Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates

Careaga, Milo; Murai, Takeshi; Bauman, Melissa D.

doi:10.1016/j.biopsych.2016.10.020

Cited by 348Autism Spectrum Disorder ResearchTryptophan and brain disordersMaternal Mental Health During Pregnancy and Postpartum

Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates

Open access

Careaga, Milo, Murai, Takeshi, Bauman, Melissa D.·2017·Biological Psychiatry

DOI 10.1016/j.biopsych.2016.10.020PMC PMC5513502

Open this paper in CoChat — free account

Abstract

A subset of women who are exposed to infection during pregnancy have an increased risk of giving birth to a child who will later be diagnosed with a neurodevelopmental or neuropsychiatric disorder. Although epidemiology studies have primarily focused on the association between maternal infection and an increased risk of offspring schizophrenia, mounting evidence indicates that maternal infection may also increase the risk of autism spectrum disorder. A number of factors, including genetic susceptibility, the intensity and timing of the infection, and exposure to additional aversive postnatal events, may influence the extent to which maternal infection alters fetal brain development and which disease phenotype (autism spectrum disorder, schizophrenia, other neurodevelopmental disorders) is expressed. Preclinical animal models provide a test bed to systematically evaluate the effects of maternal infection on fetal brain development, determine the relevance to human central nervous system disorders, and to evaluate novel preventive and therapeutic strategies. Maternal immune activation models in mice, rats, and nonhuman primates suggest that the maternal immune response is the critical link between exposure to infection during pregnancy and subsequent changes in brain and behavioral development of offspring. However, differences in the type, severity, and timing of prenatal immune challenge paired with inconsistencies in behavioral phenotyping approaches have hindered the translation of preclinical results to human studies. Here we highlight the promises and limitations of the maternal immune activation model as a preclinical tool to study prenatal risk factors for autism spectrum disorder, and suggest specific changes to improve reproducibility and maximize translational potential.

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

Crossref · 10.1016/j.biopsych.2016.10.020

Cites

147 of 147 references verified0 citation errors · 0 not checkable

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?

