Microglial phagocytosis of newborn cells is induced by endocannabinoids and sculpts sex differences in juvenile rat social play
Open accessAbstract
Brain sex differences are established developmentally and generate enduring changes in circuitry and behavior. Steroid-mediated masculinization of the rat amygdala during perinatal development produces higher levels of juvenile rough-and-tumble play by males. This sex difference in social play is highly conserved across mammals, yet the mechanisms by which it is established are unknown. Here, we report that androgen-induced increases in endocannabinoid tone promote microglia phagocytosis during a critical period of amygdala development. Phagocytic microglia engulf more viable newborn cells in males; in females, less phagocytosis allows more astrocytes to survive to the juvenile age. Blocking complement-dependent phagocytosis in males increases astrocyte survival and prevents masculinization of play. Moreover, increased astrocyte density in the juvenile amygdala reduces neuronal excitation during play. These findings highlight novel mechanisms of brain development whereby endocannabinoids induce microglia phagocytosis to regulate newborn astrocyte number and shape the sexual differentiation of social circuitry and behavior. VIDEO ABSTRACT.
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
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?
Blocking testosterone by using an androgen receptor antagonist in females treated with testosterone completely prevents these effects.
“Similarly, blocking testosterone by using an androgen receptor antagonist in females treated with testosterone completely prevents these effects (VanRyzin et al., 2019).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as VanRyzin et al., 2019
The Results section ('Testosterone Programs 2-AG Content…'; page not provided) reports that flutamide, an androgen receptor antagonist, prevented the testosterone-induced increase in amygdala 2-AG in female pups. It does not show that flutamide completely prevented the other reported effects on newborn cells, microglial phagocytosis, or social play; the play experiment instead used cannabinoid receptor antagonists. (LLM, conf=0.85)
Experimental — accuracy not yet measuredLower astrocyte density in the MeA is correlated with male-typical levels of play.
“Lower astrocyte density in the MeA is correlated for male-typical levels of play (VanRyzin et al., 2019).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as VanRyzin et al., 2019
If females are treated with CB1 and CB2 receptor agonists to mimic higher endocannabinoid levels, their newborn cell number and eventual play behavior is masculinized, even in the absence of testosterone.
“If females are treated with CB1 and CB2 receptor agonists to “mimic” the higher endocannabinoid levels, their newborn cell number and eventual play behavior is masculinized, even in the absence of testosterone (Argue et al., 2017; VanRyzin et al., 2019).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as VanRyzin et al., 2019
Studies investigating neural underpinnings of this behavioral sex difference have identified various nodes within the larger circuitry of social behavior, including the medial amygdala and lateral septum, which exert sex-specific influences on play following sexual differentiation early in life as part of typical brain development.
“Studies investigating the neural underpinnings of this behavioral sex difference have identified various nodes within the larger circuitry of social behavior, including the medial amygdala (VanRyzin et al., 2019) and lateral septum (Bredewold et al., 2014), which exert sex-specific influences on play following sexual differentiation early in life as part of typical brain development.”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as VanRyzin et al., 2019
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244 · see citing works
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · 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
Microglia Shape Adult Hippocampal Neurogenesis through Apoptosis-Coupled Phagocytosis
Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., Tsirka, S. E., & Maletic-Savatic, M. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.014 · Cited by 1,622 · see citing works
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976 · see citing works
Microglial Phagocytosis of Live Neurons
Brown, G. C., & Neher, J. J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3710 · Cited by 853 · see citing works
Layer V cortical neurons require microglial support for survival during postnatal development
Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., & Yamashita, T. (2013) · Nature Neuroscience · doi:10.1038/nn.3358 · Cited by 781 · see citing works
Microglia Promote the Death of Developing Purkinje Cells
Marı́n-Teva, J. L., Dusart, I., Colin, C., Gervais, A., van Rooijen, N., & Mallat, M. (2004) · Neuron · doi:10.1016/s0896-6273(04)00069-8 · Cited by 757 · see citing works
Reframing sexual differentiation of the brain
McCarthy, M. M., & Arnold, A. P. (2011) · Nature Neuroscience · doi:10.1038/nn.2834 · Cited by 728 · see citing works
