Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Open accessAbstract
Maternal viral infection is known to increase the risk for schizophrenia and autism in the offspring. Using this observation in an animal model, we find that respiratory infection of pregnant mice (both BALB/c and C57BL/6 strains) with the human influenza virus yields offspring that display highly abnormal behavioral responses as adults. As in schizophrenia and autism, these offspring display deficits in prepulse inhibition (PPI) in the acoustic startle response. Compared with control mice, the infected mice also display striking responses to the acute administration of antipsychotic (clozapine and chlorpromazine) and psychomimetic (ketamine) drugs. Moreover, these mice are deficient in exploratory behavior in both open-field and novel-object tests, and they are deficient in social interaction. At least some of these behavioral changes likely are attributable to the maternal immune response itself. That is, maternal injection of the synthetic double-stranded RNA polyinosinic-polycytidylic acid causes a PPI deficit in the offspring in the absence of virus. Therefore, maternal viral infection has a profound effect on the behavior of adult offspring, probably via an effect of the maternal immune response on the fetus.
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?
Evidence from neuroanatomical, animal, and epidemiologic studies supports prenatal and early postnatal origins of autism.
“evidence from neuroanatomical, animal, and epidemiologic studies support the prenatal and early postnatal origins of autism.19–24”
From Environmental Chemical Exposures and Autism Spectrum Disorders: A Review of the Epidemiological Evidence (2014) · cites this paper as [23]
MIA models have ASD-like social, vocalization, ritualistic, exploration and other behavioral deficits.
“MIA models have ASD-like social, vocalization, ritualistic, exploration and other behavioral deficits [123–125].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [123]
In animal models, an activated maternal immune response alone, without infection, is sufficient to produce changes in the offspring.
“it has now been demonstrated through animal models that merely an activated immune response in the mother, absent any infection, is sufficient to lead to changes in the offspring”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Shi et al, 2003
Shi et al. infected pregnant mice with human influenza virus and observed abnormal behavior, exploration, and social interaction in their offspring.
“Shi et al (2003) infected two strains of pregnant mice with human influenza virus and observed abnormal behavior, exploration, and social interaction in their offspring.”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Shi et al, 2003
In Shi et al., poly(I:C) treatment alone produced similar aberrant phenotypes, suggesting that the maternal immune response rather than the infection caused the effects.
“the authors observed similar aberrant phenotypes in the same mice when using only poly(I:C) treatment rather than infection, suggesting that it was the maternal immune response rather than the infection itself that was responsible”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Shi et al, 2003
The consequences of MIA include behavioral deficits of broad relevance to ASD.
“The consequences of MIA include behavioral deficits of broad relevance to ASD33, 34, 35”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [33]
Early life treatment with Bacteroides fragilis ameliorates deficits in ultrasonic vocalizations and reduces stereotypic burying behavior in maternal immune activation mice.
“Altering the postnatal gut microbiota by early life treatment with the human gut bacterium Bacteroides fragilis sufficiently ameliorated deficits in the frequency and quality of adult ultrasonic vocalizations and reduced stereotypic burying behavior exhibited by the ASD-like mice.”
From Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder (2017) · cites this paper as [31]
In a mouse model of maternal immune activation, mice develop core behavioral features of ASD, neuropathologies, and co-morbid GI and immunological symptoms.
“In a mouse model of maternal immune activation, a principal environmental risk factor for autism, mice develop core behavioral features of ASD (impaired social communication and stereotyped behaviors), as well as several neuropathologies and co-morbid gastrointestinal and immunological symptoms relevant to the human disorder (30–32).”
From Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder (2017) · cites this paper as [31]
Mice and/or non-human primates exposed to maternal immune activation through maternal infection with poly(I:C) or maternal influenza infection have offspring that develop abnormal social behaviors, deficits in immune profiles and anxiety-like phenotypes.
“Similarly, mice and/or non-human primates that are exposed to maternal immune activation (MIA) through maternal infection with the viral mimetic, polyinosinic: polycitidylic acid (poly (I:C)), or maternal influenza infection, have offspring that develop abnormal social behaviors 646566, deficits in their immune profiles and anxiety-like phenotypes 67.”