Maternal immune activation appears to play a significant role in many cases of idiopathic autism, suggesting a shared mechanism of risk.
“Interestingly, maternal immune activation (MIA) appears to play a significant role in many cases of idiopathic autism, suggesting a shared mechanism of risk [33].”
From The Relationship between Autism and Ehlers-Danlos Syndromes/Hypermobility Spectrum Disorders (2020) · cites this paper as [33]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000412 · Cited by 7,300 · see citing works
Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · Journal of Pharmacology and Pharmacotherapeutics · doi:10.4103/0976-500x.72351 · Cited by 6,277 · see citing works
Toll-like receptors and innate immunity
Medzhitov, R. (2001) · Nature Reviews Immunology · doi:10.1038/35100529 · Cited by 4,308 · see citing works
Induction of Colonic Regulatory T Cells by Indigenous <i>Clostridium</i> Species
Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., et al. (2011) · Science · doi:10.1126/science.1198469 · Cited by 3,752 · see citing works
Microbiota Modulate Behavioral and Physiological Abnormalities Associated with Neurodevelopmental Disorders
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283 · see citing works
Toward the future of psychiatric diagnosis: the seven pillars of RDoC
Cuthbert, B. N., & Insel, T. R. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-126 · Cited by 3,053 · see citing works
Neuroglial activation and neuroinflammation in the brain of patients with autism
Vargas, D. L., Nascimbene, C., Krishnan, C., Zimmerman, A. W., & Pardo, C. A. (2005) · Annals of Neurology · doi:10.1002/ana.20315 · Cited by 2,149 · see citing works
Animal models of neuropsychiatric disorders
Nestler, E. J., & Hyman, S. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2647 · Cited by 2,023 · see citing works
Maternal Immune Activation Alters Fetal Brain Development through Interleukin-6
Smith, S. E. P., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2178-07.2007 · Cited by 1,605 · see citing works
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
Neuroanatomy of autism
Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2007.12.005 · Cited by 1,492 · see citing works
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462 · see citing works
The validity of animal models of depression
Willner, P. (1984) · Psychopharmacology · doi:10.1007/bf00427414 · Cited by 1,415 · see citing works
Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies
Brown, A. S., & Derkits, E. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09030361 · Cited by 1,269 · see citing works
Policy: NIH plans to enhance reproducibility
Collins, F. S., & Tabak, L. A. (2014) · Nature · doi:10.1038/505612a · Cited by 1,247 · see citing works
Translating developmental time across mammalian species
Clancy, B., Darlington, R. B., & Finlay, B. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00171-3 · Cited by 1,221 · see citing works
The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring
Choi, G. B., Yim, Y. S., Wong, H., Kim, S., Kim, H., Kim, S. V., Hoeffer, C. A., Littman, D. R., & Huh, J. R. (2016) · Science · doi:10.1126/science.aad0314 · Cited by 1,214 · see citing works
Maternal immune activation: Implications for neuropsychiatric disorders
Estes, M. L., & McAllister, A. K. (2016) · Science · doi:10.1126/science.aag3194 · Cited by 1,206 · see citing works
A call for transparent reporting to optimize the predictive value of preclinical research
Landis, S. C., Amara, S. G., Asadullah, K., Austin, C. P., Blumenstein, R., Bradley, E. W., Crystal, R. G., Darnell, R. B., Ferrante, R. J., Fillit, H., et al. (2012) · Nature · doi:10.1038/nature11556 · Cited by 1,196 · see citing works
Visual scanning of faces in autism
Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1016374617369 · Cited by 1,187 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Maternal Infection Requiring Hospitalization During Pregnancy and Autism Spectrum Disorders
Atladóttir, H. Ó., Thorsen, P., Østergaard, L., Schendel, D. E., Lemcke, S., Abdallah, M., & Parner, E. T. (2010) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1006-y · Cited by 916 · see citing works
Maternal immune activation and abnormal brain development across CNS disorders
Knuesel, I., Chicha, L., Britschgi, M., Schobel, S. A., Bodmer, M., Hellings, J. A., Toovey, S., & Prinssen, E. P. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.187 · Cited by 880 · see citing works
Cytokines and CNS Development
Deverman, B. E., & Patterson, P. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.002 · Cited by 865 · see citing works
The Time of Prenatal Immune Challenge Determines the Specificity of Inflammation-Mediated Brain and Behavioral Pathology
Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B. K., & Feldon, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0099-06.2006 · Cited by 774 · see citing works
Immune involvement in schizophrenia and autism: Etiology, pathology and animal models
Patterson, P. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.016 · Cited by 766 · see citing works
Microglial Activation and Increased Microglial Density Observed in the Dorsolateral Prefrontal Cortex in Autism
Morgan, J. T., Chana, G., Pardo, C. A., Achim, C., Semendeferi, K., Buckwalter, J., Courchesne, E., & Everall, I. P. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.024 · Cited by 749 · see citing works
Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered
Preuss, T. M. (1995) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1995.7.1.1 · Cited by 666 · see citing works
Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism
Malkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J., & Patterson, P. H. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.011 · Cited by 662 · see citing works
Prenatal Poly(I:C) Exposure and Other Developmental Immune Activation Models in Rodent Systems
Meyer, U. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.011 · Cited by 626 · see citing works
Effects of prenatal infection on brain development and behavior: A review of findings from animal models
Boksa, P. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.03.005 · Cited by 603 · see citing works
Automated Three‐Chambered Social Approach Task for Mice
Yang, M., Silverman, J. L., & Crawley, J. N. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0826s56 · Cited by 598 · see citing works
Maternal infection and immune involvement in autism
Patterson, P. H. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.03.001 · Cited by 520 · see citing works
Immune mediators in the brain and peripheral tissues in autism spectrum disorder
Estes, M. L., & McAllister, A. K. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3978 · Cited by 514 · cited 1× · see citing works
“Although underlying genetic and environmental cause(s) remain unknown for most ASD cases, recent evidence suggests that the prenatal immune environment may be a particularly promising area of ASD etiology research (2-4).”
Background
Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia
Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.012 · Cited by 494 · see citing works
Stress in Puberty Unmasks Latent Neuropathological Consequences of Prenatal Immune Activation in Mice
Giovanoli, S., Engler, H., Engler, A., Richetto, J., Voget, M., Willi, R., Winter, C., Riva, M. A., Mortensen, P. B., Feldon, J., et al. (2013) · Science · doi:10.1126/science.1228261 · Cited by 459 · see citing works
Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice
Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., & Feldon, J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.09.012 · Cited by 457 · see citing works
Autism in children with congenital rubella
Chess, S. (1971) · Journal of Autism and Childhood Schizophrenia · doi:10.1007/bf01537741 · Cited by 457 · see citing works
Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression
Belzung, C., & Lemoine, M. (2011) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-1-9 · Cited by 445 · see citing works
Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism
Brown, A. S. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22024 · Cited by 420 · see citing works
A voice region in the monkey brain
Petkov, C. I., Kayser, C., Steudel, T., Whittingstall, K., Augath, M. A., & Logothetis, N. K. (2008) · Nature Neuroscience · doi:10.1038/nn2043 · Cited by 401 · see citing works
Autism After Infection, Febrile Episodes, and Antibiotic Use During Pregnancy: An Exploratory Study
Atladóttir, H. Ó., Henriksen, T. B., Schendel, D. E., & Parner, E. T. (2012) · Pediatrics · doi:10.1542/peds.2012-1107 · Cited by 369 · see citing works
A Neurodevelopmental Perspective on the Research Domain Criteria (RDoC) Framework
Casey, B. J., Oliveri, M. E., & Insel, T. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.01.006 · Cited by 369 · see citing works
