Sex Differences of Microglia and Synapses in the Hippocampal Dentate Gyrus of Adult Mouse Offspring Exposed to Maternal Immune Activation
Open accessAbstract
Schizophrenia is a psychiatric disorder affecting ∼1% of humans worldwide. It is earlier and more frequently diagnosed in men than woman, and men display more pronounced negative symptoms together with greater gray matter reductions. Our previous findings utilizing a maternal immune activation (mIA) mouse model of schizophrenia revealed exacerbated anxiety-like behavior and sensorimotor gating deficits in adult male offspring that were associated with increased microglial reactivity and inflammation in the hippocampal dentate gyrus (DG). However, both male and female adult offspring displayed stereotypy and impairment of sociability. We hypothesized that mIA may lead to sex-specific alterations in microglial pruning activity, resulting in abnormal synaptic connectivity in the DG. Using the same mIA model, we show in the current study sex-specific differences in microglia and synapses within the DG of adult offspring. Specifically, microglial levels of cluster of differentiation (CD)68 and CD11b were increased in mIA-exposed females. Sex-specific differences in excitatory and inhibitory synapse densities were also observed following mIA. Additionally, inhibitory synaptic tone was increased in DG granule cells of both males and females, while changes in excitatory synaptic transmission occurred only in females with mIA. These findings suggest that phagocytic and complement pathways may together contribute to a sexual dimorphism in synaptic pruning and neuronal dysfunction in mIA, and may propose sex-specific therapeutic targets to prevent schizophrenia-like behaviors.
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?
Microglia are highly affected by sex hormones.
“Microglia, which are the resident innate immune cells of the CNS, are highly affected by sex hormones [14, 16–20].”
From Sex chromosomes and sex hormones differently shape microglial properties during normal physiological conditions in the adult mouse hippocampus (2025) · cites this paper as [14]
The Introduction (page unavailable) describes substantial sex differences in microglial development, morphology, and activity, and the Discussion reports sex-specific microglial changes in the mouse model. The paper does not establish that sex hormones cause those differences or show that microglia are highly affected by them. (LLM, conf=0.79)
Experimental — accuracy not yet measuredSex differences extend to individual cells within the brain parenchyma, including microglia.
“Sex differences also extend to individual cells within the brain parenchyma, including microglia [3, 14, 15].”
From Sex chromosomes and sex hormones differently shape microglial properties during normal physiological conditions in the adult mouse hippocampus (2025) · cites this paper as [14]
Increased contacts with pre- and post-synaptic elements in the WT group might indicate enhanced synapse plasticity and maintenance.
“Increased contacts with pre- and post-synaptic elements in the WT group might indicate enhanced synapse plasticity and maintenance, as microglia are known to constantly modulate synapses during normal physiological conditions [14, 24, 87].”
From Sex chromosomes and sex hormones differently shape microglial properties during normal physiological conditions in the adult mouse hippocampus (2025) · cites this paper as [14]
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
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · 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
Kettenmann, H., Hanisch, U.-K., Noda, M., & Verkhratsky, A. (2011) · Physiological Reviews · doi:10.1152/physrev.00011.2010 · Cited by 3,547 · 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
Statistical analysis of real-time PCR data
Yuan, J. S., Reed, A., Chen, F., & Stewart, C. N. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-85 · Cited by 2,192 · see citing works
Neuroinflammation and M2 Microglia: The Good, the Bad, and the Inflamed
Cherry, J. D., Olschowka, J. A., & O’Banion, M. K. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-98 · Cited by 1,748 · see citing works
Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence?
