Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia
Open accessAbstract
We investigated the role of maternal exposure to human influenza virus (H1N1) in C57BL/6 mice on Day 9 of pregnancy on pyramidal and nonpyramidal cell density, pyramidal nuclear area, and overall brain size in Day 0 neonates and 14-week-old progeny and compared them to sham-infected cohorts. Pyramidal cell density increased significantly (p < 0.0038) by 170% in Day 0 infected mice vs. controls. Nonpyramidal cell density decreased by 33% in Day 0 infected progeny vs. controls albeit, nonsignificantly. Pyramidal cell nuclear size decreased significantly (p < 0.0465) by 29% in exposed newborn mice vs. controls. Fourteen-week-old exposed mice continued to show significant increases in both pyramidal and nonpyramidal cell density values vs. controls respectively (p < 0.0085 E1 (exposed group 1), p < 0.0279 E2 (exposed group 2) pyramidal cell density; p < 0.0092 E1, p < 0.0252 E2, nonpyramidal cell density). By the same token, pyramidal cell nuclear size exhibited 37-43% reductions when compared to control values; these were statistically significant vs. controls (p < 0.04 E1, p < 0.0259 E2). Brain and ventricular area measurements in adult exposed mice also showed significant increases and decreases respectively vs. controls. Ventricular brain ratios exhibited 38-50% decreases in exposed mice vs. controls. While the rate of pyramidal cell proliferation per unit area decreased from birth to adulthood in both control and exposed groups, nonpyramidal cell growth rate increased only in the exposed adult mice. These data show for the first time that prenatal exposure of pregnant mice on Day 9 of pregnancy to a sublethal intranasal administration of influenza virus has both short-term and long-lasting deleterious effects on developing brain structure in the progeny as evident by altered pyramidal and nonpyramidal cell density values; atrophy of pyramidal cells despite normal cell proliferation rate and final enlargement of brain. Moreover, abnormal corticogenesis is associated with development of abnormal behavior in the exposed adult mice.
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Oxytocin receptor density in the nucleus accumbens is significantly correlated with the display of alloparental behavior in both juvenile and adult virgin female prairie voles.
“There is a remarkable amount of individual variation in OTR density in the nucleus accumbens (NAcc) in prairie voles, and OTR density in the NAcc is significantly correlated with the display of alloparental behavior in both juvenile and adult virgin females [43, 44].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [43]
Cites
A simple method of estimating 50 per cent end points
Muench, H. (1938) · Medical Entomology and Zoology · Cited by 8,377 · see citing works
Rajkowska, G., Miguel-Hidalgo, J. J., Wei, J., Dilley, G., Pittman, S. D., Meltzer, H. Y., Overholser, J. C., Roth, B. L., & Stockmeier, C. A. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00041-4 · Cited by 1,477 · see citing works
Guidotti, A., Auta, J., Davis, J. M., Gerevini, V. D. G., Dwivedi, Y., Grayson, D. R., Impagnatiello, F., Pandey, G. N., Pesold, C., Sharma, R. P., et al. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.11.1061 · Cited by 1,203 · 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
Rajkowska, G., Selemon, L. D., & Goldman-Rakic, P. S. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.3.215 · Cited by 537 · see citing works
Fatemi, S. H., Earle, J. A., & McMenomy, T. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000783 · Cited by 447 · see citing works
Self-citationStartle Habituation and Sensorimotor Gating in Schizophrenia and Related Animal Models
Geyer, M. A., & BRAFF, D. L. (1987) · Schizophrenia Bulletin · doi:10.1093/schbul/13.4.643 · Cited by 411 · see citing works
Follow-up report on autism in congenital rubella
Chess, S. (1977) · Journal of Autism and Childhood Schizophrenia · doi:10.1007/bf01531116 · Cited by 378 · see citing works
Fatemi, 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-citationSerum autoantibodies to brain in Landau-Kleffner variant, autism, and other neurologic disorders
Connolly, A. M., Chez, M. G., Pestronk, A., Arnold, S. T., Mehta, S., & Deuel, R. K. (1999) · The Journal of Pediatrics · doi:10.1016/s0022-3476(99)70248-9 · Cited by 236 · see citing works
Circulating autoantibodies to neuronal and glial filament proteins in autism
Singh, V. K., Warren, R., Averett, R., & Ghaziuddin, M. (1997) · Pediatric Neurology · doi:10.1016/s0887-8994(97)00045-3 · Cited by 234 · see citing works
Dysregulation of Reelin and Bcl-2 Proteins in Autistic Cerebellum
Fatemi, S. H., Stary, J. M., Halt, A. R., & Realmuto, G. R. (2001) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1013234708757 · Cited by 212 · see citing works
Self-citationCauses of infantile autism: Some considerations from recent research
Rutter, M. L., & Bartak, L. (1971) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01537740 · Cited by 171 · 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-citationFatemi, S. H. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000129 · Cited by 151 · see citing works
Self-citationCongenital 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
Atlas of the prenatal mouse brain
Schambra, U. B., Lauder, J. M., & Silver, J. (1992) · Cited by 140 · see citing works
Fatemi, S. H., Emamian, E. S., Sidwell, R. W., Kist, D. A., Stary, J. M., Earle, J. A., & THURAS, P. D. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001046 · Cited by 116 · see citing works
Self-citationPrenatal 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-citationAutism and congenital cytomegalovirus
Stubbs, E. G., Ash, E., & Williams, C. P. S. (1984) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02409660 · Cited by 104 · see citing works
The Neurobiology and Genetics of Infantile Autism
Lotspeich, L. J., & Ciaranello, R. D. (1993) · International review of neurobiology · doi:10.1016/s0074-7742(08)60569-3 · Cited by 102 · 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-citationFamily and molecular data for a fine analysis of age at onset in Huntington disease
Squitieri, F., Sabbadini, G., Mandich, P., Gellera, C., Maria, E. D., Bellone, E., Castellotti, B., Nargi, E., de Grazia, U., Frontali, M., et al. (2000) · American Journal of Medical Genetics · doi:10.1002/1096-8628(20001211)95:4 · Cited by 48 · see citing works
Prenatal Exposures in Schizophrenia
Lindenmayer, J. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.5.831-a · Cited by 33 · see citing works
Reduced interneuronal space in schizophrenia
Buxhoeveden, D. P., Roy, E., Switala, A. E., & Casanova, M. F. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00275-9 · Cited by 33 · see citing works
Autistic Subjects with Comorbid Epilepsy: A Possible Association with Viral Infections
Barak, Y., Kimhi, R., Stein, D. J., Gutman, J., & Weizman, A. (1999) · Child Psychiatry & Human Development · doi:10.1023/a:1022669125423 · Cited by 18 · see citing works
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Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder
Dawson, G. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000370 · Cited by 1,138 · 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
Self-citationMaternal 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-citationOxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856 · see citing works
“Functioning of the immune system has become of interest in the context of autism spectrum disorders since these disorders have been associated with a vulnerability to toxins and excessive food allergies [85-88].”
BackgroundWhen 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
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
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
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
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
Courchesne, E., & Pierce, K. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2005.01.003 · Cited by 413 · 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-citationEpidemiology-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
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
Immune signalling in neural development, synaptic plasticity and disease
Boulanger, L. M., & Shatz, C. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1428 · Cited by 334 · 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
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · 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
Brain development in autism: Early overgrowth followed by premature arrest of growth
Courchesne, E. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20020 · Cited by 295 · see citing works
Samuelsson, A., Jennische, E., Hansson, H., & Holmäng, A. B. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00268.2005 · Cited by 283 · 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-citationReelin 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-citationPrenatal 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
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
Immunological Findings in Autism
Cohly, H., & Panja, A. B. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)71013-8 · Cited by 263 · see citing works
Stolp, H. B., & Dzięgielewska, K. M. (2008) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2008.01005.x · Cited by 259 · see citing works
Elovitz, M. A., Brown, A. G., Breen, K. E., Anton, L., Maubert, M. E., & Burd, I. D. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.02.011 · Cited by 254 · see citing works
Fatemi, 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-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
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
Reisinger, S. N., Khan, D., Kong, E., Berger, A., Pollak, A. J., & Pollak, D. D. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.01.001 · Cited by 219 · see citing works
A Short Review on the Current Understanding of Autism Spectrum Disorders
Park, H. R., Lee, J. M., Moon, H. E., Lee, D. S., Kim, B.-N., Kim, J., Kim, D. G., & Paek, S. H. (2016) · Experimental Neurobiology · doi:10.5607/en.2016.25.1.1 · Cited by 214 · see citing works
Osborne, S., Biaggi, A., Chua, T.-E., Preez, A. D., Hazelgrove, K. M., Nikkheslat, N., Previti, G., Zunszain, P. A., Conroy, S., & Pariante, C. M. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.06.017 · Cited by 207 · see citing works
Gumusoglu, S. B., & Stevens, H. E. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.008 · Cited by 207 · see citing works
Gene-Environment Interaction and Covariation in Schizophrenia: The Role of Obstetric Complications
Mittal, V. A., Ellman, L. M., & Cannon, T. D. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn080 · Cited by 203 · see citing works
Large Brains in Autism: The Challenge of Pervasive Abnormality
Herbert, M. R. (2005) · The Neuroscientist · doi:10.1177/0091270005278866 · Cited by 199 · see citing works
Shi, L., Tu, N., & Patterson, P. H. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.005 · Cited by 197 · see citing works
Self-citationLingering prenatal effects of the 1918 influenza pandemic on cardiovascular disease
Bhashkar Mazumder, B., Almond, D. V., Park, K., Crimmins, E. M., & Finch, C. E. (2009) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174409990031 · Cited by 196 · see citing works
Kępińska, A. P., Iyegbe, C. O., Vernon, A. C., Yolken, R., Murray, R. M., & Pollak, T. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00072 · Cited by 193 · see citing works
Prenatal and Perinatal Risk Factors for Autism in China
Zhang, X., Lv, C.-C., Tian, J., Miao, R.-J., Wei, X., Hertz‐Picciotto, I., & Qi, L. (2010) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-0992-0 · Cited by 186 · see citing works
Maternal Effects on Schizophrenia Risk
Patterson, P. H. (2007) · Science · doi:10.1126/science.1150196 · Cited by 175 · see citing works
Self-citationNawa, H., & Takei, N. (2006) · Neuroscience Research · doi:10.1016/j.neures.2006.06.002 · Cited by 174 · 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
Wischhof, L., Irrsack, E., Osorio, C., & Koch, M. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.004 · Cited by 158 · see citing works
Neural basis of psychosis-related behaviour in the infection model of schizophrenia
Meyer, U., & Feldon, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.022 · Cited by 158 · see citing works
Cerebral palsy and fetal inflammatory response syndrome: a review
Bashiri, A., Burstein, E., & Mazor, M. (2006) · Journal of Perinatal Medicine · doi:10.1515/jpm.2006.001 · Cited by 156 · see citing works
The maternal immune system during pregnancy and its influence on fetal development
Morelli, S. S., Mandal, M., Goldsmith, L. T., Kashani, B. N., & Ponzio, N. M. (2015) · Research and Reports in Biology · doi:10.2147/rrb.s80652 · Cited by 155 · see citing works
Viral infection, inflammation and schizophrenia
Kneeland, R. E., & Fatemi, S. H. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.02.001 · Cited by 152 · see citing works
Self-citationAssociation of Maternal Exposure to Childhood Abuse With Elevated Risk for Autism in Offspring
Roberts, A. L., Lyall, K., Rich-Edwards, J. W., Ascherio, A., & Weisskopf, M. G. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.447 · Cited by 152 · see citing works
Fatemi, S. H., Pearce, D. A., Brooks, A. I., & Sidwell, R. W. (2005) · Synapse · doi:10.1002/syn.20162 · Cited by 151 · see citing works
Self-citationHarvey, L., & Boksa, P. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22043 · Cited by 149 · see citing works
Li, Q., Cheung, C., Wei, R., Hui, E. S. K., Feldon, J., Meyer, U., Chung, S. K., Chua, S. E., Sham, P. C., Wu, E. X., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006354 · Cited by 149 · see citing works
Grant, W. B., & Soles, C. M. (2009) · Dermato-Endocrinology · doi:10.4161/derm.1.4.9500 · Cited by 148 · see citing works
Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function
Roumier, A., Pascual, O., Béchade, C., Wakselman, S., Poncer, J.-C., Réal, E., Triller, A., & Bessis, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002595 · Cited by 146 · see citing works
Madore, C., Leyrolle, Q., Lacabanne, C., Benmamar-Badel, A., Joffre, C., Nadjar, A., & Layé, S. (2016) · Neural Plasticity · doi:10.1155/2016/3597209 · Cited by 141 · see citing works
Parker-Athill, E. C., & Tan, J. (2010) · Neurosignals · doi:10.1159/000319828 · Cited by 140 · see citing works
Nyffeler, M., Meyer, U., Yee, B. K., Feldon, J., & Knuesel, I. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.029 · Cited by 139 · see citing works
Carter, C. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn054 · Cited by 137 · see citing works
Jaaro-Peled, H., Ayhan, Y., Pletnikov, M. V., & Sawa, A. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp133 · Cited by 134 · see citing works
Meyer, U., Engler, A., Weber, L., Schedlowski, M., & Feldon, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.031 · Cited by 135 · see citing works
Wei, H., Alberts, I. L., & Li, X. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.025 · Cited by 133 · see citing works
Makinodan, M., Tatsumi, K., Manabe, T., Yamauchi, T., Makinodan, E., Matsuyoshi, H., Shimoda, S., Noriyama, Y., Kishimoto, T., & Wanaka, A. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21673 · Cited by 130 · see citing works
Vojdani, A., Pangborn, J. B., Vojdani, E., & Cooper, E. L. (2003) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200301600302 · Cited by 130 · see citing works
Schepanski, S. N., Buß, C., Hanganu‐Opatz, I. L., & Arck, P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02186 · Cited by 129 · see citing works
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Animal models of obstetric complications in relation to schizophrenia.
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A Review of Autism and the Immune Response
Ashwood, P., & de Water, J. V. (2004) · Journal of Immunology Research · doi:10.1080/10446670410001722096 · Cited by 121 · see citing works
Genetic and Environmental Factors in Complex Neurodevelopmental Disorders
Martens, G. J. M., & van Loo, K. (2007) · Current Genomics · doi:10.2174/138920207783591717 · Cited by 120 · see citing works
Low natural killer cell cytotoxic activity in autism: The role of glutathione, IL-2 and IL-15
Vojdani, A., Mumper, E. A., Granpeesheh, D., Mielke, L., Traver, D., Bock, K., Hirani, K., Neubrander, J. A., Woeller, K. N., O’Hara, N., et al. (2008) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.09.005 · Cited by 121 · see citing works
Moreno, J. L., Kurita, M., Holloway, T. D., López, J., Cadagan, R., Martínez‐Sobrido, L., García‐Sastre, A., & González‐Maeso, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4230-10.2011 · Cited by 120 · see citing works
Baharnoori, M., Brake, W. G., & Srivastava, L. K. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.10.003 · Cited by 113 · see citing works
Inflammation and the developing brain: Consequences for hippocampal neurogenesis and behavior
Green, H. F., & Nolan, Y. M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.004 · Cited by 111 · see citing works
Maternal immune activation leads to activated inflammatory macrophages in offspring
Onore, C. E., Schwartzer, J. J., Careaga, M., Berman, R. F., & Ashwood, P. (2014) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.02.007 · Cited by 106 · see citing works
Calderoni, S., Retico, A., Biagi, L., Tancredi, R., Muratori, F., & Tosetti, M. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.070 · Cited by 106 · see citing works
Le Belle, J. E., Sperry, J., Ngo, A., Ghochani, Y., Laks, D. R., López-Aranda, M., Silva, A. J., & Kornblum, H. I. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.09.004 · Cited by 105 · see citing works
Magnesium sulfate reduces inflammation-associated brain injury in fetal mice
Burd, I. D., Breen, K. E., Friedman, A., Chai, J., & Elovitz, M. A. (2010) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.01.022 · Cited by 101 · see citing works
Evidence for linkage on 21q and 7q in a subset of autism characterized by developmental regression
Molloy, C. A., Keddache, M. A., & Martin, L. J. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001691 · Cited by 98 · see citing works
Sullivan, R. M., Wilson, D. A., Feldon, J., Yee, B. K., Meyer, U., Richter‐Levin, G., Avital, A., Tsoory, M., Gruß, M., Bock, J., et al. (2006) · Developmental Psychobiology · doi:10.1002/dev.20170 · Cited by 98 · see citing works
Lieshout, R. J. V., & Voruganti, L. P. (2008) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0837 · Cited by 100 · see citing works
Winter, C., Reutiman, T. J., Folsom, T. D., Sohr, R., Wolf, R. J., Juckel, G., & Fatemi, S. H. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.06.001 · Cited by 92 · see citing works
Self-citationHarvey, L., & Boksa, P. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.11.022 · Cited by 92 · see citing works
The neuropathology of autism: where do we stand?
Schmitz, C., & Rezaie, P. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00872.x · Cited by 86 · see citing works
Fatemi, S. H., Folsom, T. D., Reutiman, T. J., Abu-Odeh, D., Mori, S., Huang, H., & Oishi, K. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.04.014 · Cited by 86 · see citing works
Self-citationNelson, R. E. (2009) · Health Economics · doi:10.1002/hec.1544 · Cited by 85 · see citing works
Models of Neurodevelopmental Abnormalities in Schizophrenia
Powell, S. B. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_57 · Cited by 84 · see citing works
Targeting sonic hedgehog signaling in neurological disorders
Patel, S. S., Tomar, S., Sharma, D., Mahindroo, N., & Malairaman, U. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.008 · Cited by 83 · see citing works
Mandal, M., Marzouk, A. C., DONNELLY, R. J., & Ponzio, N. M. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.09.011 · Cited by 82 · see citing works
Maternal immune stimulation during pregnancy shapes the immunological phenotype of offspring
Mandal, M., Donnelly, R., Elkabes, S., Zhang, P., Davini, D., David, B. T., & Ponzio, N. M. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2013.04.012 · Cited by 81 · see citing works
Fatemi, S. H., Folsom, T. D., Rooney, R. J., Mori, S., Kornfield, T. E., Reutiman, T. J., Kneeland, R. E., Liesch, S. B., Hua, K., Hsu, J., et al. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.011 · Cited by 81 · see citing works
Self-citationDecreased pyramidal neuron size in Brodmann areas 44 and 45 in patients with autism
Jacot-Descombes, S., Uppal, N., Wicinski, B., Santos, M., Schmeidler, J., Giannakopoulos, P., Heinsein, H., Schmitz, C., & Hof, P. R. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-0976-6 · Cited by 80 · see citing works
Tohmi, M., Tsuda, N., Watanabe, Y., Kakita, A., & Nawa, H. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.05.010 · Cited by 78 · see citing works
Pratt, L., Ni, L., Ponzio, N. M., & Jonakait, G. M. (2013) · Pediatric Research · doi:10.1038/pr.2013.126 · Cited by 77 · see citing works
Infection in the First 2 Years of Life and Autism Spectrum Disorders
Rosen, N. J., Yoshida, C. K., & Croen, L. (2007) · PEDIATRICS · doi:10.1542/peds.2006-1788 · Cited by 77 · see citing works
- Authors
- Fatemi, S. H., Earle, J., Kanodia, R., Kist, D., Emamian, E. S., Patterson, P. H., Shi, L., & Sidwell, R.
- Affiliations
- University of Minnesota (US)
- California Institute of Technology (US)
- Utah State University (US)
- Corresponding author
- Fatemi, S. Hossein
- Venue
- Cellular and Molecular Neurobiology
- Published
- 2002-02
- Volume
- 22
- Issue
- 1
- Pages
- 25-33
- ISSN
- 0272-4340 (ISSN-L)
- 1573-6830
- PMC
- PMC11533729
- OpenAlex
- W1549834980
- Cited by
- 261
- References
- 26
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 6 · 2023: 3 · 2022: 9 · 2021: 6 · 2020: 5 · 2019: 5 · 2018: 10 · 2017: 5 · 2016: 7 · 2015: 19 · 2014: 11 · 2013: 14 · 2012: 15
- FWCI
- 2.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Cellular and Molecular Neurobiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- U.S. Public Health Service (I-A165291)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
- Keywords
- prenatal viral infection, H1N1 influenza, maternal infection, macrocephaly, autism spectrum disorder, schizophrenia, cortical development, brain size, ventriculomegaly, neuronal proliferation, C57BL/6 mice, brain development
- MeSH terms
- Aging, Animals, Atrophy, Autistic Disorder, Brain, Female, Mice, Inbred C57BL, Orthomyxoviridae Infections, Influenza A virus, Pregnancy, Pregnancy Complications, Infectious, Schizophrenia, Pyramidal Cells, Mice
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