. M., Sloan, S. A., Clarke, L. E., Tian, Y., Makinson, C. D., Huber, N., Kim, C. H., Park, J.-Y., O'Rourke, N. A., Nguyen, K. D., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3415 · Cited by 1,609 · see citing works
Self-citationAstroglia induce neurogenesis from adult neural stem cells
Song, H., Stevens, C. F., & Gage, F. H. (2002) · Nature · doi:10.1038/417039a · Cited by 1,452 · see citing works
The Mystery and Magic of Glia: A Perspective on Their Roles in Health and Disease
Barres, B. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.013 · Cited by 1,352 · see citing works
Self-citationControl of Synaptic Strength by Glial TNFα
Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattie, M. S., & Malenka, R. C. (2002) · Science · doi:10.1126/science.1067859 · Cited by 1,344 · see citing works
The cellular neurobiology of depression
Manji, H. K., Drevets, W. C., & Charney, D. S. (2001) · Nature Medicine · doi:10.1038/87865 · Cited by 1,182 · see citing works
von Bartheld, C. S., Bahney, J., & Herculano‐Houzel, S. (2016) · Journal of Comparative Neurology · doi:10.1002/cne.24040 · Cited by 1,063 · see citing works
Astrocyte reactivity and reactive astrogliosis: costs and benefits
Pekny, M., & Pekna, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2013 · Cited by 934 · see citing works
Eroglu, Ç., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Özkan, E., Chakraborty, C., Mulinyawe, S. B., Annis, D. S., Huberman, A. D., et al. (2009) · Cell · doi:10.1016/j.cell.2009.09.025 · Cited by 893 · see citing works
Self-citationAstrocytes Control Synapse Formation, Function, and Elimination
Chung, W.-S., Allen, N. J., & Eroglu, C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020370 · Cited by 839 · see citing works
Regulation of synaptic connectivity by glia.
Eroglu, C., & Barres, B. A. (2010) · Nature · doi:10.1038/nature09612 · Cited by 813 · see citing works
“Under these conditions, RGCs show little spontaneous synapse activity and form few synapses, whereas RGCs cultured in the presence of a feeding layer of astrocytes or astrocyte-conditioned medium show about tenfold more excitatory synapse activity and a fivefold to sevenfold increase in the number of synapse”
BackgroundSelf-citationSulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo
Nimmerjahn, A., Kirchhoff, F., Kerr, J. N. D., & Helmchen, F. (2004) · Nature Methods · doi:10.1038/nmeth706 · Cited by 784 · see citing works
Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors
Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., & Barres, B. A. (2012) · Nature · doi:10.1038/nature11059 · Cited by 764 · see citing works
Self-citationAstrocytic complexity distinguishes the human brain
Oberheim, N. A., Wang, X., Goldman, S., & Nedergaard, M. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.08.004 · Cited by 739 · see citing works
Astrocytes and disease: a neurodevelopmental perspective
Molofsky, A. V., Krenick, R., Ullian, E., Tsai, H.-H., Deneen, B., Richardson, W. D., Barres, B. A., & Rowitch, D. H. (2012) · Genes & Development · doi:10.1101/gad.188326.112 · Cited by 682 · see citing works
Self-citationHarrison, P. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1761-y · Cited by 693 · see citing works
Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC
Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., Chakraborty, C., Workman, G., Weaver, M., Sage, E. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104977108 · Cited by 642 · see citing works
Self-citationThe blood-brain barrier: an engineering perspective
Wong, A. D., Ye, M., Levy, A. F., Rothstein, J. D., Bergles, D. E., & Searson, P. C. (2013) · Frontiers in Neuroengineering · doi:10.3389/fneng.2013.00007 · Cited by 662 · see citing works
Wilhelmsson, U., Bushong, E. A., Price, D. L., Smarr, B. L., Phung, V., Terada, M., Ellisman, M. H., & Pekny, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602841103 · Cited by 643 · see citing works
Cotter, D. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.386 · Cited by 634 · see citing works
Astrocyte Pathology in Major Depressive Disorder: Insights from Human Postmortem Brain Tissue
Rajkowska, G., & Stockmeier, C. (2013) · Current Drug Targets · doi:10.2174/13894501113149990156 · Cited by 603 · see citing works