Feinberg, I. (1982) · Journal of Psychiatric Research · doi:10.1016/0022-3956(82)90038-3 · Cited by 1,395 · see citing works
Sellgren, C. M., Gracias, J., Watmuff, B., Biag, J. D., Thanos, J. M., Whittredge, P. B., Fu, T., Worringer, K. A., Brown, H. E., Wang, J. P., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0334-7 · Cited by 784 · see citing works
Lian, H., Yang, L., Cole, A., Sun, L., Chiang, A. C.-A., Fowler, S. W., Shim, D. J., Rodriguez-Rivera, J., Taglialatela, G., Jankowsky, J. L., et al. (2015) · Neuron · doi:10.1016/j.neuron.2014.11.018 · Cited by 697 · see citing works
Sex 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
Lian, H., Litvinchuk, A., Chiang, A. C.-A., Aithmitti, N., Jankowsky, J. L., & Zheng, H. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2117-15.2016 · Cited by 597 · see citing works
GABAergic interneuron origin of schizophrenia pathophysiology
Nakazawa, K., Zsiros, V., Jiang, Z., Nakao, K., Kolata, S., Zhang, S., & Belforte, J. E. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.022 · Cited by 498 · see citing works
Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease
Turmaine, M., Raza, A., Mahal, A., Mangiarini, L., Bates, G. P., & Davies, S. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.110078997 · Cited by 430 · see citing works
Dark microglia: A new phenotype predominantly associated with pathological states
Bisht, K., Sharma, K. P., Lecours, C., Gabriela Sánchez, M., El Hajj, H., Milior, G., Olmos‐Alonso, A., Gómez‐Nicola, D., Luheshi, G., Vallières, L., et al. (2016) · Glia · doi:10.1002/glia.22966 · Cited by 421 · see citing works
Self-citationPresynaptic glutamate receptors: physiological functions and mechanisms of action
Pinheiro, P. S., & Mulle, C. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2379 · Cited by 368 · see citing works
The perforant path: projections from the entorhinal cortex to the dentate gyrus
Witter, M. P. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63003-9 · Cited by 358 · see citing works
Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices
Tremblay, M., Zettel, M. L., Ison, J. R., Allen, P. D., & Majewska, A. K. (2012) · Glia · doi:10.1002/glia.22287 · Cited by 309 · see citing works
Self-citationThe enigmatic mossy cell of the dentate gyrus
Scharfman, H. E. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.87 · Cited by 290 · see citing works
What is the mammalian dentate gyrus good for?
Treves, A., Tashiro, A., Witter, M. P., & Moser, E. I. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.073 · Cited by 282 · see citing works
Sex/gender differences in the brain and cognition in schizophrenia
Mendrek, A., & Mancini-Marı̈e, A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.013 · Cited by 265 · see citing works
Sex differences in microglial phagocytosis in the neonatal hippocampus
Nelson, L. H., Warden, S., & Lenz, K. M. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.010 · Cited by 189 · see citing works
Glutamatergic Synaptic Dysregulation in Schizophrenia: Therapeutic Implications
Coyle, J. T., Basu, A., Benneyworth, M., Balu, D., & Konopaske, G. (2012) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25758-2_10 · Cited by 180 · see citing works
Fu, H., Liu, B., Frost, J. L., Hong, S., Jin, M., Ostaszewski, B., Shankar, G. M., Costantino, I. M., Carroll, M. C., Mayadas, T. N., et al. (2012) · Glia · doi:10.1002/glia.22331 · Cited by 180 · see citing works
Microglial activation in a neuroinflammational animal model of schizophrenia – a pilot study
Juckel, G., Manitz, M. P., Brüne, M., Friebe, A., Heneka, M. T., & Wolf, R. J. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.06.018 · Cited by 165 · see citing works
Hui, C. W., St-Pierre, A., Hajj, H. E., Remy, Y., Hébert, S. S., Luheshi, G. N., Srivastava, L. K., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00013 · Cited by 158 · see citing works
Self-citationBrain Microglia and Microglial Markers
Korzhevsky, D. E., & Kirik, O. V. (2016) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-016-0231-z · Cited by 148 · see citing works
