Cited by 1,206Tryptophan and brain disordersNeuroinflammation and Neurodegeneration MechanismsStress Responses and Cortisol

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Maternal immune activation: Implications for neuropsychiatric disorders

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Estes, Myka L., McAllister, A. Kimberley·2016·Science

DOI 10.1126/science.aag3194PMC PMC5650490

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Abstract

Epidemiological evidence implicates maternal infection as a risk factor for autism spectrum disorder and schizophrenia. Animal models corroborate this link and demonstrate that maternal immune activation (MIA) alone is sufficient to impart lifelong neuropathology and altered behaviors in offspring. This Review describes common principles revealed by these models, highlighting recent findings that strengthen their relevance for schizophrenia and autism and are starting to reveal the molecular mechanisms underlying the effects of MIA on offspring. The role of MIA as a primer for a much wider range of psychiatric and neurologic disorders is also discussed. Finally, the need for more research in this nascent field and the implications for identifying and developing new treatments for individuals at heightened risk for neuroimmune disorders are considered.

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Background
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Extracellular Free Water Elevations are Associated with Brain Volume and Maternal Cytokine Response in a Longitudinal Nonhuman Primate Maternal Immune Activation Model
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“…of normal brain development and healthy synaptic function, these ﬁ ndings have prompted interest in developing preclinical models that can offer better insight into the mechanism by which exposure to these in ﬂ ammatory factors may increase the risk for neurodevelopmental disorders [13, 14].”
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Resveratrol ameliorates the effect of maternal immune activation associated with schizophrenia in adulthood offspring
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Wang, H., He, H., Miao, M., Yu, Y., Liu, H., Zhang, J., Li, F., & Li, J. (2021) · Epidemiology and Psychiatric Sciences · doi:10.1017/s2045796021000421 · Cited by 16
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BackgroundMethod
Altered dendritic morphology in dorsolateral prefrontal cortex of nonhuman primates prenatally exposed to maternal immune activation
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Background
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Background
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Background
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Background
Integrative analysis identifies IL-6/JUN/MMP-9 pathway destroyed blood-brain-barrier in autism mice via machine learning and bioinformatic analysis
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Background
Association between cumulative maternal exposures related to inflammation and child attention‐deficit/hyperactivity disorder: A cohort study
Nielsen, T. C., Nassar, N., Shand, A., Jones, H. F., Han, V. X., Patel, S., Guastella, A. J., Dale, R. C., & Lain, S. J. (2023) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.13022 · Cited by 12
Maternal Influenza and Offspring Neurodevelopment
Egorova, M., Egorov, V. V., & Zabrodskaya, Y. A. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46010023 · Cited by 15
“These changes can lead to cognitive and behavioral deficits by affecting synapse formation and synaptic function in affected offspring [65].”
Background
Maternal prenatal immune activation associated with brain tissue microstructure and metabolite concentrations in newborn infants
Spann, M. N., Bansal, R., Aydin, E., Pollatou, A., Alleyne, K., Bennett, M., Sawardekar, S., Delapenha, K., Cheng, B., Lee, S., et al. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.08.025 · Cited by 13
Bi-allelic NRXN1α deletion in microglia derived from iPSC of an autistic patient increases interleukin-6 production and impairs supporting function on neuronal networking
Bose, R., Posada-Pérez, M., Karvela, E., Škandík, M., Keane, L., Falk, A., Spulber, S. D., Joseph, B., & Ceccatelli, S. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.09.001 · Cited by 15
“…by brain impairments, including altered neuronal circuits, that affect communication skills and behaviours of the affected individuals (Constantino et al., 2010; Estes and McAllister, 2016; Hahamy et al., 2015; Janecka et al., 2017; Liu et al., 2013; Tick et al., 2016; Tran and Miyake, 2017).”
Dysregulation of the mTOR-FMRP pathway and synaptic plasticity in an environmental model of ASD