Sloan, S. A., Darmanis, S., Huber, N., Khan, T. A., Birey, F., Caneda, C., Reimer, R., Quake, S. R., Barres, B. A., & Paşca, S. P. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.035 · Cited by 593 · see citing works
Self-citationNeurotoxic reactive astrocytes induce cell death via saturated lipids
Guttenplan, K. A., Weigel, M. K., Prakash, P., Wijewardhane, P. R., Hasel, P., Rufen-Blanchette, U., Münch, A. E., Blum, J. A., Fine, J., Neal, M. C., et al. (2021) · Nature · doi:10.1038/s41586-021-03960-y · Cited by 578 · see citing works
Self-citationLocal 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 · see citing works
ApoE2, ApoE3, and ApoE4 Differentially Stimulate APP Transcription and Aβ Secretion
Huang, Y.-W. A., Zhou, B., Wernig, M., & Südhof, T. C. (2017) · Cell · doi:10.1016/j.cell.2016.12.044 · Cited by 528 · see citing works
The Indispensable Roles of Microglia and Astrocytes during Brain Development
Reemst, K., Noctor, S. C., Lucassen, P. J., & Hol, E. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00566 · Cited by 516 · see citing works
Activity-dependent structural and functional plasticity of astrocyte-neuron interactions
Theodosis, D. T., Poulain, D. A., & Oliet, S. H. R. (2008) · Physiological Reviews · doi:10.1152/physrev.00036.2007 · Cited by 531 · see citing works
Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C., Poo, M., & Duan, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2431073100 · Cited by 533 · see citing works
Bialas, A. R., & Stevens, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3560 · Cited by 519 · see citing works
RetractedControl of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling
Murai, K. K., Nguyen, L. N., Irie, F., Yamaguchi, Y., & Pasquale, E. B. (2003) · Nature Neuroscience · doi:10.1038/nn994 · Cited by 516 · see citing works
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
Morales, I., Guzmán-MartÃnez, L., Cerda-Troncoso, C., FarÃas, G. A., & Maccioni, R. B. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00112 · Cited by 490 · see citing works
Wilhelmsson, U., Li, L., Pekna, M., Berthold, C.-H., Blom, S., Eliasson, C., Renner, O., Bushong, E., Ellisman, M., Morgan, T. E., et al. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0820-04.2004 · Cited by 455 · see citing works
A neuron–glia signalling network in the active brain
Bezzi, P., & Volterra, A. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00223-3 · Cited by 446 · see citing works
Astrocytes accumulate Aβ42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains
Nagele, R. G., D’Andrea, M. R., Lee, H., Venkataraman, V., & Wang, H.-Y. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02361-8 · Cited by 416 · see citing works
The neurobiology of long COVID
Monje, M., & Iwasaki, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.006 · Cited by 415 · see citing works
Do glia drive synaptic and cognitive impairment in disease?
Chung, W.-S., Welsh, C. A., Barres, B. A., & Stevens, B. (2015) · Nature Neuroscience · doi:10.1038/nn.4142 · Cited by 385 · see citing works
Self-citationAstrocyte regulation of synaptic behavior
Allen, N. J. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013053 · Cited by 343 · see citing works
Serio, A., Bilican, B., Barmada, S. J., Ando, D. M., Zhao, C., Siller, R., Burr, K., Haghi, G., Story, D., Nishimura, A. L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300398110 · Cited by 345 · see citing works
Cetaceans have complex brains for complex cognition
Marino, L., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, P. R., Lefebvre, L., Lusseau, D., McCowan, B., Nimchinsky, E. A., Pack, A. A., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050139 · Cited by 339 · see citing works
Dynamics and Mechanisms of CNS Myelination
Bercury, K. K., & Macklin, W. B. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.016 · Cited by 320 · see citing works
Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q., & Anderson, D. J. (2008) · Cell · doi:10.1016/j.cell.2008.02.046 · Cited by 331 · see citing works
Johnson, M. A., Weick, J. P., Pearce, R. A., & Zhang, S.-C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4562-06.2007 · Cited by 318 · see citing works
Outsourcing in the brain: Do neurons depend on cholesterol delivery by astrocytes?