In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works
Prenatal exposure to drugs: effects on brain development and implications for policy and education
Thompson, B. L., Levitt, P. R., & Stanwood, G. D. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2598 · Cited by 367 · see citing works
Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development
Garay, P. A., Hsiao, E. Y., Patterson, P. H., & McAllister, A. K. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.07.008 · Cited by 366 · see citing works
Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?
MEYER, U., FELDON, J., & DAMMANN, O. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e318212c196 · Cited by 357 · cited 2× · see citing works
“The emerging consensus among leaders in the field is that prenatal infection may be relevant to a number of CNS diseases and restricting interpretation to a specific human disorder may limit the utility and relevance of the MIA model (38, 39).”
Background
Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring
Zuckerman, L., & Weiner, I. (2004) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2004.08.008 · Cited by 352 · see citing works
Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: A case-control study
Goines, P. E., Croen, L. A., Braunschweig, D., Yoshida, C. K., Grether, J., Hansen, R., Kharrazi, M., Ashwood, P., & Van de Water, J. (2011) · Molecular Autism · doi:10.1186/2040-2392-2-13 · Cited by 351 · see citing works
Elevated maternal C-reactive protein and autism in a national birth cohort
Brown, A. S., Sourander, A., Hinkka-Yli-Salomäki, S., McKeague, I. W., Sundvall, J., & Surcel, H.-M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2012.197 · Cited by 343 · see citing works
Modeling an autism risk factor in mice leads to permanent immune dysregulation
Hsiao, E. Y., McBride, S. W., Chow, J., Mazmanian, S. K., & Patterson, P. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202556109 · Cited by 340 · see citing works
The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse?
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · Cited by 303 · see citing works
Maternal Infection During Pregnancy and Autism Spectrum Disorders
Zerbo, O., Qian, Y., Yoshida, C., Grether, J. K., Van de Water, J., & Croen, L. A. (2015) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-013-2016-3 · Cited by 298 · see citing works
Activation of the Maternal Immune System During Pregnancy Alters Behavioral Development of Rhesus Monkey Offspring
Bauman, M. D., Iosif, A.-M., Smith, S. E. P., Bregere, C., Amaral, D. G., & Patterson, P. H. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.025 · Cited by 294 · see citing works
Self-citation
Microglia in the Cerebral Cortex in Autism
Tetreault, N. A., Hakeem, A. Y., Jiang, S., Williams, B. A., Allman, E., Wold, B. J., & Allman, J. M. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1513-0 · Cited by 288 · see citing works
Is Maternal Influenza or Fever During Pregnancy Associated with Autism or Developmental Delays? Results from the CHARGE (CHildhood Autism Risks from Genetics and Environment) Study
Zerbo, O., Iosif, A.-M., Walker, C., Ozonoff, S., Hansen, R. L., & Hertz-Picciotto, I. (2013) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1540-x · Cited by 277 · see citing works
Activation of the maternal immune system alters cerebellar development in the offspring
Shi, L., Smith, S. E. P., Malkova, N., Tse, D., Su, Y., & Patterson, P. H. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.07.012 · Cited by 277 · see citing works
The involvement of Reelin in neurodevelopmental disorders
Folsom, T. D., & Fatemi, S. H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.015 · Cited by 275 · see citing works
Maternal inflammation disrupts fetal neurodevelopment via increased placental output of serotonin to the fetal brain
Goeden, N., Velasquez, J., Arnold, K. A., Chan, Y., Lund, B. T., Anderson, G. M., & Bonnin, A. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2534-15.2016 · Cited by 264 · see citing works
Immunological stress at the maternal–foetal interface: A link between neurodevelopment and adult psychopathology
Meyer, U., Feldon, J., Schedlowski, M., & Yee, B. K. (2005) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2005.11.003 · Cited by 260 · see citing works
Autism with intellectual disability is associated with increased levels of maternal cytokines and chemokines during gestation
Jones, K. L., Croen, L. A., Yoshida, C. K., Heuer, L., Hansen, R., Zerbo, O., DeLorenze, G. N., Kharrazi, M., Yolken, R., Ashwood, P., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.77 · Cited by 260 · see citing works
Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology
Abazyan, B., Nomura, J., Kannan, G., Ishizuka, K., Tamashiro, K. L., Nucifora, F., Pogorelov, V., Ladenheim, B., Yang, C., Krasnova, I. N., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.022 · Cited by 255 · see citing works
Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling
Meyer, U., Murray, P. J., Urwyler, A., Yee, B. K., Schedlowski, M., & Feldon, J. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002042 · Cited by 252 · see citing works
Autistic disorder and viral infections
Libbey, J., Sweeten, T., McMahon, W., & Fujinami, R. (2005) · Journal of NeuroVirology · doi:10.1080/13550280590900553 · Cited by 252 · see citing works
To poly(I:C) or not to poly(I:C): Advancing preclinical schizophrenia research through the use of prenatal immune activation models
Meyer, U., & Feldon, J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.009 · Cited by 247 · see citing works
Autism spectrum disorders and neuropathology of the cerebellum
Hampson, D. R., & Blatt, G. J. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00420 · Cited by 247 · see citing works
Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia
Bitanihirwe, B. K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., & Meyer, U. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.129 · Cited by 237 · see citing works
Comparison of social cognitive functioning in schizophrenia and high functioning autism: more convergence than divergence
Couture, S. M., Penn, D. L., Losh, M. C., Adolphs, R., Hurley, R. S. E., & Piven, J. (2009) · Psychological Medicine · doi:10.1017/s003329170999078x · Cited by 231 · see citing works
Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy
Fortier, M., Luheshi, G. N., & Boksa, P. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.016 · Cited by 229 · see citing works
The autistic brain: birth through adulthood
Courchesne, E., Redcay, E., & Kennedy, D. P. (2004) · Current Opinion in Neurology · doi:10.1097/01.wco.0000137542.14610.b4 · Cited by 228 · see citing works
Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice
Schwartzer, J. J., Careaga, M., Onore, C. E., Rushakoff, J. A., Berman, R. F., & Ashwood, P. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.16 · Cited by 227 · see citing works
Self-citation
Recent Advances in Autism Research as Reflected in DSM-5 Criteria for Autism Spectrum Disorder
Lord, C., & Bishop, S. L. (2015) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032814-112745 · Cited by 224 · cited 1× · see citing works
“However, manifestation of social challenges varies greatly among individuals with ASD (58), and will require sophisticated behavioral phenotyping tools to evaluate in preclinical models (59).”
Background
Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders
Garay, P. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00136 · Cited by 217 · see citing works
Relative Prenatal and Postnatal Maternal Contributions to Schizophrenia-Related Neurochemical Dysfunction after In Utero Immune Challenge
Meyer, U., Nyffeler, M., Schwendener, S., Knuesel, I., Yee, B. K., & Feldon, J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301413 · Cited by 215 · see citing works
Abnormal microglial–neuronal spatial organization in the dorsolateral prefrontal cortex in autism
Morgan, J. T., Chana, G., Abramson, I., Semendeferi, K., Courchesne, E., & Everall, I. P. (2012) · Brain Research · doi:10.1016/j.brainres.2012.03.036 · Cited by 214 · see citing works
What the Laboratory Rat has Taught us About Social Play Behavior: Role in Behavioral Development and Neural Mechanisms
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Perinatal risk factors and infantile autism
Maimburg, R. D., & Væth, M. (2006) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2006.00805.x · Cited by 192 · see citing works
Minocycline rescues decrease in neurogenesis, increase in microglia cytokines and deficits in sensorimotor gating in an animal model of schizophrenia
Mattei, D., Djodari-Irani, A., Hadar, R., Pelz, A., de Cossío, L. F., Goetz, T., Matyash, M., Kettenmann, H., Winter, C., & Wolf, S. A. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.019 · Cited by 188 · see citing works