Self-citationSex differences in microglial colonization of the developing rat brain
Schwarz, J. M., Sholar, P. W., & Bilbo, S. D. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07630.x · Cited by 672 · see citing works
Nonpsychotropic Cannabinoid Receptors Regulate Microglial Cell Migration
Walter, L. M., Franklin, A. A., Witting, A., Wade, C. B., Xie, Y., Kunos, G., Mackie, K., & Stella, N. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01398.2003 · Cited by 666 · see citing works
Microglia Modulate Wiring of the Embryonic Forebrain
Squarzoni, P., Oller, G., Hoeffel, G., Pont‐Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., & Garel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.042 · Cited by 655 · see citing works
Microglia contact induces synapse formation in developing somatosensory cortex
Miyamoto, A., Wake, H., Ishikawa, A. W., Eto, K., Shibata, K., Murakoshi, H., Koizumi, S., Moorhouse, A. J., Yoshimura, Y., & Nabekura, J. (2016) · Nature Communications · doi:10.1038/ncomms12540 · Cited by 649 · see citing works
Microglia Are Essential to Masculinization of Brain and Behavior
Lenz, K. M., Nugent, B. M., Haliyur, R., & McCarthy, M. M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1268-12.2013 · Cited by 526 · see citing works
Self-citationMicroglia Enhance Neurogenesis and Oligodendrogenesis in the Early Postnatal Subventricular Zone
Shigemoto‐Mogami, Y., Hoshikawa, K., Goldman, J. E., Sekino, Y., & Sato, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1619-13.2014 · Cited by 499 · see citing works
CD47 Protects Synapses from Excess Microglia-Mediated Pruning during Development
Lehrman, E. K., Wilton, D. K., Litvina, E. Y., Welsh, C. A., Chang, S. T., Frouin, A., Walker, A. J., Heller, M. D., Umemori, H., Chen, C., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.017 · Cited by 464 · see citing works
Choi, G. B., Dong, H.-W., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Swanson, L. W., & Anderson, D. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.011 · Cited by 462 · see citing works
Local cues establish and maintain region-specific phenotypes of basal ganglia microglia
De Biase, L. M., Schuebel, K. E., Fusfeld, Z. H., Jair, K., Hawes, I. A., Cimbro, R., Zhang, H.-Y., Liu, Q.-R., Shen, H., Xi, Z.-X., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.020 · Cited by 432 · see citing works
Veerhuis, R., Nielsen, H. M., & Tenner, A. J. (2011) · Molecular Immunology · doi:10.1016/j.molimm.2011.04.003 · Cited by 420 · see citing works
Hong, W., Kim, D.-W., & Anderson, D. J. (2014) · Cell · doi:10.1016/j.cell.2014.07.049 · Cited by 405 · see citing works
Hanamsagar, R., Alter, M. D., Block, C. S., Sullivan, H., Bolton, J. L., & Bilbo, S. D. (2017) · Glia · doi:10.1002/glia.23176 · Cited by 384 · see citing works
Wakselman, S., Béchade, C., Roumier, A., Bernard, D., Triller, A., & Bessis, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1006-08.2008 · Cited by 351 · see citing works
Phagocytosis promotes programmed cell death in C. elegans
Reddien, P. W., Cameron, S., & Horvitz, H. R. (2001) · Nature · doi:10.1038/35084096 · Cited by 348 · see citing works
Synapse-specific astrocyte gating of amygdala-related behavior
Martin-Fernandez, M., Jamison, S., Robin, L. M., Zhao, Z., Martin, E. D., Aguilar, J., Benneyworth, M. A., Marsicano, G., & Araque, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4649 · Cited by 345 · cited 1× · see citing works
“, 1999; Amateau and McCarthy, 2002), or MePD astrocytes may perform ‘‘real-time’’ synaptic gating of social information during a play bout (Martin-Fernandez et al., 2017).”
Carrier, E. J., Kearn, C. S., Barkmeier, A. J., Breese, N. M., Yang, W., Nithipatikom, K., Pfister, S. L., Campbell, W. B., & Hillard, C. J. (2004) · Molecular Pharmacology · doi:10.1124/mol.65.4.999 · Cited by 336 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning
Mulder, J., Aguado, T., Keimpema, E., Barabás, K., Rosado, C. J. B., Nguyen, L., Monory, K., Marsicano, G., Marzo, V. D., Hurd, Y. L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803545105 · Cited by 328 · see citing works
The endocannabinoid system drives neural progenitor proliferation
Aguado, T., Monory, K., Palazuelos, J., Stella, N., Cravatt, B. F., Lutz, B., Marsicano, G., Kokaia, Z., Guzmán, M., & Galve‐Roperh, I. (2005) · The FASEB Journal · doi:10.1096/fj.05-3995fje · Cited by 327 · see citing works
Eaten alive! Cell death by primary phagocytosis: ‘phagoptosis’
Brown, G. C., & Neher, J. J. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.05.002 · Cited by 320 · see citing works
Programming of neural cells by (endo)cannabinoids: from physiological rules to emerging therapies
Maccarrone, M., Guzmán, M., Mackie, K., Doherty, P., & Harkany, T. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3846 · Cited by 298 · see citing works
Hanamsagar, R., Alter, M. D., Block, C. L., Sullivan, H. K., Bolton, J. L., & Bilbo, S. D. (2017) · Glia · doi:10.1002/glia.23277 · Cited by 297 · see citing works
Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans
Hoeppner, D. J., Hengartner, M. O., & Schnabel, R. (2001) · Nature · doi:10.1038/35084103 · Cited by 295 · see citing works
Berghuis, P., Dobszay, M. B., Wang, X., Spano, S., Ledda, F., Sousa, K. M., Schulte, G., Ernfors, P., Mackie, K., Paratcha, G., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509494102 · Cited by 291 · see citing works
Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice
Li, Y., Mathis, A., Grewe, B. F., Osterhout, J. A., Ahanonu, B., Schnitzer, M. J., Murthy, V. N., & Dulac, C. (2017) · Cell · doi:10.1016/j.cell.2017.10.015 · Cited by 291 · see citing works
Microglia Actively Regulate the Number of Functional Synapses
Ji, K., Akgul, G., Wollmuth, L. P., & Tsirka, S. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056293 · Cited by 280 · see citing works
Endocannabinoid signaling in microglial cells
Stella, N. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.037 · Cited by 271 · see citing works
The Endocannabinoid System Promotes Astroglial Differentiation by Acting on Neural Progenitor Cells
Aguado, T., Palazuelos, J., Monory, K., Stella, N., Cravatt, B. F., Lutz, B., Marsicano, G., Kokaia, Z., Guzmán, M., & Galve‐Roperh, I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3101-05.2006 · Cited by 269 · see citing works
Tortoriello, G., Morris, C. V., Alpár, A., Fuzik, J., Shirran, S. L., Calvigioni, D., Keimpema, E., Botting, C. H., Reinecke, K., Herdegen, T., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201386035 · Cited by 255 · see citing works
Cannabis use during pregnancy: Pharmacokinetics and effects on child development
Grant, K. S., Petroff, R., Isoherranen, N., Stella, N., & Burbacher, T. M. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.08.014 · Cited by 253 · see citing works
Sex-specific processing of social cues in the medial amygdala
Bergan, J. F., Ben-Shaul, Y., & Dulac, C. (2014) · eLife · doi:10.7554/elife.02743 · Cited by 237 · see citing works
Zuloaga, D. G., Puts, D. A., Jordan, C. L., & Breedlove, S. M. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.013 · Cited by 236 · see citing works
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · see citing works
Mong, J. A., Glaser, E. M., & McCarthy, M. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01464.1999 · Cited by 226 · see citing works
Self-citationActive endocannabinoids are secreted on extracellular membrane vesicles
Gabrielli, M., Battista, N., Riganti, L., Prada, I., Antonucci, F., Cantone, L., Matteoli, M., Maccarrone, M., & Verderio, C. (2015) · The EMBO Reports · doi:10.15252/embr.201439668 · Cited by 221 · see citing works
Atlas of the Developing Rat Nervous System
(1994) · Elsevier eBooks · doi:10.1016/c2009-0-02416-7 · Cited by 221 · see citing works
A Novel Mechanism of Dendritic Spine Plasticity Involving Estradiol Induction of Prostaglandin-E2
Amateau, S. K., & McCarthy, M. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-19-08586.2002 · Cited by 206 · see citing works
Self-citationP2X 7 receptors control 2-arachidonoylglycerol production by microglial cells
Witting, A., Walter, L. M., Wacker, J. L., Möller, T., & Stella, N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306707101 · Cited by 187 · see citing works
(2016) · Elsevier eBooks · doi:10.1016/c2014-1-00784-3 · Cited by 175 · see citing works
Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (2008) · Neuroendocrinology · doi:10.1159/000123524 · Cited by 144 · see citing works
Wu, C., Zhu, J., Wager‐Miller, J., Wang, S., O’Leary, D. D. M., Monory, K., Lutz, B., Mackie, K., & Lu, H. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07337.x · Cited by 138 · see citing works
Pellis, S. M., & McKenna, M. M. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80295-5 · Cited by 134 · see citing works
Krebs-Kraft, D. L., Hill, M. N., Hillard, C. J., & McCarthy, M. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005003107 · Cited by 130 · see citing works
Self-citationSex-dependent effects of amygdaloid lesions on the social play of prepubertal rats.
Meaney, M. J., Dodge, A. M., & Beatty, W. W. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90175-x · Cited by 126 · see citing works
Metabolic Interplay between Astrocytes and Neurons Regulates Endocannabinoid Action
Viader, A., Blankman, J. L., Zhong, P., Liu, X., Schlosburg, J. E., Joslyn, C. M., Liu, Q.-S., Tomarchio, A. J., Lichtman, A. H., Selley, D. E., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.06.075 · Cited by 122 · see citing works
Meaney, M. J., & McEwen, B. S. (1986) · Brain Research · doi:10.1016/0006-8993(86)91492-7 · Cited by 122 · see citing works
Viader, A., Ogasawara, D., Joslyn, C. M., Sánchez-Alavez, M., Mori, S., Nguyen, W., Conti, B., & Cravatt, B. F. (2016) · eLife · doi:10.7554/elife.12345 · Cited by 109 · see citing works
Vitalis, T., Lainé, J., Simon, A., Roland, A. B., Leterrier, C., & Lenkei, Z. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06484.x · Cited by 106 · see citing works
Fine‐tuning of social play in juvenile lowland gorillas (gorilla gorilla gorilla)
Palagi, E., Antonacci, D., & Cordoni, G. (2007) · Developmental Psychobiology · doi:10.1002/dev.20219 · Cited by 86 · see citing works
Dyadic Play in Hamadryas Baboons
LeResche, L. (1976) · Behaviour · doi:10.1163/156853976x00514 · Cited by 73 · see citing works
Characterization of juvenile play in rats: importance of sex of self and sex of partner
Argue, K. J., & McCarthy, M. M. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0034-x · Cited by 71 · see citing works
Self-citationMorena, M., Castro, V. D., Gray, J. M., Palmery, M., Trezza, V., Roozendaal, B., Hill, M. N., & Campolongo, P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1983-15.2015 · Cited by 70 · see citing works
Self-citationQi, M., Morena, M., Vecchiarelli, H. A., Hill, M. N., & Schriemer, D. C. (2015) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.7277 · Cited by 61 · see citing works
Self-citationSexual Differentiation of the Brain: A Fresh Look at Mode, Mechanisms, and Meaning
McCarthy, M. M., Vries, G. J. D., & Forger, N. G. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00091-2 · Cited by 56 · see citing works
Self-citationArgue, K. J., VanRyzin, J. W., Falvo, D. J., Whitaker, A. R., Yu, S. J., & McCarthy, M. M. (2017) · eneuro · doi:10.1523/eneuro.0344-16.2017 · Cited by 47 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Microglia states and nomenclature: A field at its crossroads
Paolicelli, R. C., Sierra, A., Stevens, B., Tremblay, M.-E., Aguzzi, A., Ajami, B., Amit, I., Audinat, E., Bechmann, I., Bennett, M., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.020 · Cited by 1,973 · see citing works
The Semantics of Microglia Activation: Neuroinflammation, Homeostasis, and Stress
Woodburn, S. C., Bollinger, J. L., & Wohleb, E. S. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02309-6 · Cited by 783 · see citing works
Microglia morphophysiological diversity and its implications for the CNS
Vidal-Itriago, A., Radford, R. A. W., Aramideh, J. A., Maurel, C., Scherer, N. M., Don, E. K., Lee, A., Chung, R. S., Graeber, M. B., & Morsch, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.997786 · Cited by 412 · see citing works
Microglia Actively remodel adult hippocampal neurogenesis through the phagocytosis secretome
Diaz-Aparicio, I., Paris, I., Sierra-Torre, V., Plaza-Zabala, A., Rodríguez-Iglesias, N., Márquez-Ropero, M., Beccari, S., Huguet, P., Abiega, O., Alberdi, E., et al. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0993-19.2019 · Cited by 333 · see citing works
Shaping Neuronal Fate: Functional Heterogeneity of Direct Microglia-Neuron Interactions
Cserép, C., Pósfai, B., & Dénes, Á. (2021) · Neuron · doi:10.1016/j.neuron.2020.11.007 · Cited by 256 · see citing works
Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons
Tang, Y., Benusiglio, D., Lefevre, A., Hilfiger, L., Althammer, F., Bludau, A., Hagiwara, D., Baudon, A., Darbon, P., Schimmer, J., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0674-y · Cited by 249 · see citing works
Cien Años de Microglía: Milestones in a Century of Microglial Research
Sierra, A., Paolicelli, R. C., & Kettenmann, H. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.09.004 · Cited by 229 · see citing works
Transcriptional and epigenetic decoding of the microglial aging process
Li, X., Li, Y., Jin, Y., Zhang, Y., Wu, J., Xu, Z., Huang, Y., Cai, L., Gao, S., Liu, T., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00479-x · Cited by 225 · see citing works
Microglia as Dynamic Cellular Mediators of Brain Function
Wright-Jin, E. C., & Gutmann, D. H. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.08.013 · Cited by 186 · see citing works
THC and CBD: Similarities and differences between siblings
Stella, N. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.022 · Cited by 149 · see citing works
Cell of all trades: oligodendrocyte precursor cells in synaptic, vascular, and immune functionPreprint
Akay, L. A., Effenberger, A. H., & Tsai, L. (2021) · Genes & Development · doi:10.1101/gad.344218.120 · Cited by 142 · see citing works
Brain macrophage development, diversity and dysregulation in health and disease
Silvin, A., Qian, J., & Ginhoux, F. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-01053-6 · Cited by 137 · see citing works
The immune system and psychiatric disease: a basic science perspective
Bennett, F. C., & Molofsky, A. V. (2019) · Clinical & Experimental Immunology · doi:10.1111/cei.13334 · Cited by 133 · see citing works
Bordt, E. A., Ceasrine, A. M., & Bilbo, S. D. (2020) · Glia · doi:10.1002/glia.23753 · Cited by 118 · see citing works
Azcoitia, I., Barreto, G. E., & Garcia-Segura, L. M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100787 · Cited by 125 · see citing works
Zhou, T. G., Li, Y., Li, X., Zeng, F., Rao, Y., He, Y., Wang, Y., Liu, M., Li, D., Xu, Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33932-3 · Cited by 122 · see citing works
Microglial Corpse Clearance: Lessons From Macrophages
Márquez-Ropero, M., Benito, E., Plaza‐Zabala, A., & Sierra, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00506 · Cited by 112 · see citing works
CD4 T Cells Induce A Subset of MHCII-Expressing Microglia that Attenuates Alzheimer Pathology