Pfrieger, F. W. (2003) · BioEssays · doi:10.1002/bies.10195 · Cited by 308 · see citing works
Inflammation, Glutamate, and Glia in Depression:<i>A Literature Review</i>
McNally, L., Bhagwagar, Z., & Hannestad, J. (2008) · CNS Spectrums · doi:10.1017/s1092852900016734 · Cited by 289 · see citing works
Graham, A. M., Rasmussen, J. M., Rudolph, M. D., Heim, C. M., Gilmore, J. H., Styner, M., Potkin, S. G., Entringer, S., Wadhwa, P. D., Fair, D. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.05.027 · Cited by 282 · see citing works
Synaptic Changes in Alzheimer's Disease
Gylys, K. H., Fein, J. A., Yang, F., Wiley, D. J., Miller, C. A., & Cole, G. M. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63436-0 · Cited by 253 · see citing works
Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain
Alfonso-Loeches, S., & Guerri, C. (2011) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2011.580567 · Cited by 254 · see citing works
An epigenetic barrier sets the timing of human neuronal maturation
Ciceri, G., Baggiolini, A., Cho, H. S., Kshirsagar, M., Benito-Kwiecinski, S., Walsh, R. M., Aromolaran, K. A., Gonzalez-Hernandez, A. J., Munguba, H., Koo, S. Y., et al. (2024) · Nature · doi:10.1038/s41586-023-06984-8 · Cited by 240 · see citing works
Tchieu, J., Calder, E. L., Guttikonda, S. R., Gutzwiller, E. M., Aromolaran, K. A., Steinbeck, J. A., Goldstein, P. A., & Studer, L. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0035-0 · Cited by 231 · see citing works
Garwood, C. J., Ratcliffe, L. E., Simpson, J. E., Heath, P. R., Ince, P. G., & Wharton, S. B. (2017) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12338 · Cited by 233 · see citing works
Astrocytes locally translate transcripts in their peripheral processes
Sakers, K., Lake, A. M., Khazanchi, R., Ouwenga, R., Vasek, M. J., Dani, A., & Dougherty, J. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617782114 · Cited by 202 · see citing works
Chen, C., Jiang, P., Xue, H., Peterson, S. E., Tran, H. T., McCann, A. E., Parast, M. M., Li, S., Pleasure, D. E., Laurent, L. C., et al. (2014) · Nature Communications · doi:10.1038/ncomms5430 · Cited by 219 · see citing works
Bridges, R., Lutgen, V., Lobner, D., & Baker, D. A. (2012) · Pharmacological Reviews · doi:10.1124/pr.110.003889 · Cited by 205 · see citing works
Faissner, A., Pyka, M., Geissler, M., Sobik, T., Frischknecht, R., Gundelfinger, E. D., & Seidenbecher, C. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.01.001 · Cited by 207 · see citing works
A crucial role for Olig2 in white matter astrocyte development
Cai, J., Chen, Y., Cai, W.-H., Hurlock, E. C., Wu, H., Kernie, S. G., Parada, L. F., & Lu, Q. R. (2007) · Development · doi:10.1242/dev.02847 · Cited by 203 · see citing works
Farhy-Tselnicker, I., van Casteren, A. C. M., Lee, A., Chang, V. T., Aricescu, A. R., & Allen, N. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.053 · Cited by 199 · see citing works
Neuronal Pentraxins Mediate Synaptic Refinement in the Developing Visual System
Bjartmar, L., Huberman, A. D., Ullian, E. M., Renteria, R. C., Liu, X., Xu, W., Prezioso, J., Susman, M. W., Stellwagen, D., Stokes, C. C., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4212-05.2006 · Cited by 179 · see citing works
Self-citationMAP Kinase Activation by Fluoxetine and Its Relation to Gene Expression in Cultured Rat Astrocytes
Mercier, G., Lennon, A. M., Renouf, B., Dessouroux, A., Ramaugé, M., Courtin, F., & Pierre, M. (2004) · Journal of Molecular Neuroscience · doi:10.1385/jmn:24:2:207 · Cited by 176 · see citing works
Altered emotional behavioral responses in mice lacking brain‐type fatty acid‐binding protein gene
Owada, Y., Abdelwahab, S. A., Kitanaka, N., Sakagami, H., Takano, H., Sugitani, Y., Sugawara, M., Kawashima, H., Kiso, Y., Mobarakeh, J. I., et al. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04855.x · Cited by 154 · see citing works