Amniotic fluid inflammatory cytokines: Potential markers of immunologic dysfunction in autism spectrum disorders
Abdallah, M. W., Larsen, N., Grove, J., Nørgaard-Pedersen, B., Thorsen, P., Mortensen, E. L., & Hougaard, D. M. (2013) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.639803 · Cited by 186 · see citing works
The Neurobiology of Infantile Autism
Ciaranello, A. L., & Ciaranello, R. D. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.000533 · Cited by 184 · see citing works
Antipurinergic Therapy Corrects the Autism-Like Features in the Poly(IC) Mouse Model
Naviaux, R. K., Zolkipli‐Cunningham, Z., Wang, L., Nakayama, T., Naviaux, J. C., Le, T., Schuchbauer, M. A., Rogač, M., Tang, Q., Dugan, L. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057380 · Cited by 171 · see citing works
Modeling Autistic Features in Animals
Patterson, P. H. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e318212b80f · Cited by 169 · 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
Effects of maternal immune activation on gene expression patterns in the fetal brain
Garbett, K. A., Hsiao, E. Y., Kalman, J. L., Patterson, P. H., & Mirnics, K. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.24 · Cited by 163 · see citing works
VIRAL EXPOSURE AND AUTISM
DEYKIN, E. Y., & MACMAHON, B. (1979) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a112726 · Cited by 161 · see citing works
Neuroethology of primate social behavior
Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301213110 · Cited by 157 · cited 1× · see citing works
“Rhesus monkeys live in large social hierarchies and communicate with a variety of social signals, including vocalizations, facial expressions and body postures (54).”
Background
Prenatal and postnatal animal models of immune activation: Relevance to a range of neurodevelopmental disorders
Harvey, L., & Boksa, P. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22043 · Cited by 149 · see citing works
Maternal Immune Activation during Gestation Interacts withDisc1Point Mutation to Exacerbate Schizophrenia-Related Behaviors in Mice
Lipina, T. V., Zai, C. C. H., Hlousek, D., Roder, J., & Wong, A. H. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0091-13.2013 · Cited by 146 · see citing works
Congenital rubella encephalitis
Desmond, M. M., Wilson, G. S., Melnick, J. L., Singer, D. B., Zion, T. E., Rudolph, A. J., Pineda, R. G., Ziai, M.-H., & Blattner, R. J. (1967) · The Journal of Pediatrics · doi:10.1016/s0022-3476(67)80291-9 · Cited by 145 · see citing works
Animal Models Relevant to Schizophrenia and Autism: Validity and Limitations
Tordjman, S., Drapier, D., Bonnot, O., Graignic-Philippe, R., Fortes, S., Cohen, D., Millet, B., Laurent‐Levinson, C., & Roubertoux, P. L. (2006) · Behavior Genetics · doi:10.1007/s10519-006-9120-5 · Cited by 144 · see citing works
Clozapine Administration in Adolescence Prevents Postpubertal Emergence of Brain Structural Pathology in an Animal Model of Schizophrenia
Piontkewitz, Y., Assaf, Y., & Weiner, I. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.005 · Cited by 143 · see citing works
Risperidone Administered During Asymptomatic Period of Adolescence Prevents the Emergence of Brain Structural Pathology and Behavioral Abnormalities in an Animal Model of Schizophrenia
Piontkewitz, Y., Arad, M., & Weiner, I. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq040 · Cited by 143 · see citing works
Maternal immune activation and autism spectrum disorder: interleukin-6 signaling as a key mechanistic pathway
Parker-Athill, E. C., & Tan, J. (2010) · Neurosignals · doi:10.1159/000319828 · Cited by 140 · see citing works
Maternal immune activation in nonhuman primates alters social attention in juvenile offspring
Machado, C. J., Whitaker, A. M., Smith, S. E. P., Patterson, P. H., & Bauman, M. D. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.035 · Cited by 136 · see citing works
Self-citation
Reversal of autism-like behaviors and metabolism in adult mice with single-dose antipurinergic therapy
Naviaux, J. C., Schuchbauer, M. A., Li, K., Wang, L., Risbrough, V. B., Powell, S. B., & Naviaux, R. K. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.33 · Cited by 134 · see citing works
Assessing behavioural and cognitive domains of autism spectrum disorders in rodents: current status and future perspectives
Kas, M. J., Glennon, J. C., Buitelaar, J., Ey, E., Biemans, B., Crawley, J., Ring, R. H., Lajonchere, C., Esclassan, F., Talpos, J., et al. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3268-5 · Cited by 132 · see citing works
The risk for behavioural deficits is determined by the maternal immune response to prenatal immune challenge in a neurodevelopmental model
Missault, S., Van den Eynde, K., Vanden Berghe, W., Fransen, E., Weeren, A., Timmermans, J. P., Kumar-Singh, S., & Dedeurwaerdere, S. (2014) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.06.013 · Cited by 128 · see citing works
Prenatal Immune Activation Interacts with Genetic<i>Nurr1</i>Deficiency in the Development of Attentional Impairments
Vuillermot, S., Joodmardi, E., Perlmann, T., Ove Ögren, S., Feldon, J., & Meyer, U. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4831-11.2012 · Cited by 127 · see citing works
Effect of pioglitazone treatment on behavioral symptoms in autistic children.
Boris, M., Kaiser, C. C., Goldblatt, A., Elice, M. W., Edelson, S. M., Adams, J. B., & Feinstein, D. L. (2007) · Journal of Neuroinflammation · doi:10.1186/1742-2094-4-3 · Cited by 124 · see citing works
Amniotic fluid chemokines and autism spectrum disorders: An exploratory study utilizing a Danish Historic Birth Cohort
Abdallah, M. W., Larsen, N., Grove, J., Nørgaard‐Pedersen, B., Thorsen, P., Mortensen, E. L., & HOUGAARD, D. M. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.09.003 · Cited by 124 · see citing works
Late prenatal immune activation causes hippocampal deficits in the absence of persistent inflammation across aging
Giovanoli, S., Notter, T., Richetto, J., Labouesse, M. A., Vuillermot, S., Riva, M. A., & Meyer, U. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0437-y · Cited by 124 · see citing works
Gestational immune activation and Tsc2 haploinsufficiency cooperate to disrupt fetal survival and may perturb social behavior in adult mice
Ehninger, D., Sano, Y., de Vries, P. J., Dies, K., Franz, D., Geschwind, D. H., Kaur, M., Lee, Y.-S., Li, W., Lowe, J. K., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2010.115 · Cited by 120 · see citing works
Evaluating Early Preventive Antipsychotic and Antidepressant Drug Treatment in an Infection-Based Neurodevelopmental Mouse Model of Schizophrenia
Meyer, U., Spoerri, E., Yee, B. K., Schwarz, M., & Feldon, J. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn131 · Cited by 115 · see citing works
Tracing the development of psychosis and its prevention: what can be learned from animal models
Piontkewitz, Y., Arad, M., & Weiner, I. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.019 · Cited by 108 · see citing works
Induction of Toll-Like Receptor 3-Mediated Immunity during Gestation Inhibits Cortical Neurogenesis and Causes Behavioral Disturbances
Miranda, J. D., Yaddanapudi, K., Hornig, M., Villar, G., Serge, R., & Lipkin, W. I. (2010) · mBio · doi:10.1128/mbio.00176-10 · Cited by 102 · see citing works
Developing better and more valid animal models of brain disorders.
Stewart, A., & Kalueff, A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.024 · Cited by 101 · see citing works
Maternal immune activation alters behavior in adult offspring, with subtle changes in the cortical transcriptome and epigenome
Connor, C., Dincer, A., Straubhaar, J., Galler, J. R., Houston, I. B., & Akbarian, S. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.06.037 · Cited by 100 · see citing works
TLR3 activation efficiency by high or low molecular mass poly I:C
Zhou, Y., Guo, M. S., Wang, X., et al. (2012) · Innate Immunity · doi:10.1177/1753425912459975 · Cited by 100 · see citing works
Hypolocomotive behaviour associated with increased microglia in a prenatal immune activation model with relevance to schizophrenia
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
Neuroimaging in autism—from basic science to translational research
Ecker, C., & Murphy, D. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2013.276 · Cited by 98 · see citing works
Maternal immune activation promotes hippocampal kindling epileptogenesis in mice
Pineda, E., Shin, D. H., You, S. J., Auvin, S., Sankar, R., & Mazarati, A. M. (2013) · Annals of Neurology · doi:10.1002/ana.23898 · Cited by 98 · see citing works
Brief Report: Autistic Disorder in Three Children with Cytomegalovirus Infection
Sweeten, T. L., Posey, D. J., & McDougle, C. J. (2004) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-004-2552-y · Cited by 97 · see citing works
Stereological Study of Amygdala Glial Populations in Adolescents and Adults with Autism Spectrum Disorder