From Gastrointestinal Issues and Autism Spectrum Disorder (2020) · cites this paper as [66]
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
Koch, M. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00098-7 · Cited by 1,287 · see citing works
Adult Schizophrenia Following Prenatal Exposure to an Influenza Epidemic
Mednick, S. A. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800260109013 · Cited by 1,198 · see citing works
A decrease of reelin expression as a putative vulnerability factor in schizophrenia
Impagnatiello, F., Guidotti, A. R., Pesold, C., Dwivedi, Y., Caruncho, H. J., Pisu, M. G., Uzunov, D. P., Smalheiser, N. R., Davis, J. M., Pandey, G. N., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15718 · Cited by 753 · see citing works
Maturation, Activation, and Protection of Dendritic Cells Induced by Double-stranded RNA
Cella, M., Salio, M., Sakakibara, Y., Langen, H., Julkunen, I., & Lanzavecchia, A. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.5.821 · Cited by 709 · see citing works
Malhotra, A. K. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00036-5 · Cited by 681 · see citing works
Swerdlow, N. R., & Geyer, M. A. (1998) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033326 · Cited by 616 · see citing works
Postmortem brain abnormalities of the glutamate neurotransmitter system in autism
Purcell, A. E., Jeon, O. H., Zimmerman, A. W., Blue, M. E., & Pevsner, J. (2001) · Neurology · doi:10.1212/wnl.57.9.1618 · Cited by 518 · see citing works
Marenco, S., & Weinberger, D. R. (2000) · Development and Psychopathology · doi:10.1017/s0954579400003138 · Cited by 482 · see citing works
Brain anatomy and sensorimotor gating in Asperger's syndrome
McAlonan, G. M. (2002) · Brain · doi:10.1093/brain/awf150 · Cited by 447 · see citing works
Jyonouchi, H., Sun, S., & Le, H. (2001) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(01)00421-0 · Cited by 396 · see citing works
Ellison, G. D. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(94)00014-g · Cited by 304 · see citing works
Brown, A. S., Schaefer, C. A., Wyatt, R. J., Goetz, R. R., Begg, M. D., Gorman, J. M., & Susser, E. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033453 · Cited by 273 · see citing works
Verdijk, R. M., Mutis, T., Esendam, B., Kamp, J., Melief, C. J. M., Brand, A., & Goulmy, E. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.1.57 · Cited by 273 · see citing works
Maternal infection: window on neuroimmune interactions in fetal brain development and mental illness
Patterson, P. H. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00299-4 · Cited by 269 · see citing works
Self-citationFatemi, S. H., Earle, J., Kanodia, R., Kist, D., Emamian, E. S., Patterson, P. H., Shi, L., & Sidwell, R. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1015337611258 · Cited by 261 · see citing works
Self-citationFatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 259 · see citing works
Self-citationTumpey, T. M., Lu, X., Morken, T., Zaki, S. R., & Katz, J. M. (2000) · Journal of Virology · doi:10.1128/jvi.74.13.6105-6116.2000 · Cited by 251 · see citing works
Cytokines in the pathogenesis of influenza
Reeth, K. V. (2000) · Veterinary Microbiology · doi:10.1016/s0378-1135(00)00171-1 · Cited by 233 · see citing works
Irving, W. L., James, D. K., Stephenson, T. J., Laing, P., Jameson, C. L., OXFORD, J. S., Chakraverty, P., Brown, D. W. G., Boon, A. C. M., & Zambon, M. C. F. A. (2000) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2000.tb11621.x · Cited by 232 · see citing works
Review of immunological and immunopathological findings in schizophrenia.