Hilal, M. L., Rosina, E., Pedini, G., Restivo, L., & Bagni, C. (2025) · Molecular Psychiatry · doi:10.1038/s41380-024-02805-0 · Cited by 13
Dynamic neuro-immune regulation of psychiatric risk loci in human neurons
Townsley, K. G., Lee, S. H., Williams, S., Cartwright, S., Cohen, S., Sen, A., Jia, M., Young, H. E., Dobbyn, L., Deans, M., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-77114-x · Cited by 14
“Neurodevelopment represents a key window during which environmental exposures interact with genetic risk 14 .”
Non-reassuring foetal status and neonatal irritability in the Japan Environment and Children’s Study: A cohort study
Morokuma, S., Michikawa, T., Kato, K., Sanefuji, M., Shibata, E., Tsuji, M., Senju, A., Kawamoto, T., Ohga, S., & Kusuhara, K. (2018) · Scientific Reports · doi:10.1038/s41598-018-34231-y · Cited by 13
Inflammation in pediatric epilepsies: Update on clinical features and treatment options
Granata, T., Fusco, L., Matricardi, S., Tozzo, A., Janigro, D., & Nabbout, R. (2021) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2021.107959 · Cited by 14
Inflammatory cytokines, placental pathology, and neurological outcomes in infants born to preterm preeclamptic mothers
Sotiros, A., Thornhill, D., Post, M. D., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0260094 · Cited by 13
Maternal immune activation downregulates schizophrenia genes in the foetal mouse brain
Handunnetthi, L., Saatci, D., Hamley, J. C., & Knight, J. C. (2021) · Brain Communications · doi:10.1093/braincomms/fcab275 · Cited by 13
“For example, offspring from mice exposed to polyinosinic:polycytidylic acid (polyI:C), a synthetic doublestranded RNA molecule that mimics viral infection, show pathological neurochemical and behavioural phenotypes that are characteristic of schizophrenia.(14,15) However, our understanding of the mechanisms by which M…”
Neonatal immune challenge influences the microbiota and behaviour in a sexually dimorphic manner
Cuskelly, A., Hoedt, E. C., Harms, L. R., Talley, N. J., Tadros, M. A., Keely, S., & Hodgson, D. M. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.04.023 · Cited by 13
Modulation of human endogenous retroviruses and cytokines expression in peripheral blood mononuclear cells from autistic children and their parents
Cipriani, C., Giudice, M., Petrone, V., Fanelli, M., Minutolo, A., Miele, M. T., Toschi, N., Maracchioni, C., Siracusano, M., Benvenuto, A., et al. (2022) · Retrovirology · doi:10.1186/s12977-022-00603-6 · Cited by 14
“Indeed, during pregnancy, the maternal immune response induced by several environmental insults could affect different stages of neurodevelopment in the foetus, contributing to the appearance of altered phenotypes early in childhood as well as adult or aged progeny, highlighting the close interconnection between the i…”
Background
Impact of prenatal COVID-19 vaccination on delivery and neonatal outcomes: Results from a New York City cohort
Ibroçi, E., Liu, X., Lieb, W., Jessel, R. H., Gigase, F. A. J., Chung, K., Graziani, M., Lieber, M., Ohrn, S., Lynch, J., et al. (2022) · Vaccine · doi:10.1016/j.vaccine.2022.09.095 · Cited by 13
“animal [12,13] and epidemiological [14–16] research suggests that prenatal exposure to inflammation may lead to adverse pregnancy outcomes.”
Background
Neonatal inflammation increases hippocampal KCC2 expression through methylation-mediated TGF-β1 downregulation leading to impaired hippocampal cognitive function and synaptic plasticity in adult mice
Rong, J., Yang, Y., Liang, M., Zhong, H., Li, Y., Zhu, Y., Sha, S., Chen, L., & Zhou, R. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02697-x · Cited by 13
Interaction between maternal immune activation and peripubertal stress in rats: impact on cocaine addiction-like behaviour, morphofunctional brain parameters and striatal transcriptome
Capellán, R., Orihuel, J., Marcos, A., Ucha, M., Moreno, M. G., Casquero‐Veiga, M., Soto‐Montenegro, M. L., Desco, M., Oteo, M., Ibanez-Moragues, M., et al. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02378-6 · Cited by 13
“MIA models recapitulate several aspects of the disease [4, 5].”
Background
Interaction of the pre- and postnatal environment in the maternal immune activation model
Gundacker, A., Rico, L. C., Stöhrmann, P., Tillmann, K. E., Weber‐Stadlbauer, U., & Pollak, D. D. (2023) · Discover Mental Health · doi:10.1007/s44192-023-00042-5 · Cited by 15
“…of MIA for phenotypes related to neuropsychiatric disorders, including the anxiety disorder and depression, as well as autism spectrum disorders and schizophrenia have been repeatedly and robustly demonstrated across a wide range of experimental set-ups and animal species [16, 46, 74–76 , 78 ].”
Background
Mid-gestation cytokine profiles in mothers of children affected by autism spectrum disorder: a case–control study
Carter, M., Casey, S., O’Keeffe, G. W., Gibson, L., & Murray, D. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-01662-z · Cited by 13
Neuropsychiatric disorders: An immunological perspective
Aw, E., Zhang, Y., Yalçın, E., Herrmann, U., & Carroll, M. C. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.09.002 · Cited by 13
Efficacy of Virtual Reality–Based Interventions on Cognitive Function in Patients With Neuropsychiatric Disorders: Systematic Review and Meta-Analysis of Randomized Controlled Trials
Du, Q., Wei, Y., Ma, Y., Liu, C., Du, S., Zhang, Q., Gong, X., Yang, J., Li, Q., & Li, K. (2025) · JMIR Serious Games · doi:10.2196/67501 · Cited by 15
““Patients with neuropsychiatric disorders” refer to individuals enduring neurological or psychiatric conditions, or those exhibiting symptoms pertinent to both neurology and psychiatry [1].”
Supplementation of 2′-Fucosyllactose during the Growth Period Improves Neurodevelopmental Disorders in Offspring Mice Induced by Maternal Immune Activation
Wu, X., Cao, T., Ye, J., Shi, R., Bao, X., Ge, Y., Li, D., Hao, S., Liu, F., & Liu, X. (2025) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5c01184 · Cited by 11
Neurodevelopmental Impact of Maternal Immune Activation and Autoimmune Disorders, Environmental Toxicants and Folate Metabolism on Autism Spectrum Disorder
Ayoub, G. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47090721 · Cited by 12
“This imbalance underlies symptoms such as cognitive rigidity and repetitive behaviors, hallmarks of ASD [15,16,18–22].”
Environmental factors associated with microcephaly in Africa: A systematic review
Izabayo, P., Hakizimana, J. C., Uwineza, A., & Alagbonsi, A. I. (2025) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2025.107577 · Cited by 13
Cord Serum Cytokines at Birth and Children’s Anxiety-Depression Trajectories From 3 to 8 Years: The EDEN Mother–Child Cohort
Galéra, C., Barbosa, S., Collet, O. A., Khalfallah, O., Aouizerate, B., Sutter‐Dallay, A., Koehl, M., Capuron, L., van der Waerden, J. E. B., Melchior, M., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.10.009 · Cited by 12
WWOX P47T partial loss-of-function mutation induces epilepsy, progressive neuroinflammation, and cerebellar degeneration in mice phenocopying human SCAR12
Hussain, T., Sanchez, K. G., Crayton, J., Saha, D., Jeter, C. R., Lu, Y., Abba, M. C., Seo, R., Noebels, J. L., Fonken, L. K., et al. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102425 · Cited by 11
“Further, microglial dysfunction is implicated in several neurodevelopmental and neurodegenerative disorders; for example, microgliosis is known to contribute to deficits in social behavior in other contexts (Estes and McAllister, 2016).”
Sex differences in offspring risk and resilience following 11β-hydroxylase antagonism in a rodent model of maternal immune activation
Martz, J., Shelton, M. A., Geist, L., Seney, M. L., & Kentner, A. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01771-5 · Cited by 12
“Moreover, these observed disruptions can be mirrored in laboratory animals by administering bacterial and viral mimetics during pregnancy [3].”
Influential
Prenatal particulate matter exposure is linked with neurobehavioural development in early life
Cosemans, C., Madhloum, N., Sleurs, H., Alfano, R., Verheyen, L., Wang, C., Vanbrabant, K., Vanpoucke, C., Lefebvre, W., Nawrot, T. S., et al. (2024) · Environmental Research · doi:10.1016/j.envres.2024.118879 · Cited by 12
Maternal immune activation induces sex-dependent behavioral differences in a rat model of schizophrenia
Yunxia, L., Hang, X., Zhang, Y., Fang, Y., Yuan, S., Zhang, Y., Wu, B., Kong, Y., Kuang, Z., & Sun, W. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1375999 · Cited by 12
Cannabidiol improves maternal obesity-induced behavioral, neuroinflammatory and neurochemical dysfunctions in the juvenile offspring
Rodrigues, F. D. S., Jantsch, J., Fraga, G. D. F., Milczarski, V. L. D. C., Dias, V. S., Scheid, C., Merib, J. D. O., Giovernardi, M., & Guedes, R. P. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.04.010 · Cited by 13
Prenatal maternal Inflammation, childhood cognition and adolescent depressive symptoms
Pike, M. R., Lipner, E., O’Brien, K. J., Breen, E. C., Cohn, B. A., Cirillo, P. M., Krigbaum, N. Y., Kring, A. M., Olino, T. M., Alloy, L. B., et al. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.05.012 · Cited by 12
“…biological vulnerabilities and environmental stressors during childhood and adolescence (e.g., postnatal stress and adversity) that combine with the sequalae of higher PNMI exposure to increase the likelihood of offspring developing psychiatric disorders (Estes & McAllister, 2016).”
Maternal Immune Activation with Toll-Like Receptor 7 Agonist During Mid-Gestation Alters Juvenile and Adult Developmental Milestones and Behavior
Sheng, J. A., & Tobet, S. (2024) · Journal of neuroendocrinology · doi:10.1111/jne.13417 · Cited by 11
Arachidonic acid‐derived dihydroxy fatty acids in neonatal cord blood relate symptoms of autism spectrum disorders and social adaptive functioning: Hamamatsu Birth Cohort for Mothers and Children ( HBC Study )
Hirai, T., Umeda, N., Harada, T., Okumura, A., Nakayasu, C., Ohto‐Nakanishi, T., Tsuchiya, K. J., Nishimura, T., & Matsuzaki, H. (2024) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.13710 · Cited by 16
“8 Intriguingly, alterations in cytokine and metabolic pro ﬁ ling in cord and maternal mid-pregnancy plasma from mothers of children with ASD have been found to differ between the sexes.”
Background
Microglial regulation of white matter development and its disruption in autism spectrum disorder
Canada, K., Evans, T. M., & Pelphrey, K. A. (2025) · Cerebral Cortex · doi:10.1093/cercor/bhaf109 · Cited by 13
The close link between the fetal programming imprinting and neurodegeneration in adulthood: The key role of “hemogenic endothelium” programming
Allegra, A., Giarratana, R. M., Scola, L., & Balistreri, C. R. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111461 · Cited by 12
Prenatal exposure to metals and autism spectrum disorder: Current status and future directions
Campbell, K. A., Hickman, R. C., Fallin, M. D., & Bakulski, K. M. (2021) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2021.04.001 · Cited by 12
Mouse models of immune dysfunction: their neuroanatomical differences reflect their anxiety-behavioural phenotype
Fernandes, D., Spring, S., Corre, C., Tu, A., Qiu, L. R., Hammill, C. F., Vousden, D. A., Noakes, T. L. S., Nieman, B. J., Bowdish, D. M. E., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01535-5 · Cited by 12
Maternal rheumatoid arthritis and risk of autism in the offspring
Yin, W., Norrbäck, M., Levine, S. Z., Rivera, N. V., Buxbaum, J. D., Zhu, H., Yip, B. H. K., Reichenberg, A., Askling, J., & Sandin, S. (2023) · Psychological Medicine · doi:10.1017/s0033291723000855 · Cited by 12
“Children of mothers with RA are potentially exposed to auto-antibodies and inflammatory mediators in utero which may alter fetal brain development (Estes & McAllister, 2016; Parker-Athill & Tan, 2010; Smith et al., 2007).”
The first cortical circuits: Subplate neurons lead the way and shape cortical organization
Kanold, P. O. (2018) · e-Neuroforum · doi:10.1515/nf-2018-0010 · Cited by 11
“Similarly, maternal stress or inflammation (Estes and McAllister, 2016) can potentially alter SPN function.”
Background
Impact of Season of Birth on Psychiatric Disorder Susceptibility and Drug Abuse Incidence in a Population from the Köppen Tropical Savanna Region of Brazil
Ferreira, F. R., de Paula, G. C., de Carvalho, R. J. V., Ribeiro-Barbosa, É. R., & Spini, V. B. M. G. (2019) · Neuropsychobiology · doi:10.1159/000503069 · Cited by 12
Shedding light on the role of CX3CR1 in the pathogenesis of schizophrenia
Chamera, K., Szuster-Głuszczak, M., & Basta‐Kaim, A. (2021) · Pharmacological Reports · doi:10.1007/s43440-021-00269-5 · Cited by 12
“One of the approaches to investigate schizophrenia-like disturbances in animals involves the maternal immune activation (MIA) paradigm [163, 164] (Table 2).”
Background
Alterations of Electrophysiological Properties and Ion Channel Expression in Prefrontal Cortex of a Mouse Model of Schizophrenia
Mi, Z., Yang, J., He, Q., Zhang, X., Xiao, Y., & Shu, Y. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00554 · Cited by 12
“There is ample evidence that maternal immune activation (MIA) can act as a disease primer to increase the risk of neuropsychiatric disorders in offspring (Feigenson et al., 2014; Davis et al., 2016; Estes and McAllister, 2016), while social deprivation during adolescence has been thought to work as a second-hit leadin…”
Background
Redox System Dysfunction as a Key Mechanism in Autism Spectrum Disorder Pathogenesis
de Oliveira, C. A., Iorio, E. L., & Espíndola, F. S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26209850 · Cited by 12
“Glutathione depletion correlates with oxidative injury in the hippocampus, cerebellum, and temporal cortex, reinforcing excitatory/inhibitory imbalance [239,300].”
Interaction of extraembryonic microglia and neonatal brain development
Sharma, R., Mei, A., Mathew, V., Kashpur, O., & Wallingford, M. C. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.113986 · Cited by 11

Authors: Estes, M. L., & McAllister, A. K.
Affiliations: University of California, Davis (US)
Corresponding author: McAllister, A. Kimberley
ORCID: Estes, Myka L.
McAllister, A. Kimberley
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2016-08-19
Volume: 353
Issue: 6301
Pages: 772-777
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.aag3194
PMC: PMC5650490
OpenAlex: W2515897135
Semantic Scholar: 70e346df06748a0e6435133309a1011e2a43f998
Cited by: 1,206
References: 86
Citations by year: 2026: 109 · 2025: 134 · 2024: 134 · 2023: 128 · 2022: 158 · 2021: 139 · 2020: 119 · 2019: 114 · 2018: 104 · 2017: 54 · 2016: 10
FWCI: 5.73
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01-NS060125-05)
National Institute of Mental Health (P50-MH106438-01)
Simons Foundation (321998)
University of California Davis Research Investments in Science and Engineering Program
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: maternal immune activation, maternal infection, autism spectrum disorder, schizophrenia, neuropsychiatric disorders, animal models, neuropathology, neuroimmunological diseases, molecular mechanisms, risk factors
MeSH terms: Autism Spectrum Disorder, Adolescent, Animals, Brain, Child, Child, Preschool, Disease Models, Animal, Female, Humans, Immune System, Immune System Diseases, Mothers, Pregnancy, Pregnancy Complications, Infectious, Risk Factors, Schizophrenia, Gastrointestinal Tract, Young Adult

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Maternal immune activation: Implications for neuropsychiatric disorders

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