Glutamate Dysfunction in Hippocampus: Relevance of Dentate Gyrus and CA3 Signaling
Tamminga, C. A., Southcott, S. A., Sacco, C., Wagner, A. D., & Ghose, S. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs062 · Cited by 144 · see citing works
Glutamate Receptors and Transporters in the Hippocampus in Schizophrenia
Harrison, P. J., Law, A. J., & Eastwood, S. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.006 · Cited by 141 · see citing works
Giovanoli, S., Weber‐Stadlbauer, U., Schedlowski, M., Meyer, U., & Engler, H. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.015 · Cited by 139 · see citing works
Mongan, D., Ramesar, M., Föcking, M., Cannon, M., & Cotter, D. (2020) · Early Intervention in Psychiatry · doi:10.1111/eip.12859 · Cited by 123 · see citing works
Yanguas‐Casás, N., Crespo‐Castrillo, A., CEBALLOS, M. L. D., Chowen, J. A., Azcoitia, Í., Arévalo, M., & García‐Segura, L. M. (2017) · Glia · doi:10.1002/glia.23263 · Cited by 116 · see citing works
Oxidative Stress and Reactive Nitrogen Species Generation during Renal Ischemia
Walker, L. M. (2001) · Toxicological Sciences · doi:10.1093/toxsci/63.1.143 · Cited by 115 · see citing works
Sexual dimorphism of microglia and synapses during mouse postnatal development
Weinhard, L., Neniskyte, U., Vadisiute, A., di Bartolomei, G., Aygün, N., Riviere, L., Zonfrillo, F., Dymecki, S., & Gross, C. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22568 · Cited by 107 · see citing works
Complement System in Brain Architecture and Neurodevelopmental Disorders
Magdalon, J., Mansur, F., Silva, A. L. T. E., de Goes, V. A., Reiner, O., & Sertie, A. L. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00023 · Cited by 104 · see citing works
den Eynde, K. V., Missault, S., Fransén, E., Raeymaekers, L., Willems, R., Drinkenburg, W. H. I. M., Timmermans, J., Kumar‐Singh, S., & Dedeurwaerdere, S. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.005 · Cited by 99 · see citing works
Complement-Mediated Events in Alzheimer’s Disease: Mechanisms and Potential Therapeutic Targets
Tenner, A. J. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901068 · Cited by 99 · see citing works
Gallagher, J. J., Minogue, A., & Lynch, M. (2012) · Neurodegenerative Diseases · doi:10.1159/000337458 · Cited by 96 · see citing works
Molecular evidence of synaptic pathology in the CA1 region in schizophrenia
Matosin, N., Fernandez, F., Lum, J. S., Engel, M., Andrews, J. L., Gassen, N. C., Wagner, K. V., Schmidt, M. V., & Newell, K. A. (2016) · Schizophrenia · doi:10.1038/npjschz.2016.22 · Cited by 92 · see citing works
Roberts, R. C., Barksdale, K. A., Roche, J. K., & Lahti, A. C. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.07.016 · Cited by 89 · see citing works
Li, W., Ghose, S., Gleason, K., Begović, A., Perez, J. M., Bartko, J. J., Russo, S. J., Wagner, A. D., Selemon, L. D., & Tamminga, C. A. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.14010123 · Cited by 84 · see citing works
Emerging Roles of Complement in Psychiatric Disorders
Druart, M., & Magueresse, C. L. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00573 · Cited by 84 · see citing works
Complement activation contributes to perioperative neurocognitive disorders in mice
Xiong, C., Liu, J., Lin, D., Zhang, J., Terrando, N., & Wu, A. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1292-4 · Cited by 81 · see citing works
Luchena, C., Zuazo-Ibarra, J., Alberdi, E. M., Matute, C., & Capetillo‐Zarate, E. (2018) · Mediators of Inflammation · doi:10.1155/2018/2530414 · Cited by 81 · see citing works
Pratt, L., Ni, L., Ponzio, N. M., & Jonakait, G. M. (2013) · Pediatric Research · doi:10.1038/pr.2013.126 · Cited by 77 · see citing works
González Ibanez, F., Picard, K., Bordeleau, M., Sharma, K., Bisht, K., & Tremblay, M.-È. (2019) · Journal of Visualized Experiments · doi:10.3791/60510 · Cited by 77 · see citing works