Rothermundt, M., Arolt, V., & Bayer, T. (2001) · Brain, behavior, and immunity · doi:10.1006/brbi.2001.0648 · Cited by 200 · see citing works
Cytokine and growth factor involvement in schizophrenia—support for the developmental model
Nawa, H., Takahashi, M., & Patterson, P. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000730 · Cited by 189 · see citing works
Self-citationThe 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
Association between −G308A tumor necrosis factor alpha gene polymorphism and schizophrenia
Boin, F., Zanardini, R., Pioli, R., Altamura, C. A., Maes, M. H. J., & Gennarelli, M. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000815 · Cited by 179 · see citing works
Grant, K. A., Shively, C. A., Nader, M. A., Ehrenkaufer, R. L., Line, S. W., Morton, T. E., Gage, H. D., & Mach, R. H. (1998) · Synapse · doi:10.1002/(sici)1098-2396(199805)29:1 · Cited by 160 · see citing works
Self-citationThe role of immune function in schizophrenia: an overview
Müller, N., Riedel, M. K. M., Ackenheil, M., & Schwarz, M. (1999) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/pl00014187 · Cited by 158 · see citing works
Schizophrenia and viral infection during neurodevelopment: a focus on mechanisms
Pearce, B. D. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000956 · Cited by 152 · see citing works
Influenza. The Viruses and the Disease.
Tyrrell, D. A. J. (1977) · Annals of Internal Medicine · doi:10.7326/0003-4819-87-4-500_2 · Cited by 148 · see citing works
Seroquel, clozapine and chlorpromazine restore sensorimotor gating in ketamine-treated rats
Swerdlow, N. R., Bakshi, V. P., Waikar, M. V., Taaid, N., & Geyer, M. A. (1998) · Psychopharmacology · doi:10.1007/s002130050741 · Cited by 131 · see citing works
Prenatal viral infection causes alterations in nNOS expression in developing mouse brains
Fatemi, S. H., Cuadra, A. E., El‐Fakahany, E. E., Sidwell, R. W., & THURAS, P. D. (2000) · Neuroreport · doi:10.1097/00001756-200005150-00027 · Cited by 109 · see citing works
Self-citationHornig, M., & Lipkin, W. I. (2001) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.1028 · Cited by 89 · see citing works
Measurement of Anxiety in Transgenic Mice
Weiss, S. Μ., Lightowler, S., Stanhope, K. J., Kennett, G. A., & Dourish, C. T. (2000) · Reviews in the Neurosciences · doi:10.1515/revneuro.2000.11.1.59 · Cited by 55 · see citing works
Cotter, D. (1995) · Schizophrenia Research · doi:10.1016/0920-9964(94)e0082-i · Cited by 49 · see citing works
Fatemi, S. H., Sidwell, R. W., Kist, D. A., Akhter, P., Meltzer, H. Y., Bailey, K. W., THURAS, P. D., & Sedgwick, J. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00450-8 · Cited by 49 · see citing works
Self-citationSchizophrenia: Prenatal Influenza and Autoimmunity
Wright, P., & Murray, R. M. (1993) · Annals of Medicine · doi:10.3109/07853899309147318 · Cited by 43 · see citing works
Familial and genetic mechanisms in schizophrenia
Torrey, E. F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00028-4 · Cited by 41 · see citing works
Gonik, B. (1994) · CPOBGYN. Clinical perspectives in obstetrics and gynecology · doi:10.1007/978-1-4612-2640-6 · Cited by 40 · see citing works
Planning for the next pandemic of influenza
Gust, I. D., Hampson, A. W., & Lavanchy, D. (2001) · Reviews in Medical Virology · doi:10.1002/rmv.301 · Cited by 39 · see citing works
Influenza infections during pregnancy in the mouse
Williams, K., & Mackenzie, J. S. (1977) · Journal of Hygiene · doi:10.1017/s0022172400053067 · Cited by 39 · see citing works
Effect of selenazofurin on influenza A and B virus infections of mice
Sidwell, R. W., Huffman, J. H., Call, E., Alaghamandan, H. A., Cook, P. D., & Robins, R. K. (1986) · Antiviral Research · doi:10.1016/0166-3542(86)90016-1 · Cited by 37 · see citing works
Self-citationFile, S. E. (1985) · PubMed · Cited by 28 · see citing works
The Neurobiology of Infantile Autism
Ciaranello, A. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.18.1.101 · Cited by 11 · see citing works
Influenza: The viruses and the disease, 2nd edn
Sweet, C. (1987) · Microbial Pathogenesis · doi:10.1016/0882-4010(87)90029-5 · Cited by 8 · see citing works
Burger (1998) · doi:10.1002/(sici)1098-2779(1998)4:2
Flagged first, then by citations
Research works printed but not linked: 1
- Shahab SZ, Glezen WP (1994) Influenza virus. In: Viral diseases in preg- nancy (Gonik B, ed), pp 215-223. New York: Springer.