Morgan, J. T., Barger, N., Amaral, D. G., & Schumann, C. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110356 · Cited by 96 · see citing works
Effects of risperidone treatment in adolescence on hippocampal neurogenesis, parvalbumin expression, and vascularization following prenatal immune activation in rats
Piontkewitz, Y., Bernstein, H., Dobrowolny, H., Bogerts, B., Weiner, I., & Keilhoff, G. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.11.004 · Cited by 93 · see citing works
A stereological comparison of GAD67 and reelin expression in the hippocampal stratum oriens of offspring from two mouse models of maternal inflammation during pregnancy
Harvey, L., & Boksa, P. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.11.022 · Cited by 92 · see citing works
Autism as One of Several Disabilities in Two Children with Congenital Cytomegalovirus Infection
Ivarsson, S. A., Bjerre, I., Vegfors, P., & Ahlfors, K. (1990) · Neuropediatrics · doi:10.1055/s-2008-1071471 · Cited by 90 · see citing works
Of mice and monkeys: using non-human primate models to bridge mouse- and human-based investigations of autism spectrum disorders
Watson, K. K., & Platt, M. L. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-21 · Cited by 90 · see citing works
Minocycline alleviates behavioral deficits and inhibits microglial activation in the offspring of pregnant mice after administration of polyriboinosinic–polyribocytidilic acid
Zhu, F., Zheng, Y., Liu, Y. H., Zhang, X., & Zhao, J. (2014) · Psychiatry Research · doi:10.1016/j.psychres.2014.06.046 · Cited by 87 · see citing works
Adaptations for social cognition in the primate brain
Platt, M. L., Seyfarth, R. M., & Cheney, D. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0096 · Cited by 87 · see citing works
Preliminary evidence of neuropathology in nonhuman primates prenatally exposed to maternal immune activation
Weir, R. K., Forghany, R., Smith, S. E. P., Patterson, P. H., McAllister, A. K., Schumann, C. M., & Bauman, M. D. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.03.009 · Cited by 86 · see citing works
Length of dsRNA (poly I:C) drives distinct innate immune responses, depending on the cell type
Mian, M. F., Ahmed, A. N., Rad, M., Babaian, A., Bowdish, D. M. E., & Ashkar, A. A. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.0312125 · Cited by 85 · see citing works
The interaction between maternal immune activation and alpha 7 nicotinic acetylcholine receptor in regulating behaviors in the offspring
Wu, W., Adams, C. E., Stevens, K. E., Chow, K.-H. K., Freedman, R., & Patterson, P. H. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.005 · Cited by 84 · see citing works
Prenatal versus postnatal maternal factors in the development of infection-induced working memory impairments in mice
Richetto, J., Calabrese, F., Meyer, U., & Riva, M. A. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.07.006 · Cited by 84 · see citing works
Single and combined effects of prenatal immune activation and peripubertal stress on parvalbumin and reelin expression in the hippocampal formation
Giovanoli, S., Weber, L., & Meyer, U. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.04.005 · Cited by 81 · see citing works
Maternal inflammation promotes fetal microglial activation and increased cholinergic expression in the fetal basal forebrain: role of interleukin-6
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
Autism in a child with congenital cytomegalovirus infection
Markowitz, P. I. (1983) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01531564 · Cited by 77 · see citing works
Future Directions for Research in Autism Spectrum Disorders
Damiano, C. R., Mazefsky, C. A., White, S. W., & Dichter, G. S. (2014) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2014.945214 · Cited by 76 · see citing works
Behavioral Phenotyping of Juvenile Long-Evans and Sprague-Dawley Rats: Implications for Preclinical Models of Autism Spectrum Disorders
Ku, K. M., Weir, R. K., Silverman, J. L., Berman, R. F., & Bauman, M. D. (2016) · PLOS ONE · doi:10.1371/journal.pone.0158150 · Cited by 74 · see citing works
Self-citation
Current visual scanpath research: a review of investigations into the psychotic, anxiety, and mood disorders
Toh, W. L., Rossell, S. L., & Castle, D. J. (2011) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2010.12.005 · Cited by 72 · see citing works
Behavioral alterations in rat offspring following maternal immune activation and ELR-CXC chemokine receptor antagonism during pregnancy: Implications for neurodevelopmental psychiatric disorders
Ballendine, S. A., Greba, Q., Dawicki, W., Zhang, X., Gordon, J., & Howland, J. G. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.11.002 · Cited by 71 · see citing works
Increased affective ultrasonic communication during fear learning in adult male rats exposed to maternal immune activation
Yee, N., Schwarting, R. K. W., Fuchs, E., & Wöhr, M. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.05.010 · Cited by 71 · see citing works
Ethological concepts enhance the translational value of animal models
Peters, S. M., Pothuizen, H. H. J., & Spruijt, B. M. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.03.043 · Cited by 70 · see citing works
Maternal mid-pregnancy C-reactive protein and risk of autism spectrum disorders: the early markers for autism study
Zerbo, O., Traglia, M., Yoshida, C., Heuer, L. S., Ashwood, P., Delorenze, G. N., Hansen, R. L., Kharrazi, M., Van de Water, J., Yolken, R. H., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.46 · Cited by 67 · see citing works
Toward a Valid Animal Model of Bipolar Disorder: How the Research Domain Criteria Help Bridge the Clinical-Basic Science Divide
Cosgrove, V. E., Kelsoe, J. R., & Suppes, T. M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.09.002 · Cited by 66 · see citing works
Maternal immune activation evoked by polyinosinic:polycytidylic acid does not evoke microglial cell activation in the embryo
Smolders, S., Smolders, S., Swinnen, N., Gärtner, A., Rigo, J., Legendre, P., & Brône, B. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00301 · Cited by 66 · see citing works
Differential effects of maternal immune activation and juvenile stress on anxiety-like behaviour and physiology in adult rats: No evidence for the “double-hit hypothesis”
Yee, N., Ribic, A., de Roo, C. C., & Fuchs, E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.040 · Cited by 64 · see citing works
Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia
Wolff, A. R., Cheyne, K. R., & Bilkey, D. K. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.033 · Cited by 64 · see citing works
Deficient maternal care resulting from immunological stress during pregnancy is associated with a sex-dependent enhancement of conditioned fear in the offspring
Schwendener, S., Meyer, U., & Feldon, J. (2008) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-008-9000-9 · Cited by 61 · see citing works
Variability in PolyIC induced immune response: Implications for preclinical maternal immune activation models
Careaga, M., Taylor, S. L., Chang, C., Chiang, A., Ku, K. M., Berman, R. F., de Water, J. V., & Bauman, M. D. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.06.014 · Cited by 51 · see citing works
Self-citation
Maternal Anti-Fetal Brain IgG Autoantibodies and Autism Spectrum Disorder: Current Knowledge and its Implications for Potential Therapeutics
Edmiston, E., & de Water, J. V. (2015) · CNS Drugs · doi:10.1007/s40263-015-0279-2 · Cited by 49 · see citing works
Maternal Immune Activation Produces Cerebellar Hyperplasia and Alterations in Motor and Social Behaviors in Male and Female Mice
Aavani, T., Rana, S. A., Hawkes, R. B., & Pittman, Q. J. (2015) · The Cerebellum · doi:10.1007/s12311-015-0669-5 · Cited by 46 · see citing works
Maternal Immune Activation Impairs Reversal Learning and Increases Serum Tumor Necrosis Factor-α in Offspring
Xiao, H., Li, N., Meng, Q., Shao, F., & Wang, W. (2011) · Neuropsychobiology · doi:10.1159/000322455 · Cited by 36 · see citing works
Antipsychotic Interventions in Prodromal Psychosis
Liu, C., & Demjaha, A. (2013) · CNS Drugs · doi:10.1007/s40263-013-0046-1 · Cited by 28 · see citing works
No association between prenatal exposure to influenza and autism
Dassa, D., Takei, N., Sham, P. C., & Murray, R. M. (1995) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1995.tb09558.x · Cited by 23 · see citing works
Poly I‐C Induces Early Embryo Loss in F344 Rats: a Potential Role for NK Cells
Arad, M., Atzil, S., Shakhar, K., Adoni, A., & Ben‐Eliyahu, S. (2005) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2005.00286.x · Cited by 13 · see citing works
Is ‘bench-to-bedside’ realistic for autism? An integrative neuroscience approach
Bauman, M. D., & Schumann, C. M. (2013) · Neuropsychiatry · doi:10.2217/npy.13.18 · Cited by 13 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