Self-citationRatnayake, U., Quinn, T. A., Castillo-Melendez, M., Dickinson, H., & Walker, D. W. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.08.011 · Cited by 75 · see citing works
Bordeleau, M., Carrier, M., Luheshi, G. N., & Tremblay, M.-È. (2019) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2019.06.001 · Cited by 75 · see citing works
Self-citationSchröder‐Heurich, B., Idrissi, N. B. E., Donev, R., Petri, S., Claus, P., Neal, J., Morgan, B. P., & Ramaglia, V. (2011) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2011.03.011 · Cited by 63 · see citing works
Audoy-Rémus, J., Bozoyan, L., Dumas, A., Filali, M., Lecours, C., Lacroix, S., Rivest, S., Tremblay, M., & Vallières, L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.01.010 · Cited by 61 · see citing works
Self-citationTian, L., Hui, C. W., Bisht, K., Tan, Y., Sharma, K. P., Chen, S., Zhang, X., & Tremblay, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.007 · Cited by 47 · see citing works
Self-citationIbáñez, F. G., Picard, K., Bordeleau, M., Sharma, K. P., Bisht, K., & Tremblay, M. (2019) · Journal of Visualized Experiments · doi:10.3791/60510-v · Cited by 41 · see citing works
Self-citationBozoyan, L., Audoy-Rémus, J., Dumas, A., Filali, M., Lacroix, S., Rivest, S., Tremblay, M., & Vallières, L. (2014) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.08.351 · Cited by 36 · see citing works
Self-citationHenry, M. S., Bisht, K., Vernoux, N., Gendron, L., Torres‐Berrío, A., Drolet, G., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00100 · Cited by 34 · see citing works
Self-citationZhao, Y., Luo, C., Chen, J., Sun, Y., Pu, D., Lv, A., Zhu, S., Wu, J., Wang, M., Zhou, J., et al. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13884 · Cited by 31 · see citing works
David, L. S., & Topolnik, L. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.03.007 · Cited by 28 · see citing works
Self-citationDentate Gyrus Immaturity in Schizophrenia
Tavitian, A., Song, W., & Schipper, H. M. (2019) · The Neuroscientist · doi:10.1177/1073858418824072 · Cited by 25 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Exploring Sex-Related Differences in Microglia May Be a Game-Changer in Precision Medicine
Lynch, M. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.868448 · Cited by 146 · see citing works
de Bartolomeis, A., Barone, A., Vellucci, L., Mazza, B., Austin, M. C., Iasevoli, F., & Ciccarelli, M. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02976-3 · Cited by 113 · see citing works
Hall, M. B., Willis, D. E., Rodriguez, E. L., & Schwarz, J. M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1135559 · Cited by 112 · see citing works
Tastan, B., Arioz, B. I., Tüfekçi, K. U., Tarakcioglu, E., Gonul, C. P., Genç, K., & Genç, Ş. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.737065 · Cited by 100 · see citing works
Woods, R. M., Lorusso, J. M., Fletcher, J., ElTaher, H., McEwan, F., Harris, I., Kowash, H. M., D'Souza, S. W., Harte, M., Hager, R., et al. (2023) · Neuronal Signaling · doi:10.1042/ns20220064 · Cited by 81 · see citing works
Sex difference in human diseases: mechanistic insights and clinical implications
Shi, Y., Ma, J., Li, S., Liu, C., Liu, Y., Chen, J., Liu, N., Liu, S., & Huang, H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01929-7 · Cited by 82 · see citing works
Rahimian, R., Belliveau, C., Chen, R., & Mechawar, N. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.871997 · Cited by 73 · see citing works
Sex-Specific Immune Responses in Stroke
Banerjee, A., & McCullough, L. D. (2022) · Stroke · doi:10.1161/strokeaha.122.036945 · Cited by 57 · see citing works
Microglia-neuron interactions in schizophrenia
Hartmann, S.-M., Heider, J., Wüst, R., Fallgatter, A. J., & Volkmer, H. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1345349 · Cited by 56 · see citing works
Krukowski, K., Grue, K. A., Becker, M., Elizarraras, E., Frias, E. S., Halvorsen, A. T., Koenig-Zanoff, M., Frattini, V., Nimmagadda, H., Feng, X., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg6702 · Cited by 51 · see citing works