Cited by
Sorted by citations
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
Self-citationBehavioural 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
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
Almond, D. (2006) · Journal of Political Economy · doi:10.1086/507154 · Cited by 1,190 · see citing works
Serologic Evidence of Prenatal Influenza in the Etiology of Schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.8.774 · Cited by 1,048 · see citing works
The unique immunological and microbial aspects of pregnancy
Mor, G., Aldo, P., & Alvero, A. B. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.64 · Cited by 1,041 · 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
Ashwood, P., Krakowiak, P., Hertz-Picciotto, I., Hansen, R., Pessah, I., & Van de Water, J. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.08.003 · Cited by 940 · 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
The Neurodevelopmental Hypothesis of Schizophrenia, Revisited
Fatemi, S. H., & Folsom, T. D. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn187 · Cited by 860 · see citing works
Self-citationMeyer, 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
Animal models of schizophrenia
Jones, C., Watson, D., & Fone, K. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01386.x · Cited by 771 · 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
Self-citationMorgan, 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
The environment and susceptibility to schizophrenia
Brown, A. S. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.09.003 · Cited by 664 · see citing works
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
Self-citationEarly-life programming of later-life brain and behavior: a critical role for the immune system
Bilbo, S. D. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.014.2009 · Cited by 652 · 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
When Is the Brain Enlarged in Autism? A Meta-Analysis of All Brain Size Reports
Redcay, E., & Courchesne, E. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.026 · Cited by 604 · see citing works
Boksa, P. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.03.005 · Cited by 603 · see citing works
Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder
Vuong, H. E., & Hsiao, E. Y. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.024 · Cited by 595 · see citing works
The immune system and developmental programming of brain and behavior
Bilbo, S. D., & Schwarz, J. M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.08.006 · Cited by 579 · see citing works
The “quad‐partite” synapse: Microglia‐synapse interactions in the developing and mature CNS
Schafer, D. P., Lehrman, E. K., & Stevens, B. (2013) · Glia · doi:10.1002/glia.22389 · Cited by 570 · see citing works
Prenatal Infection as a Risk Factor for Schizophrenia
Brown, A. S. (2006) · Schizophrenia Bulletin · doi:10.1093/schbul/sbj052 · Cited by 540 · see citing works
The Role of the Immune System in Autism Spectrum Disorder
Meltzer, A., & Van de Water, J. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.158 · Cited by 533 · see citing works
Realistic expectations of prepulse inhibition in translational models for schizophrenia research
Swerdlow, N. R., Weber, M., Qu, Y., Light, G. A., & Braff, D. L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1072-4 · Cited by 529 · see citing works
The immune response in autism: a new frontier for autism research
Ashwood, P., Wills, S., & Van de Water, J. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.1205707 · Cited by 528 · see citing works
Hagberg, H., Gressèns, P., & Mallard, C. E. (2011) · Annals of Neurology · doi:10.1002/ana.22620 · Cited by 519 · see citing works
Viral Infections During Pregnancy
Silasi, M., Cardenas, I., Kwon, J., Racicot, K. E., Aldo, P. B., & Mor, G. (2015) · American Journal of Reproductive Immunology · doi:10.1111/aji.12355 · Cited by 502 · see citing works
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
Khandaker, G. M., Zimbron, J., Lewis, G., & Jones, P. B. (2012) · Psychological Medicine · doi:10.1017/s0033291712000736 · Cited by 468 · see citing works
Ozawa, K., Hashimoto, K., Kishimoto, T., Shimizu, E., Ishikura, H., & Iyo, M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.031 · Cited by 467 · see citing works
Immunity, neuroglia and neuroinflammation in autism
Pardo, C. A., Vargas, D. L., & Zimmerman, A. W. (2005) · International Review of Psychiatry · doi:10.1080/02646830500381930 · Cited by 460 · see citing works
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
Belmonte, M. K., Cook, E. H., Anderson, G. M., Rubenstein, J. L. R., Greenough, W. T., Beckel-Mitchener, A., Courchesne, E., Boulanger, L. M., Powell, S. B., Levitt, P. R., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001499 · Cited by 442 · see citing works
Maternal lifestyle and environmental risk factors for autism spectrum disorders