Maternal immune activation and neuroinflammation in human neurodevelopmental disorders
Han, V. X., Patel, S., Jones, H. F., & Dale, R. C. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00530-8 · Cited by 683 · see citing works
The contribution of environmental exposure to the etiology of autism spectrum disorder
Bölte, S., Girdler, S., & Marschik, P. B. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2988-4 · Cited by 509 · see citing works
Prenatal developmental origins of future psychopathology: mechanisms and pathways
Monk, C., Lugo-Candelas, C., & Trumpff, C. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095539 · Cited by 388 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Maternal immune activation in neurodevelopmental disorders
Solek, C. M., Farooqi, N., Verly, M., Lim, T. K., & Ruthazer, E. S. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24612 · Cited by 168 · see citing works
Linking inflammation, aberrant glutamate-dopamine interaction, and post-synaptic changes: translational relevance for schizophrenia and antipsychotic treatment: a systematic review
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
The Relationship between Autism and Ehlers-Danlos Syndromes/Hypermobility Spectrum Disorders
Casanova, E. L., Baeza-Velasco, C., Buchanan, C. B., & Casanova, M. F. (2020) · Journal of Personalized Medicine · doi:10.3390/jpm10040260 · Cited by 109 · see citing works
Prenatal environmental risk factors for autism spectrum disorder and their potential mechanisms
Love, C., Sominsky, L., O’Hely, M., Berk, M., Vuillermin, P., & Dawson, S. L. (2024) · BMC Medicine · doi:10.1186/s12916-024-03617-3 · Cited by 110 · see citing works
Alteration of gut microbiota-associated epitopes in children with autism spectrum disorders
Wang, M., Zhou, J., He, F., Cai, C., Wang, H., Wang, Y., Lin, Y., Rong, H., Cheng, G., Xu, R., et al. (2019) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.10.006 · Cited by 77 · see citing works
Prenatal and early-life diesel exhaust exposure causes autism-like behavioral changes in mice
Chang, Y.-C., Cole, T. B., & Costa, L. G. (2018) · Particle and Fibre Toxicology · doi:10.1186/s12989-018-0254-4 · Cited by 65 · see citing works
Circuits for social learning: a unified model and application to autism spectrum disorder
DeMayo, M. M., Young, L. J., Hickie, I. B., Song, Y. J. C., & Guastella, A. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.034 · Cited by 52 · see citing works
Prenatal disruption of blood–brain barrier formation via cyclooxygenase activation leads to lifelong brain inflammation
Zhao, Q., Dai, W., Chen, H. Y., Jacobs, R. E., Zlokovic, B. V., Lund, B. T., Montagne, A., & Bonnin, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2113310119 · Cited by 52 · see citing works
Modulation of Immunological Pathways in Autistic and Neurotypical Lymphoblastoid Cell Lines by the Enteric Microbiome Metabolite Propionic Acid
Frye, R. E., Nankova, B., Bhattacharyya, S., Rose, S., Bennuri, S. C., & MacFabe, D. F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01670 · Cited by 51 · see citing works
Untitled work
Bennett (2023) · doi:10.1097/yco.0000000000000775 · Cited by 51 · see citing works
Maternal prenatal infection and anxiety predict neurodevelopmental outcomes in middle childhood
O'Connor, T. G., Ciesla, A. A., Sefair, A. V., Thornburg, L. L., Brown, A. S., Glover, V., & O'Donnell, K. J. (2022) · Journal of Psychopathology and Clinical Science · doi:10.1037/abn0000746 · Cited by 31 · see citing works