Bobotis, B. C., Braniff, O., Gargus, M., Akinluyi, E. T., Awogbindin, I. O., & Tremblay, M.-È. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110752 · Cited by 40 · see citing works
Self-citationWestacott, L. J., & Wilkinson, L. S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.840266 · Cited by 44 · see citing works
Microglia sequelae: brain signature of innate immunity in schizophrenia
Rodrigues‐Neves, A. C., Ambrósio, A. F., & Gomes, C. A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02197-1 · Cited by 34 · see citing works
The X factor in neurodegeneration
Voskuhl, R. R., & Itoh, Y. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211488 · Cited by 34 · see citing works
Otero, A. M., Connolly, M. G., Gonzalez-Ricon, R., Wang, S. S., Allen, J. M., & Antonson, A. M. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02648-9 · Cited by 31 · see citing works
Patient-Derived In Vitro Models of Microglial Function and Synaptic Engulfment in Schizophrenia
Sheridan, S. D., Horng, J. E., & Perlis, R. H. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.01.004 · Cited by 30 · see citing works
Guma, E., Cupo, L., Ma, W., Gallino, D., Moquin, L., Gratton, A. P., Devenyi, G. A., & Chakravarty, M. M. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110642 · Cited by 28 · see citing works
Niraula, A., Fasnacht, R. D., Ness, K. M., Frey, J. M., Cuschieri, S. A., Dorfman, M. D., & Thaler, J. P. (2022) · Diabetes · doi:10.2337/db21-1072 · Cited by 27 · 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
Self-citationShi, L., Xia, Z., Guo, J., Wang, L., Peng, Z., Qiu, D., Zhou, Y., Zhou, D., Kuang, L., & Qiu, T. (2023) · Journal of Affective Disorders · doi:10.1016/j.jad.2023.02.016 · Cited by 25 · see citing works
Li, J., Wang, Y., Yuan, X., Kang, Y., & Song, X. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1126632 · Cited by 19 · see citing works
Bobotis, B. C., Halvorson, T., Carrier, M., & Tremblay, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1317125 · Cited by 21 · see citing works
Self-citationTowriss, M., MacVicar, B. A., & Ciernia, A. V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24108967 · Cited by 18 · see citing works
Le, L., Feidler, A. M., Rodrı́guez, L., Cealie, M. Y., Plunk, E. C., Li, H., Kara-Pabani, K., Lamantia, C. E., O’Banion, M. K., & Majewska, A. K. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.04.022 · Cited by 18 · see citing works
Bobotis, B. C., Khakpour, M., Braniff, O., de Andrade, E. G., Gargus, M., Allen, M., Carrier, M., Baillargeon, J., Rangachari, M., & Tremblay, M.-È. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03341-6 · Cited by 17 · see citing works
“Microglia, which are the resident innate immune cells of the CNS, are highly affected by sex hormones [14, 16– 20].”
InfluentialSelf-citationYan, S., Wang, L., Samsom, J., Ujic, D., & Liu, F. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105480 · Cited by 17 · see citing works
Goikolea-Vives, A., & Stolp, H. B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158220 · Cited by 15 · see citing works
Carrier, M., Hui, C. W., Watters, V., Šimončičová, E., Picard, K., Ibáñez, F. G., Vernoux, N., Droit, A., Desjardins, M., & Tremblay, M. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.11.025 · Cited by 15 · see citing works
Self-citationPramanik, S., Harini Devi, M., Chakrabarty, S., Paylar, B., Pradhan, A., Thaker, M., Ayyadhury, S., Manavalan, A., Olsson, P., Pramanik, G., et al. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105834 · Cited by 18 · see citing works
Zengeler, K. E., Shapiro, D. A., Bruch, K. R., Lammert, C. R., Ennerfelt, H. E., & Lukens, J. R. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.10.024 · Cited by 14 · see citing works
Le, L., Eliseeva, S. I., Plunk, E. C., Kara-Pabani, K., Li, H., Yarovinsky, F., & Majewska, A. K. (2025) · Cell Reports · doi:10.1016/j.celrep.2024.115176 · Cited by 12 · see citing works
Mawson, E. R., & MORRIS, B. J. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110773 · Cited by 13 · see citing works