Mittal, K., Eremenko, E., Berner, O., Elyahu, Y., Strominger, I., Apelblat, D., Nemirovsky, A., Spiegel, I., & Monsonego, A. (2019) · iScience · doi:10.1016/j.isci.2019.05.039 · Cited by 114 · see citing works
Augusto‐Oliveira, M., Arrifano, G. D. P., Delage, C. I., Tremblay, M., Lopez, M. E. C., & Verkhratsky, A. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12797 · Cited by 107 · see citing works
Quantifying microglial morphology: an insight into function
Green, T. R. F., & Rowe, R. K. (2024) · Clinical & Experimental Immunology · doi:10.1093/cei/uxae023 · Cited by 106 · see citing works
Puñal, V. M., Paisley, C. E., Brecha, F. S., Lee, M. A., Perelli, R. M., Wang, J., O’Koren, E. G., Ackley, C. R., Saban, D. R., Reese, B. E., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000492 · Cited by 101 · see citing works
Maternal diet disrupts the placenta–brain axis in a sex-specific manner
Ceasrine, A. M., Devlin, B. A., Bolton, J. L., Green, L. A., Jo, Y. C., Huynh, C., Patrick, B., Washington, K., Sanchez, C. L., Joo, F., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00693-8 · Cited by 94 · see citing works
A new view of sexual differentiation of mammalian brain
McCarthy, M. M. (2020) · Journal of Comparative Physiology A · doi:10.1007/s00359-019-01376-8 · Cited by 85 · see citing works
Self-citationMicroglia‐dependent remodeling of neuronal circuits
Guedes, J. R., Ferreira, P. A., Costa, J. M., Cardoso, A. L., & Peça, J. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15689 · Cited by 93 · see citing works
The emerging tale of microglia in psychiatric disorders
Rahimian, R., Wakid, M., O’Leary, L. A., & Mechawar, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.023 · Cited by 91 · see citing works
Phagocytic astrocytes: Emerging from the shadows of microglia
Konishi, H., Koizumi, S., & Kiyama, H. (2022) · Glia · doi:10.1002/glia.24145 · Cited by 88 · see citing works
Sex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 89 · see citing works
Noteworthy perspectives on microglia in neuropsychiatric disorders
Zhu, H., Guan, A., Liu, J., Li, P., Zhang, Z., & Wang, S. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02901-y · Cited by 90 · see citing works
The Cross-Talk Between the Dopaminergic and the Immune System Involved in Schizophrenia
Vidal, P. M., & Pacheco, R. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00394 · Cited by 89 · see citing works
Althammer, F., Ferreira‐Neto, H. C., Rubaharan, M., Roy, R. K., Patel, A. A., Murphy, A. Z., Cox, D. N., & Stern, J. E. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01892-4 · Cited by 85 · see citing works
Microglia and sexual differentiation of the developing brain: A focus on extrinsic factors
VanRyzin, J. W., Marquardt, A. E., Pickett, L. A., & McCarthy, M. M. (2019) · Glia · doi:10.1002/glia.23740 · Cited by 81 · see citing works
Self-citationLoth, M. K., & Donaldson, Z. R. (2020) · Endocrinology · doi:10.1210/endocr/bqaa223 · Cited by 74 · see citing works
A novel Tmem119-tdTomato reporter mouse model for studying microglia in the central nervous system
Ruan, C., Sun, L., Kroshilina, A., Beckers, L., Jager, P. L. D., Bradshaw, E. M., Hasson, S. A., Yang, G., & Elyaman, W. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.10.009 · Cited by 71 · see citing works
Microglial control of neuronal development via somatic purinergic junctions
Cserép, C., Schwarcz, A. D., Pósfai, B., László, Z. I., Kellermayer, A., Környei, Z., Kisfali, M., Nyerges, M., Lele, Z., Katona, I., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111369 · Cited by 67 · see citing works
Alarmins and c-Jun N-Terminal Kinase (JNK) Signaling in Neuroinflammation
Anfinogenova, Y., Quinn, M. T., Schepetkin, I. A., & Atochin, D. N. (2020) · Cells · doi:10.3390/cells9112350 · Cited by 67 · see citing works
Wang, X., & Li, L. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.722028 · Cited by 67 · see citing works
Sex Differences in Neurodevelopmental Disorders: A Key Role for the Immune System
Breach, M. R., & Lenz, K. M. (2022) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2022_308 · Cited by 62 · see citing works
Crespo‐Castrillo, A., & Arévalo, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093219 · Cited by 62 · see citing works
Silva, N. J., Dorman, L. C., Vainchtein, I. D., Horneck, N. C., & Molofsky, A. V. (2021) · Nature Communications · doi:10.1038/s41467-021-26206-x · Cited by 67 · see citing works
Androgens and the developing hippocampus
Kight, K. E., & McCarthy, M. M. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00307-6 · Cited by 55 · see citing works
Self-citationNeuroendocrine-Immune Crosstalk Shapes Sex-Specific Brain Development
Arambula, S. E., & McCarthy, M. M. (2020) · Endocrinology · doi:10.1210/endocr/bqaa055 · Cited by 55 · see citing works
Self-citationThe neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
Comparative Review of Microglia and Monocytes in CNS Phagocytosis
Andoh, M., & Koyama, R. (2021) · Cells · doi:10.3390/cells10102555 · Cited by 52 · see citing works
Microglial ontogeny, diversity and neurodevelopmental functions
Thion, M. S., & Garel, S. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.06.013 · Cited by 53 · see citing works
Yue, Q., Wang, K., Guan, M., Zhao, Z., Li, X., Yu, P., & Mao, L. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202117596 · Cited by 51 · see citing works
Malvaso, A., Gatti, A., Negro, G., Calatozzolo, C., Medici, V., & Poloni, T. E. (2023) · Cells · doi:10.3390/cells12242824 · Cited by 51 · see citing works
Alzheimer’s disease-related transcriptional sex differences in myeloid cells
Coales, I., Tsartsalis, S., Fancy, N., Weinert, M., Clode, D., Owen, D., & Matthews, P. M. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02604-w · Cited by 49 · see citing works
Molecular and neurocircuitry mechanisms of social avoidance
Gellner, A., Voelter, J., Schmidt, U., Beins, E. C., Stein, V., Philipsen, A., & Hurlemann, R. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03649-x · Cited by 51 · see citing works
IL-4 Shapes Microglia-Dependent Pruning of the Cerebellum During Postnatal Development
Guedes, J. R., Ferreira, P. A., Costa, J., Laranjo, M., Pinto, M. J., Reis, T., Cardoso, A. M., Lebre, C., Casquinha, M., Gomes, M. A., et al. (2022) · Neuron · doi:10.1016/j.neuron.2023.09.031 · Cited by 46 · see citing works
Chromosome X-wide common variant association study in autism spectrum disorder
de Aquino, M. M., Chen, D., Engchuan, W., Leal, T. P., Thiruvahindrapuram, B., Trost, B., Howe, J., Pellecchia, G., Nalpathamkalam, T., Alexandrova, R., et al. (2024) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2024.11.008 · Cited by 45 · see citing works
Sexual dimorphic distribution of cannabinoid 1 receptor mRNA in adult C57BL/6J mice
Liu, X., Li, X., Zhao, G., Wang, F., & Wang, L. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24868 · Cited by 44 · see citing works
Embryonic microglia influence developing hypothalamic glial populations
Marsters, C. M., Nesan, D., Far, R., Klenin, N., Pittman, Q. J., & Kurrasch, D. M. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01811-7 · Cited by 45 · see citing works
The molecular determinants of microglial developmental dynamics
Barry-Carroll, L., & Gómez‐Nicola, D. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00813-1 · Cited by 45 · see citing works
Pickett, L. A., VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212646120 · Cited by 43 · see citing works
Self-citationMicroglia and Sensitive Periods in Brain Development
Dziabis, J. E., & Bilbo, S. D. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_242 · Cited by 42 · see citing works
Tirado-Muñoz, J., López-Rodríguez, A. B., Fonseca, F., Farré, M., Torrens, M., & Viveros, M. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100841 · Cited by 42 · see citing works
Microglial Phagocytosis—Rational but Challenging Therapeutic Target in Multiple Sclerosis
Pinto, M. V., & Fernandes, A. M. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21175960 · Cited by 41 · see citing works
Microglia Drive Pockets of Neuroinflammation in Middle Age
Moca, E. N., Lecca, D., Hope, K. T., Etienne, F., Schaler, A. W., Espinoza, K., Chappell, M. S., Gray, D. T., Tweedie, D., Sidhu, S., et al. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.1922-21.2022 · Cited by 42 · see citing works
Microglia regulate neuronal activity via structural remodeling of astrocytes
Gu, N., Makashova, O. E., Laporte, C., Chen, C. Q., Li, B., Chevillard, P., Lean, G., Yang, J., Wong, C., Fan, J., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.07.024 · Cited by 43 · see citing works
Self-citationEndocannabinoid signaling in microglia
Marinelli, S., Marrone, M. C., Domenico, M. D., & Marinelli, S. (2022) · Glia · doi:10.1002/glia.24281 · Cited by 40 · see citing works
Todd, S. W., Lumsden, E. W., Aracava, Y., Mamczarz, J., Albuquerque, E. X., & Pereira, E. F. R. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108271 · Cited by 41 · see citing works
Smith, C. J. W., Kingsbury, M. A., Dziabis, J. E., Hanamsagar, R. M., Malacon, K. E., Tran, J. N., Norris, H. A., Gulino, M., Bordt, E. A., & Bilbo, S. D. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.08.013 · Cited by 43 · see citing works
Early life high fructose impairs microglial phagocytosis and neurodevelopment
Wang, Z., Lipshutz, A. B., de la Torre, C. M., Trzeciak, A. J., Liu, Z.-L., Miranda, I. C., Lazarov, T., Codo, A. C., Romero-Pichardo, J. E., Nair, A., et al. (2025) · Nature · doi:10.1038/s41586-025-09098-5 · Cited by 45 · see citing works
Baglot, S. L., VanRyzin, J. W., Marquardt, A. E., Aukema, R. J., Petrie, G. N., Hume, C., Reinl, E. L., Bieber, J. B., McLaughlin, R. J., McCarthy, M. M., et al. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24992 · Cited by 37 · see citing works
Self-citationNeural Control of Sexually Dimorphic Social Behavior: Connecting Development to Adulthood
McCarthy, M. M. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-121522-110856 · Cited by 36 · see citing works
Self-citationBreach, M. R., Dye, C. N., Joshi, A., Platko, S., Gilfarb, R. A., Krug, A. R., Franceschelli, D. V., Galan, A., Dodson, C. M., & Lenz, K. M. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.03.025 · Cited by 35 · see citing works
Microglial heterogeneity in aging and Alzheimer's disease: Is sex relevant?
Delage, C. I., Šimončičová, E., & Tremblay, M. (2021) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2021.03.006 · Cited by 35 · see citing works
Movers and shakers: Microglial dynamics and modulation of neural networks
Whitelaw, B. S., Stoessel, M. B., & Majewska, A. K. (2022) · Glia · doi:10.1002/glia.24323 · Cited by 33 · see citing works
Developmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
“Fish, 1976), or paired as same-sex play partners and provided a ‘play date’ each day (Argue & McCarthy, 2015a; Krebs-Kraft, Hill, Hillard, & McCarthy, 2010; VanRyzin et al., 2019).”
BackgroundInfluentialSelf-citationSurala, M., Soso-Zdravkovic, L., Munro, D. A. D., Rifat, A., Ouk, K., Vida, I., Priller, J., & Madry, C. (2024) · EMBO Reports · doi:10.1038/s44319-024-00130-9 · Cited by 36 · see citing works
Maes, M. H. J., Anderson, G., Medina, S. R. B., Seo, M., & Ojala, J. O. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666191102165459 · Cited by 33 · see citing works
RNA sequence analysis reveals ITGAL/CD11A as a stromal regulator of murine low-grade glioma growth
Costa, A. D. A., Chatterjee, J., Cobb, O. M., Sanapala, S., Scheaffer, S. M., Guo, X., Dahiya, S. M., & Gutmann, D. H. (2021) · Neuro-Oncology · doi:10.1093/neuonc/noab130 · Cited by 33 · see citing works
de Soysa, Y., Therrien, M., Walker, A. C., & Stevens, B. (2022) · Seminars in Immunology · doi:10.1016/j.smim.2022.101651 · Cited by 33 · see citing works
Defining Microglial States and Nomenclature: A Roadmap to 2030Preprint
Paolicelli, R. C., Sierra, A., Stevens, B., Tremblay, M., Aguzzi, A., Ajami, B., Amit, I., Audinat, É., Bechmann, I., Bennett, M. L., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4065080 · Cited by 33 · see citing works
Smith, B. L., Guzman, T. A., Brendle, A. H., Laaker, C. J., Ford, A., Hiltz, A. R., Zhao, J., Setchell, K. D. R., & Reyes, T. M. (2022) · eNeuro · doi:10.1523/eneuro.0238-22.2022 · Cited by 32 · see citing works
Marquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1076765 · Cited by 31 · see citing works
Self-citationOxytocin and microglia in the development of social behaviour
Gonzalez, A. M., & Hammock, E. A. D. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0059 · Cited by 32 · see citing works
Smith, C. J. W., Lintz, T., Clark, M. J., Malacon, K. E., Abiad, A., Constantino, N. J., Kim, V. J., Jo, Y. C., Alonso‐Caraballo, Y., Bilbo, S. D., et al. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01376-4 · Cited by 30 · see citing works
Microglia‐leucocyte axis in cerebral ischaemia and inflammation in the developing brain
Rayasam, A., Fukuzaki, Y., & Vexler, Z. S. (2021) · Acta Physiologica · doi:10.1111/apha.13674 · Cited by 31 · see citing works
Hao, K., Wang, H., Zhang, Y., Xie, X., Huang, H., Cheng Ann, C. H. E. N., Xu, S., Xu, R., Shu, C., Liu, Z., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02591-y · Cited by 29 · see citing works
Boerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 29 · see citing works
Zheng, H., Zhang, C., Zhang, J., & Duan, L. (2023) · Protein & Cell · doi:10.1093/procel/pwad020 · Cited by 29 · see citing works
Deivasigamani, S., Miteva, M. T., Natale, S., Gutierrez‐Barragan, D., Basilico, B., Angelantonio, S. D., Weinhard, L., Molotkov, D., Deb, S., Pape, C., et al. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad313 · Cited by 26 · see citing works
Liberman, D. A., Walker, K. A., Gore, A. C., & Bell, M. R. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106880 · Cited by 25 · see citing works
Imaging the Neuroimmune Dynamics Across Space and Time
Carrier, M., Robert, M.-È., Ibáñez, F. G., Desjardins, M., & Tremblay, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00903 · Cited by 27 · see citing works
Pinto, M. J., Cottin, L., Dingli, F., Laigle, V., Ribeiro, L. F., Triller, A., Henderson, F., Loew, D., Fabre, V., & Bessis, A. (2022) · The EMBO Journal · doi:10.15252/embj.2022111485 · Cited by 24 · see citing works
Sousa, F. J., Correia, R. G., Cruz, A., Martins, J., Rodrigues, M. S., Gomes, C. A., Ambrósio, A. F., & Baptista, F. I. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100075 · Cited by 25 · see citing works
Morphological evidence indicates a role for microglia in shaping the PCOS‐like brain
Sati, A., Prescott, M., Holland, S., Jasoni, C. L., Desroziers, E., & Campbell, R. E. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.12999 · Cited by 26 · see citing works
Lipid endocannabinoids in energy metabolism, stress and developmental programming
de Almeida, M. M., Dias-Rocha, C. P., Calviño, C., & Trevenzoli, I. H. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111522 · Cited by 27 · see citing works
Sickness and the Social Brain: How the Immune System Regulates Behavior across Species
Devlin, B. A., Smith, C. J. W., & Bilbo, S. D. (2021) · Brain Behavior and Evolution · doi:10.1159/000521476 · Cited by 26 · see citing works
Reelin cells and sex‐dependent synaptopathology in autism following postnatal immune activation
Ardalan, M., Chumak, T., Quist, A., Hermans, E. C., Rafati, A. H., Gravina, G., Shiadeh, S. M. J., Svedin, P., Alabaf, S., Hansen, B., et al. (2022) · British Journal of Pharmacology · doi:10.1111/bph.15859 · Cited by 26 · see citing works
Astrocytes and microglia in the coordination of CNS development and homeostasis
Lopez‐Ortiz, A. O., & Eyo, U. B. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.16006 · Cited by 29 · see citing works
Paton, S. E. J., Solano, J. L., Coulombe-Rozon, F., Lebel, M., & Ménard, C. (2023) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.220218 · Cited by 24 · see citing works
Reactive microglia partially envelop viable neurons in prion diseases
Makarava, N., Safadi, T., Bocharova, O. V., Mychko, O., Pandit, N. P., Molesworth, K., Baiardi, S., Zhang, L., Parchi, P., & Baskakov, I. V. (2024) · Journal of Clinical Investigation · doi:10.1172/jci181169 · Cited by 26 · see citing works
Loewen, S. M., Chavesa, A. M., Murray, C. J., Traetta, M. E., Burns, S. E., Pekarik, K. H., & Tremblay, M. (2023) · Developmental Neuroscience · doi:10.1159/000530185 · Cited by 25 · see citing works
Kamei, R., & Okabe, S. (2023) · Glia · doi:10.1002/glia.24379 · Cited by 26 · see citing works
A Healthy Gut for a Healthy Brain: Preclinical, Clinical and Regulatory Aspects
Petrella, C., Vecchioli, S. F., Cisale, G. Y., Strimpakos, G., Borg, J.-J., Ceccanti, M., Fiore, M., Monteleone, G., & Nisticò, R. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200730111528 · Cited by 24 · see citing works
Bruce, M. R., Jones, K. L., Vernon, A. C., Silverman, J. L., Crawley, J. N., Ellegood, J., Lerch, J. P., & de Water, J. V. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01215-w · Cited by 24 · see citing works
Dawson, M. S., Gordon-Fleet, K., Yan, L., Tardos, V., He, H., Mui, K., Nawani, S., Asgarian, Z., Catani, M., Fernandes, C., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05215-0 · Cited by 24 · see citing works
Peng, X., Mao, Y., Liu, Y., Dai, Q., Tai, Y., Luo, B., Liang, Y., Guan, R., Zhou, W., Chen, L., et al. (2024) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14674 · Cited by 23 · see citing works
- Authors
- VanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M.
- Affiliations
- University of Maryland, Baltimore (US)
- University of Calgary (CA)
- Corresponding author
- McCarthy, Margaret M.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2019-04
- Volume
- 102
- Issue
- 2
- Pages
- 435-449.e6
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC8046232
- OpenAlex
- W2918315099
- Cited by
- 272
- References
- 65
- Citations by year
- 2026: 20 · 2025: 31 · 2024: 48 · 2023: 44 · 2022: 41 · 2021: 36 · 2020: 38 · 2019: 14
- FWCI
- 19.53
- Type
- journal article
- Language
- en
- Update notices
- erratum (2022-04-06)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (R01MH52716, R01DA039062)
- Natural Sciences and Engineering Council of Canada
- Canadian Institutes of Health Research
- CIHR
- Alberta Innovates
- BranchOut Neurological Foundation
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- microglial phagocytosis, endocannabinoids, sex differences, social play, rough-and-tumble play, amygdala development, masculinization, androgens, astrocyte survival, neuronal excitation, social behavior, sexual differentiation of the brain
- MeSH terms
- Amygdala, Androgen Antagonists, Androgens, Animals, Animals, Newborn, Arachidonic Acids, Astrocytes, Behavior, Animal, Cell Survival, Complement System Proteins, Female, Flutamide, Glycerides, Male, Phagocytosis, Play and Playthings, Sex Characteristics, Social Behavior, Testosterone, Microglia, Rats, Polyunsaturated Alkamides, Endocannabinoids
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