Comorbid Rate of Other Neurodevelopmental Disorder with Autism Spectrum Disorder in a Total Population Sample of 5-Years-Old Children.
Terui, A. (2019) · INSAR 2019 Annual Meeting
De novo and inherited variants in ZNF292 underlie a neurodevelopmental disorder with features of autism spectrum disorder
Mirzaa, G., Chong, J. X., Piton, A., Popp, B., Foss, K., Guo, H., Harripaul, R., Xia, K., Scheck, J., Aldinger, K. A., et al. (2019) · Genetics in Medicine · doi:10.1038/s41436-019-0693-9 · Cited by 49 · see citing works
The link between maternal obesity and offspring neurobehavior: A systematic review of animal experiments
Menting, M. D., van de Beek, C., Mintjens, S., Wever, K. E., Kőrösi, A., Ozanne, S. E., Limpens, J., Roseboom, T. J., Hooijmans, C. R., & Painter, R. C. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.12.023 · Cited by 43 · see citing works
Variants in PRKAR1B cause a neurodevelopmental disorder with autism spectrum disorder, apraxia, and insensitivity to pain
Marbach, F., Stoyanov, G., Erger, F., Stratakis, C. A., Settas, N., London, E., Rosenfeld, J. A., Torti, E. E., Haldeman‐Englert, C. R., Sklirou, E., et al. (2021) · Genetics in Medicine · doi:10.1038/s41436-021-01152-7 · Cited by 28 · see citing works
Behaviorally associated changes in neuroconnectivity following autologous umbilical cord blood infusion in young children with autism spectrum disorder
Frye, R. E. (2019) · Annals of Translational Medicine · doi:10.21037/atm.2019.05.55 · Cited by 2 · see citing works