Maternal immune response during pregnancy and neurodevelopmental outcomes: A longitudinal approach
Euclydes, V. L. V., Braga, C., Gouveia, G. R., Martinez, R. C. R., Camilo, C., Simões, S. N., Martins, D., Fracolli, L. A., Argeu, A., Ferraro, A. A., et al. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100832 · Cited by 11 · see citing works
Ultrastructural features of psychological stress resilience in the brain: a microglial perspective
Ibáñez, F. G., VanderZwaag, J., Deslauriers, J., & Tremblay, M. (2024) · Open Biology · doi:10.1098/rsob.240079 · Cited by 9 · see citing works
Self-citationSanfilippo, C., Castrogiovanni, P., Imbesi, R., Fagone, P., Scuderi, G., Vinciguerra, M., & Rosa, M. D. (2025) · GeroScience · doi:10.1007/s11357-025-01740-4 · Cited by 8 · see citing works
Gonzalez-Ricon, R., Otero, A. M., Chalen, I., Savas, J. N., Adetunji, S. A., & Antonson, A. M. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106069 · Cited by 8 · see citing works
Griego, E., Cerna, C., Sollozo-Dupont, I., Fuenzalida, M., & Galván, E. J. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.09.012 · Cited by 7 · see citing works
Rodriguez‐Zas, S. L., Southey, N. L., Rund, L. A., Antonson, A. M., Nowak, R. A., & Johnson, R. W. (2023) · PLoS ONE · doi:10.1371/journal.pone.0292952 · Cited by 7 · see citing works
Prenatal drivers of microglia vulnerability in the adult
Tagliatti, E., Bizzotto, M., Morini, R., Filipello, F., Rasile, M., & Matteoli, M. (2024) · Immunological Reviews · doi:10.1111/imr.13418 · Cited by 6 · see citing works
Felice, E. D., Bobotis, B. C., Rigillo, G., Khakpour, M., de Andrade, E. G., Benatti, C., Vilella, A., Tascedda, F., Limatola, C., Tremblay, M., et al. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.11.034 · Cited by 5 · see citing works
Self-citationDisruption of Alternative Splicing in the Amygdala of Pigs Exposed to Maternal Immune Activation
Southey, B. R., Keever-Keigher, M. R., Rymut, H. E., Rund, L. A., Johnson, R. W., & Rodriguez‐Zas, S. L. (2021) · Immuno · doi:10.3390/immuno1040035 · Cited by 5 · see citing works
Itoh, Y., Itoh, N., Wendin, S., Higgins, N., & Voskuhl, R. R. (2025) · Science Translational Medicine · doi:10.1126/scitranslmed.adq3401 · Cited by 5 · see citing works
Collins, B., Lemanski, E. A., & Wright-Jin, E. C. (2024) · Biomedicines · doi:10.3390/biomedicines12112559 · Cited by 4 · see citing works
Microglia as critical mediators linking perinatal immune stress to mental health trajectories
Raju, R. M., & Smith, C. J. W. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02162-8 · Cited by 4 · see citing works
Li, Z., Kruck, G., Thng, G., & Nagy, C. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.05.023 · Cited by 2 · see citing works
Gargus, M., Poyhia, L., Errico, J. P., Rogers, M. K. N., & Tremblay, M. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1827714 · Cited by 2 · see citing works
Self-citationCupo, L., Guma, E., Gallino, D., Mar, K., Fowler, C., Dehghani, M., Near, J., Devenyi, G. A., & Chakravarty, M. M. (2022) · Preprints.org · doi:10.20944/preprints202203.0136.v1 · Cited by 2 · see citing works
Toll-like receptors as a missing link in Notch signaling cascade during neurodevelopment
Stojanovic, M., & Bognar, S. K. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1465023 · Cited by 1 · see citing works
Rodrigues‐Neves, A. C., Monteiro, J., Coimbra, B., Gaspar, R., Domingues, V., Soares‐Cunha, C., Patrício, P., Pereira, M. I., Cardoso, A. L., Pinto, L., et al. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.06.009 · Cited by 1 · see citing works
Albrecht, G. L., Ramirez, R., Moradpour, D., Mar, J. S., Fortes, R. C., McGregor, M. A., Raghuraman, V., & Farhy-Tselnicker, I. (2025) · iScience · doi:10.1016/j.isci.2025.113997 · Cited by 1 · see citing works
van de Garde, N., Meng, Q., Dontamsetti, G., Kiridena, P., Lü, D., Masson, B. A., Adithya, P., Liao, H., Reisinger, S. N., & Hannan, A. J. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106599 · Cited by 1 · see citing works
Le, L., Eliseeva, S. I., Kara-Pabani, K., Li, H., Yarovinsky, F., & Majewska, A. K. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4795163
Lcn2 deficiency leads to social impairments independent of maternal immune activationPreprint
Pękała, M., Zawiślak, S., Romanis, S., Nader, K., Cabaj, A., Madecka, A., Puścian, A., Knapska, E., Pawlak, R., Kaczmarek, L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.27.661499
Li, R., Fu, X., Li, C., Yuan, L., Liu, Y., Yang, L., Fang, X., Zhang, X., Zhang, G., & Du, X. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1697383
Lcn2 deficiency leads to long-lasting social impairments independent of maternal immune activation
Pekala, M., Zawiślak, S., Romanis, S., Nader, K., Dzwonek, J., Cabaj, A., Madecka, A., Puścian, A., Knapska, E., Pawlak, R., et al. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03742-1
Boughanmi, M.-E., Leboyer, M., Demily, C., & Rey, R. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.18.709827
Shi, J., Pan, Y., Tao, Y., Wang, J., Huang, J., & Liu, W. W. (2026) · Psychopharmacology · doi:10.1007/s00213-026-07051-6
P2X4 Drives Sex-Specific neuroprotection in autoimmune neuroinflammation
Mata, P., Bosch-Juan, M., Luengo-Arias, S., Montilla, A., Astiz, M., Battefeld, A., Carracedo, S., Sánchez‐Gómez, M. V., Matute, C., Pérez‐Samartín, A., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106771
Spagnuolo, M. S., Macchioni, G., Petecca, N., Petruccioli, G., Magistris, M. D., Palma, F. D., Prisco, M., Cipriani, C., Siracusano, M., Calamandrei, G., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106820
Boughanmi, M.-E., Lespine, L., Leboyer, M., Demily, C., & Rey, R. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106865
McEwan, F., Santo, J. D., Kambara, C., Tarrat-Castells, M., Woods, R. M., Harte, M., Glazier, J. D., & Hager, R. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106895
Sentyabreva, A. V., Lyamtsev, A. S., Melnikova, E. A., Aliper, G. M., & Kosyreva, A. M. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27188222
Anguiano-Buenfil, J., Sollozo-Dupont, I., Márquez, L. A., Zepeda, A., & Galván, E. J. (2026) · Hippocampus · doi:10.1002/hipo.70132
Hyperexcitable but seizure-free: hippocampal network dysfunction in a Wolfram syndrome modelPreprint
Ahmadi, S., Pinera, J. G., Dokholyan, S., Sauerbeck, A. D., Phan, H. N., Carman, B., Debnath, A., Brunwasser, S., Skinner, G., Rensing, N. R., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.27.754840
- Authors
- Hui, C. W., Vecchiarelli, H. A., Gervais, É., Luo, X., Michaud, F., Scheefhals, L., Bisht, K., Sharma, K., Topolnik, L., & Tremblay, M.-È.
- Affiliations
- Centre hospitalier de l'Université Laval (CA)
- University of Victoria (CA)
- Utrecht University (NL)
- University of British Columbia (CA)
- Corresponding author
- Topolnik, Lisa
- Tremblay, Marie-Ève
- ORCID
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2020-10-15
- Volume
- 14
- Pages
- 558181-558181
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC7593822
- OpenAlex
- W3093181376
- Cited by
- 64
- References
- 57
- Citations by year
- 2026: 13 · 2025: 10 · 2024: 14 · 2023: 11 · 2022: 12 · 2021: 4
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Brain and Behavior Research Foundation
- Université Laval
- University of Victoria
- National Alliance for Research on Schizophrenia and Depression
- Canadian Institutes of Health Research (Tier 2, 137072_1, FDN341846, 142447_1, 13707_2)
- Natural Sciences and Engineering Research Council of Canada (342292, 342292-2012)
- Fonds de Recherche du Québec - Santé
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- maternal immune activation, schizophrenia, sex differences, microglia, synaptic pruning, dentate gyrus, excitatory synapses, inhibitory synapses, CD68, CD11b, phagocytosis, complement system, anxiety-like behavior, sensorimotor gating, sociability, stereotypy, granule cells, mouse model
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