Microglial priming of antigen presentation and adaptive stimulation in Alzheimer’s disease
Das, R., & Chinnathambi, S. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03132-2 · Cited by 147 · see citing works
Osipovitch, M., Asenjo Martinez, A., Mariani, J. N., Cornwell, A., Dhaliwal, S., Zou, L., Chandler-Militello, D., Wang, S., Li, X., Benraiss, S.-J., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2018.11.010 · Cited by 120 · see citing works
Blood, A. J., Iosifescu, D. V., Makris, N., Perlis, R. H., Kennedy, D. N., Dougherty, D. D., Kim, B. W., Lee, M. J., Wu, S., Lee, S., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013945 · Cited by 126 · see citing works
Panossian, A., Seo, E.-J., & Efferth, T. (2018) · Phytomedicine · doi:10.1016/j.phymed.2018.09.204 · Cited by 127 · see citing works
Role of glial cells in the formation and maintenance of synapses
Pfrieger, F. W. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.11.002 · Cited by 124 · see citing works
Garcia, O., Torres, M., Helguera, P., Coskun, P., & Busciglio, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014200 · Cited by 122 · see citing works
Tracking neuroinflammation in Alzheimer’s disease: the role of positron emission tomography imaging
Zimmer, E. R., Leuzy, A., Benedet, A. L., Breitner, J., Gauthier, S., & Rosa-Neto, P. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-120 · Cited by 121 · see citing works
Astrocyte–neuron interplay in maladaptive plasticity.
Papa, M., De Luca, C., Petta, F., Alberghina, L., & Cirillo, G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.010 · Cited by 104 · see citing works
Interleukins, Inflammation, and Mechanisms of Alzheimer's Disease
Weisman, D., Hakimian, E., & Ho, G. J. (2006) · Vitamins & Hormones · doi:10.1016/s0083-6729(06)74020-1 · Cited by 95 · see citing works
Zhang, Z., Bassam, B., Thomas, A. G., Williams, M., Liu, J., Nance, E., Rojas, C., Slusher, B. S., & Kannan, S. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.06.010 · Cited by 84 · see citing works
Human neuronal maturation comes of age: cellular mechanisms and species differences
Wallace, J. L., & Pollen, A. A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00760-3 · Cited by 82 · see citing works
Falcone, C., Penna, E., Hong, T., Tarantal, A. F., Hof, P. R., Hopkins, W. D., Sherwood, C. C., Noctor, S. C., & Martínez-Cerdeño, V. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhaa231 · Cited by 72 · see citing works
Long-term culture of astrocytes attenuates the readily releasable pool of synaptic vesicles
Kawano, H., Katsurabayashi, S., Kakazu, Y., Yamashita, Y., Kubo, N., Kubo, M., Okuda, H., Takasaki, K., Kubota, K., Mishima, K., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048034 · Cited by 68 · see citing works
Astrocyte modulation of in vitro β‐amyloid neurotoxicity
Paradisi, S., Sacchetti, B., Balduzzi, M., Gaudi, S., & Malchiodi‐Albedi, F. (2004) · Glia · doi:10.1002/glia.20005 · Cited by 68 · see citing works
Bridging the gap: microfluidic devices for short and long distance cell–cell communication
Vu, T. Q., de Castro, R. M. B., & Qin, L. (2017) · Lab on a Chip · doi:10.1039/c6lc01367h · Cited by 63 · see citing works
The Role of the Classical Complement Cascade in Synapse Loss During Development and Glaucoma
Rosen, A. M., & Stevens, B. (2010) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4419-5635-4_6 · Cited by 60 · see citing works
Krzisch, M., Temprana, S. G., Mongiat, L. A., Armida, J., Schmutz, V., Virtanen, M. A., Kocher-Braissant, J., Kraftsik, R., Vutskits, L., Conzelmann, K.-K., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0768-y · Cited by 57 · see citing works
Redefining varicose projection astrocytes in primates.
Falcone, C., McBride, E. L., Hopkins, W. D., Hof, P. R., Manger, P. R., Sherwood, C. C., Noctor, S. C., & Martínez‐Cerdeño, V. (2022) · Glia · doi:10.1002/glia.24093 · Cited by 56 · see citing works
Calcium-Sensing Receptors of Human Neural Cells Play Crucial Roles in Alzheimer's Disease
Chiarini, A., Armato, U., Liu, D., & Dal Prà, I. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00134 · Cited by 51 · see citing works
The presence of apoE4, not the absence of apoE3, contributes to AD pathology
Teter, B., Raber, J., Nathan, B., & Crutcher, K. A. (2002) · Journal of Alzheimer's Disease · doi:10.3233/jad-2002-4305 · Cited by 37 · see citing works
Astrocytes, emerging stars of energy homeostasis
Camandola, S. (2018) · Cell Stress · doi:10.15698/cst2018.10.157 · Cited by 25 · see citing works
Sun, X., Pan, S., Li, D., Su, M., Zheng, H., Zhang, Y.-W., & Li, Y. (2025) · The Journal of Neuroscience · doi:10.1523/jneurosci.0967-24.2025 · Cited by 4 · see citing works
- Authors
- Ullian, E. M., Sapperstein, S. K., Christopherson, K. S., & Barres, B. A.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Ullian, Erik M.
- Venue
- Science
- Published
- 2001-01-26
- Volume
- 291
- Issue
- 5504
- Pages
- 657-661
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2031611126
- Cited by
- 1,380
- References
- 1
- Citations by year
- 2026: 33 · 2025: 30 · 2024: 43 · 2023: 48 · 2022: 47 · 2021: 68 · 2020: 44 · 2019: 45 · 2018: 49 · 2017: 59 · 2016: 72 · 2015: 39 · 2014: 64 · 2013: 58 · 2012: 53
- FWCI
- 31.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1f32ns010784-01)
- National Institute of Neurological Disorders and Stroke (NS10784)
- 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
- astrocytes, glial cells, synapse number, synapse maturation, synapse maintenance, glial development, synaptic plasticity, central nervous system neurons, neuron-glia interactions
- MeSH terms
- Quaternary Ammonium Compounds, Animals, Astrocytes, Calcium, Calcium-Binding Proteins, Cell Communication, Cells, Cultured, Fluorescent Dyes, Membrane Glycoproteins, Microscopy, Electron, Nerve Tissue Proteins, Synaptic Transmission, Neuronal Plasticity, Pyridinium Compounds, Retinal Ganglion Cells, Superior Colliculi, Synapses, Synaptic Vesicles, Ionomycin, Synaptophysin, Rats, Sprague-Dawley, Patch-Clamp Techniques, Glutamic Acid, Coculture Techniques, Excitatory Postsynaptic Potentials, Synaptotagmins, Rats
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