Lyall, K., Schmidt, R. J., & Hertz-Picciotto, I. (2014) · International Journal of Epidemiology · doi:10.1093/ije/dyt282 · Cited by 427 · see citing works
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432 · see citing works
The neuropoietic cytokine family in development, plasticity, disease and injury
Bauer, Š., Kerr, B. J., & Patterson, P. H. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2054 · Cited by 412 · see citing works
Self-citationSex Differences in Vulnerability and Resilience to Stress Across the Life Span
Hodes, G. E., & Epperson, C. N. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.028 · Cited by 417 · see citing works
Courchesne, E., & Pierce, K. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2005.01.003 · Cited by 413 · see citing works
Activation of the maternal immune system induces endocrine changes in the placenta via IL-6
Hsiao, E. Y., & Patterson, P. H. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.12.017 · Cited by 402 · see citing works
Self-citationAshdown, H. F., Dumont, Y., Ng, M., Poole, S., Boksa, P., & Luheshi, G. N. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001748 · Cited by 387 · see citing works
Immune transcriptome alterations in the temporal cortex of subjects with autism
Garbett, K., Ebert, P. J., Mitchell, A., Lintas, C., Manzi, B., Mirnics, K., & Persico, A. M. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.01.012 · Cited by 375 · see citing works
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
Self-citationAutism 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
Epidemiology-driven neurodevelopmental animal models of schizophrenia
Meyer, U., & Feldon, J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.018 · Cited by 366 · see citing works
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
Self-citationMaternal 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
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
Maternal immune activation and autism spectrum disorder: From rodents to nonhuman and human primates
Careaga, M., Murai, T., & Bauman, M. D. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.10.020 · Cited by 348 · see citing works
Pandemic Influenza and Pregnant Women
Rasmussen, S. A., Jamieson, D. J., & Bresee, J. (2008) · Emerging infectious diseases · doi:10.3201/eid1401.070667 · Cited by 345 · see citing works
The ASD Living Biology: from cell proliferation to clinical phenotype
Courchesne, E., Pramparo, T., Gazestani, V. H., Lombardo, M. V., Pierce, K., & Lewis, N. E. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0056-y · Cited by 333 · see citing works
Bilbo, S. D., Block, C. L., Bolton, J. L., Hanamsagar, R., & Tran, P. K. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.07.002 · Cited by 323 · see citing works
A Review of the Fetal Brain Cytokine Imbalance Hypothesis of Schizophrenia
Meyer, U., Feldon, J., & Yee, B. K. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn022 · Cited by 318 · see citing works
Cytokine dysregulation in autism spectrum disorders (ASD): Possible role of the environment
Goines, P. E., & Ashwood, P. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.07.006 · Cited by 314 · see citing works
Modeling madness in mice: one piece at a time
Arguello, P. A., & Gogos, J. A. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.023 · Cited by 309 · see citing works
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · Cited by 303 · see citing works
Hippocampal-Prefrontal Interactions in Cognition, Behavior and Psychiatric Disease
Sigurdsson, T., & Duvarci, S. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00190 · Cited by 309 · see citing works
Reversing behavioural abnormalities in mice exposed to maternal inflammation
Shin Yim, Y., Park, A., Berrios, J., Lafourcade, M., Pascual, L. M., Soares, N., Yeon Kim, J., Kim, S., Kim, H., Waisman, A., et al. (2017) · Nature · doi:10.1038/nature23909 · Cited by 303 · see citing works
Developmental neuroinflammation and schizophrenia
Meyer, U. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2011.11.003 · Cited by 300 · see citing works
Fatemi, S. H., Stary, J. M., Earle, J. A., Araghi‐Niknam, M., & Eagan, E. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.02.017 · Cited by 300 · see citing works
Self-citationMaternal 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
Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C. L., Joy, B., Hercher, E., & Brady, D. L. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.030 · Cited by 297 · see citing works
Genes, circuits, and precision therapies for autism and related neurodevelopmental disorders
Sahin, M., & Sur, M. (2015) · Science · doi:10.1126/science.aab3897 · Cited by 295 · see citing works
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-citationPreeclampsia, Placental Insufficiency, and Autism Spectrum Disorder or Developmental Delay
Walker, C. K., Krakowiak, P., Baker, A., Hansen, R. L., Ozonoff, S., & Hertz-Picciotto, I. (2015) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2014.2645 · Cited by 292 · see citing works
The Neuropeptide Tac2 Controls a Distributed Brain State Induced by Chronic Social Isolation Stress
Zelikowsky, M., Hui, M., Karigo, T., Choe, A., Yang, B., Blanco, M. R., Beadle, K., Gradinaru, V., Deverman, B. E., & Anderson, D. J. (2018) · Cell · doi:10.1016/j.cell.2018.03.037 · Cited by 282 · see citing works
Maternal Immune Activation and Neuropsychiatric Illness: A Translational Research Perspective
Brown, A. S., & Meyer, U. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2018.17121311 · Cited by 285 · see citing works
Inflammation and the two-hit hypothesis of schizophrenia
Feigenson, K. A., Kusnecov, A., & Silverstein, S. M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.11.006 · Cited by 280 · 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
Self-citationAltered T cell responses in children with autism
Ashwood, P., Krakowiak, P., Hertz-Picciotto, I., Hansen, R., Pessah, I. N., & Van de Water, J. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.09.002 · Cited by 281 · see citing works
Reelin signaling is impaired in autism
Fatemi, S. H., Snow, A. V., Stary, J. M., Araghi-Niknam, M., Reutiman, T. J., Lee, S., Brooks, A. I., & Pearce, D. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.018 · Cited by 280 · see citing works
Self-citationZerbo, 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
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
Self-citationIL-17a promotes sociability in mouse models of neurodevelopmental disorders
Reed, M. D., Yim, Y. S., Wimmer, R. D., Kim, H., Ryu, C., Welch, G. M., Andina, M., King, H. O., Waisman, A., Halassa, M. M., et al. (2020) · Nature · doi:10.1038/s41586-019-1843-6 · Cited by 274 · see citing works
Prenatal stress: Role in psychotic and depressive diseases
Markham, J. A., & Koenig, J. I. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2035-0 · Cited by 274 · see citing works
Matrisciano, F., Tueting, P., Dalal, I., Kadriu, B., Grayson, D. R., Davis, J. M., Nicoletti, F., & Guidotti, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.04.013 · Cited by 271 · see citing works
Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin
Lee, P. R., Brady, D. L., Shapiro, R. A., Dorsa, D. M., & Koenig, J. I. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.042 · Cited by 270 · see citing works
Kalkbrenner, A. E., Schmidt, R. J., & Penlesky, A. C. (2014) · Current Problems in Pediatric and Adolescent Health Care · doi:10.1016/j.cppeds.2014.06.001 · Cited by 268 · see citing works
Smith, S. E. P., Zhou, Y.-D., Zhang, G., Jin, Z., Stoppel, D. C., & Anderson, M. P. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002627 · Cited by 267 · see citing works
Cannon, T. D., van Erp, T. G. M., Bearden, C. E., Loewy, R. L., Thompson, P. M., Toga, A. W., Huttunnen, M. O., Keshavan, M. S., Seidman, L. J., & Tsuang, M. T. (2003) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a007037 · Cited by 267 · see citing works
Bondy, S. C. (2015) · NeuroToxicology · doi:10.1016/j.neuro.2015.12.002 · Cited by 263 · see citing works
Brain changes in a maternal immune activation model of neurodevelopmental brain disorders
Bergdolt, L., & Dunaevsky, A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.002 · Cited by 266 · see citing works
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
Enstrom, A. M., Lit, L., Onore, C. E., Gregg, J. P., Hansen, R. L., Pessah, I. N., Hertz-Picciotto, I., Van de Water, J. A., Sharp, F. R., & Ashwood, P. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.08.001 · Cited by 257 · see citing works
Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M., & Herkenham, M. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.015 · Cited by 248 · 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
The kynurenine pathway in schizophrenia and bipolar disorder
Erhardt, S., Schwieler, L., Imbeault, S., & Engberg, G. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.05.020 · Cited by 257 · see citing works
Kentner, A. C., Bilbo, S. D., Brown, A. S., Hsiao, E. Y., McAllister, A. K., Meyer, U., Pearce, B. D., Pletnikov, M. V., Yolken, R. H., & Bauman, M. D. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0185-7 · Cited by 245 · see citing works
Hertz‐Picciotto, I., Park, H., Dostal, M., Kocan, A., Trnovec, T., & Sram, R. (2008) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00190.x · Cited by 253 · 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
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
Bilbo, S. D., Biedenkapp, J. C., Der-Avakian, A., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1748-05.2005 · Cited by 251 · see citing works
“Furthermore, an increasing body of evidence from both animal (Hornig et al., 1999; Shi et al., 2003) and human (Rantakallio et al.”
BackgroundFatemi, S. H., Reutiman, T. J., Folsom, T. D., Huang, H., Oishi, K., Mori, S., Smee, D. F., Pearce, D. A., Winter, C., Sohr, R., et al. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2007.11.018 · Cited by 250 · see citing works
Self-citationMeyer, U., & Feldon, J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.009 · Cited by 247 · see citing works
Gilmore, J. H., Jarskog, L. F., Vadlamudi, S., & Lauder, J. M. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300446 · Cited by 246 · see citing works
Reelin glycoprotein: structure, biology and roles in health and disease
Fatemi, S. H. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001613 · Cited by 241 · see citing works
Self-citationWinter, C., Djodari-Irani, A., Sohr, R., Morgenstern, R., Feldon, J., Juckel, G., & Meyer, U. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009206 · Cited by 242 · see citing works
Cytokines as emerging regulators of central nervous system synapses
Zipp, F., Bittner, S., & Schafer, D. P. (2023) · Immunity · doi:10.1016/j.immuni.2023.04.011 · Cited by 239 · see citing works
Models of Fetal Brain Injury, Intrauterine Inflammation, and Preterm Birth
Burd, I. D., Balakrishnan, B., & Kannan, S. (2012) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2012.01110.x · Cited by 238 · see citing works
- Authors
- Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H.
- Affiliations
- California Institute of Technology (US)
- University of Minnesota (US)
- Utah State University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-01-01
- Volume
- 23
- Issue
- 1
- Pages
- 297-302
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742135
- OpenAlex
- W2143217444
- Cited by
- 1,025
- References
- 43
- Citations by year
- 2026: 10 · 2025: 15 · 2024: 34 · 2023: 29 · 2022: 48 · 2021: 45 · 2020: 42 · 2019: 35 · 2018: 47 · 2017: 46 · 2016: 47 · 2015: 59 · 2014: 57 · 2013: 57 · 2012: 66
- FWCI
- 11.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health (n01ai065291-009)
- National Institute of Allergy and Infectious Diseases (N01 AI 65291)
- Topics
- 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
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- maternal influenza infection, prenatal viral infection, offspring behavior, prepulse inhibition, acoustic startle response, clozapine, chlorpromazine, ketamine, exploratory behavior, social interaction deficits, maternal immune response, polyinosinic-polycytidylic acid, schizophrenia, autism spectrum disorder, mouse strain differences
- MeSH terms
- Acoustic Stimulation, Animals, Animals, Newborn, Antiviral Agents, Anxiety, Behavior, Animal, Chlorpromazine, Clozapine, Exploratory Behavior, Female, Immunity, Ketamine, Mice, Inbred BALB C, Mice, Inbred C57BL, Motor Activity, Orthomyxoviridae Infections, Poly I-C, Pregnancy, Social Behavior, Antipsychotic Agents, Maternal-Fetal Relations, Mice
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