Authors: Careaga, M., Murai, T., & Bauman, M. D.
Affiliations: University of California, Davis (US)
Sumitomo Dainippon Pharma (Japan) (JP)
Corresponding author: Bauman, Melissa D.
ORCID: Careaga, Milo
Murai, Takeshi
Bauman, Melissa D.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2017-03
Volume: 81
Issue: 5
Pages: 391-401
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2016.10.020
PMC: PMC5513502
OpenAlex: W2534869317
Cited by: 348
References: 147
Citations by year: 2026: 30 · 2025: 29 · 2024: 40 · 2023: 24 · 2022: 58 · 2021: 34 · 2020: 36 · 2019: 48 · 2018: 32 · 2017: 16
FWCI: 3.36
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (P51OD011107)
University of California, Davis (T32MH073124, P50MH106438)
Intellectual and Developmental Disabilities Research Center (U54-HD079125)
National Institute of Mental Health (K18MH105099, T32MH073124, P50MH106438)
National Institute of Child Health and Human Development
Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD079125, R21HD080498)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: maternal immune activation, autism spectrum disorder, prenatal infection, maternal infection, fetal brain development, schizophrenia, neurodevelopmental disorders, animal models, non-human primates, translational research, behavioral phenotyping, reproducibility
MeSH terms: Autism Spectrum Disorder, Animals, Brain, Disease Models, Animal, Female, Humans, Macaca mulatta, Maternal-Fetal Exchange, Poly C, Pregnancy, Pregnancy Complications, Infectious, Prenatal Exposure Delayed Effects, Risk Factors, Mice, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks