Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice
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Maternal infection during pregnancy increases the risk for neurodevelopmental disorders such as schizophrenia and autism in the offspring. This association appears to be critically dependent on the precise prenatal timing. However, the extent to which distinct adult psychopathological and neuropathological traits may be sensitive to the precise times of prenatal immune activation remains to be further characterized. Here, we evaluated in a mouse model of prenatal immune challenge by the viral mimic, polyriboinosinic-polyribocytidilic acid (PolyIC), whether prenatal immune activation in early/middle and late gestation may influence the susceptibility to some of the critical cognitive, pharmacological, and neuroanatomical dysfunctions implicated in schizophrenia and autism. We revealed that PolyIC-induced prenatal immune challenge on gestation day (GD) 9 but not GD17 significantly impaired sensorimotor gating and reduced prefrontal dopamine D1 receptors in adulthood, whereas prenatal immune activation specifically in late gestation impaired working memory, potentiated the locomotor reaction to the NMDA-receptor antagonist dizocilpine, and reduced hippocampal NMDA-receptor subunit 1 expression. On the other hand, potentiation of the locomotor reaction to the dopamine-receptor agonist amphetamine and reduction in Reelin- and Parvalbumin-expressing prefrontal neurons emerged independently of the precise times of prenatal immune challenge. Our findings thus highlight that prenatal immune challenge during early/middle and late fetal development in mice leads to distinct brain and behavioral pathological symptom clusters in adulthood. Further examination and evaluation of in utero immune challenge at different times of gestation may provide important new insight into the neuroimmunological and neuropathological mechanisms underlying the segregation of different symptom clusters in heterogeneous neuropsychiatric disorders such as schizophrenia and autism.
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Early-life pro-inflammatory conditions, such as maternal and neonatal immune challenges, cause a persistent decrease in the number of prefrontal and/or hippocampal parvalbumin-immunoreactive interneurons.
“Early-life pro-inflammatory conditions, such as maternal and neonatal immune challenges, cause a persistent decrease in number of prefrontal and/or hippocampal parvalbumin-immunoreactive interneurons (Jenkins et al., 2009; Meyer et al., 2008).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Meyer et al., 2008
Inflammation induced at different prenatal periods can lead to distinct adult phenotypes.
“Moreover, inflammation induced at different prenatal periods can lead to distinct adult phenotypes (Meyer et al., 2008).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Meyer et al., 2008
The oxidative stress-induced PVI deficit may also hold for other brain regions like the hippocampus, as shown in some models of schizophrenia (e.g., GCLM KO, ketamine, MAM, poly(I:C), and social defeat).
“Although our analysis focused on oxidative stress-induced PVI deficit in the prefrontal cortex, this deficit may also hold for other brain regions like the hippocampus, as shown in some models of schizophrenia (for example, GCLM KO, ketamine, MAM, poly(I:C) and social defeat.22, 37, 47, 48, 84”
From Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia (2017) · cites this paper as [22]
Cites
Implications of Normal Brain Development for the Pathogenesis of Schizophrenia
Weinberger, D. R. (1987) · Archives of General Psychiatry · doi:10.1001/archpsyc.1987.01800190080012 · Cited by 3,724 · see citing works
Krystal, J. H. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950030035004 · Cited by 3,330 · see citing works
Cortical inhibitory neurons and schizophrenia
Lewis, D. A., Hashimoto, T., & Volk, D. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1648 · Cited by 2,297 · see citing works
The Atlas of Mouse Development
Kaufman, M. H. (1992) · Medical Entomology and Zoology · Cited by 1,749 · see citing works
BRAFF, D. L., Geyer, M. A., & Swerdlow, N. R. (2001) · Psychopharmacology · doi:10.1007/s002130100810 · Cited by 1,701 · see citing works
The atlas of mouse development
Beddington, R. S. P. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90071-o · Cited by 1,431 · see citing works
Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.006 · Cited by 1,329 · see citing works
Laruelle, M., Abi-Dargham, A., van Dyck, C. H., Gil, R., D'Souza, C. D., Erdos, J., McCance, E., Rosenblatt, W., Fingado, C., Zoghbi, S. S., et al. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.17.9235 · Cited by 1,291 · see citing works
Fritschy, J., & Mohler, H. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590111 · Cited by 1,244 · 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
Working memory dysfunction in schizophrenia
(1994) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.6.4.348 · Cited by 1,068 · 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
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
The neurodevelopmental model of schizophrenia: update 2005
Rapoport, J. L., Addington, A. M., Frangou, S., & Psych, M. R. C. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001642 · Cited by 993 · see citing works
Measuring normal and pathological anxiety-like behaviour in mice: a review
Belzung, C., & Griebel, G. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00291-1 · Cited by 912 · see citing works
Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies
D’Esposito, M., Postle, B. R., & Rypma, B. (2000) · Experimental Brain Research · doi:10.1007/s002210000395 · Cited by 796 · see citing works
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
Self-citationIncreased dopamine transmission in schizophrenia: relationship to illness phases.
Laruelle, M., Abi-Dargham, A., Gil, R. B., Kegeles, L., & Innis, R. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00067-0 · Cited by 744 · see citing works
NMDA Receptor Function and Human Cognition: The Effects of Ketamine in Healthy Volunteers
Malhotra, A. K. (1996) · Neuropsychopharmacology · doi:10.1016/0893-133x(95)00137-3 · Cited by 680 · see citing works
Effects of Ketamine in Normal and Schizophrenic Volunteers
Lahti, A. C. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00243-3 · Cited by 674 · see citing works
The pharmacological and anatomical substrates of the amphetamine response in the rat
Creese, I., & Iversen, S. D. (1975) · Brain Research · doi:10.1016/0006-8993(75)90834-3 · Cited by 583 · see citing works
Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., Rozov, A., Whittington, M. A., Traub, R. D., Rawlins, J. N. P., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.031 · Cited by 532 · see citing works
Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi‐Reig, L., Wilson, M. A., & Tonegawa, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00165-x · Cited by 506 · see citing works
Zuckerman, L., Rehavi, M., Nachman, R., & Weiner, I. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300248 · Cited by 501 · 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
Self-citationHashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J. G., Morris, H. M., Volk, D. W., Mirnics, K., & Lewis, D. A. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002011 · Cited by 490 · 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
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
Swerdlow, N. R., BRAFF, D. L., & Geyer, M. A. (2000) · Behavioural Pharmacology · doi:10.1097/00008877-200006000-00002 · Cited by 392 · see citing works
Weiner, I. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1313-x · Cited by 387 · see citing works
Arndt, T. L., Stodgell, C., & Rodier, P. M. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.11.001 · Cited by 369 · see citing works
Fortier, M., Kent, S., Ashdown, H. F., Poole, S., Boksa, P., & Luheshi, G. N. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00293.2004 · Cited by 354 · see citing works
Sensorimotor gating deficits in adults with autism
Perry, W., Minassian, A., Lopez, B., Maron, L., & Lincoln, A. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.09.025 · Cited by 352 · see citing works
Under the curve: Critical issues for elucidating D1 receptor function in working memory
Williams, G. V., & Castner, S. A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.09.028 · Cited by 326 · see citing works
Fritschy, J., Weinmann, O., Wenzel, A., & Benke, D. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980112)390:2 · Cited by 321 · see citing works
Cunningham, C., Campion, S., Teeling, J., Felton, L., & Perry, V. H. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.12.007 · Cited by 318 · see citing works
Meyer, U., Yee, B. K., & Feldon, J. (2007) · The Neuroscientist · doi:10.1177/1073858406296401 · Cited by 303 · see citing works
Self-citationSamuelsson, 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
Acute Effects of Ketamine on Memory Systems and Psychotic Symptoms in Healthy Volunteers
Morgan, C. J. A., Mofeez, A., Brandner, B., Bromley, L. M., & Curran, H. V. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300342 · Cited by 277 · see citing works
Prefrontal DA Transmission at D1 Receptors and the Pathology of Schizophrenia
Abi‐Dargham, A., & Moore, H. M. (2003) · The Neuroscientist · doi:10.1177/1073858403252674 · Cited by 275 · see citing works
Volk, D. W. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.10.1063 · Cited by 264 · see citing works
In utero infection and adult schizophrenia
Brown, A. S., & Susser, E. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10004 · Cited by 261 · 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
Self-citationMeyer, 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
Self-citationDammann, O., Kuban, K., & Leviton, A. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10005 · Cited by 250 · see citing works
Spatial Working Memory Deficits in Autism
Steele, S. D., Minshew, N. J., Luna, B., & Sweeney, J. A. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-006-0202-2 · Cited by 235 · see citing works
Prenatal Exposure to Maternal Genital and Reproductive Infections and Adult Schizophrenia
Babulas, V. P., Factor-Litvak, P. R., Goetz, R. R., Schaefer, C. A., & Brown, A. S. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.5.927 · Cited by 233 · see citing works
Juul-Dam, N., Townsend, J., & Courchesne, E. (2001) · PEDIATRICS · doi:10.1542/peds.107.4.e63 · Cited by 230 · see citing works
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
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
Self-citationSchizophrenia as an inflammation-mediated dysbalance of glutamatergic neurotransmission
Müller, N., & Schwarz, M. (2006) · Neurotoxicity Research · doi:10.1007/bf03033242 · Cited by 214 · see citing works
Niewoehner, B., Single, F. N., Hvalby, Ø., Jensen, V., Borgloh, S. M. Z. A., SEEBURG, P. H., Rawlins, J. N. P., Sprengel, R., & Bannerman, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05312.x · Cited by 209 · see citing works
Prepulse inhibition and latent inhibition: the role of dopamine in the medial prefrontal cortex
Ellenbroek, B. A., Budde, S., & Cools, A. R. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00307-7 · Cited by 197 · see citing works
Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse
Bayer, S. A., Wills, K. V., Triarhou, L., & Ghetti, B. F. (1995) · Experimental Brain Research · doi:10.1007/bf00240955 · Cited by 182 · see citing works
Nawa, H., & Takei, N. (2006) · Neuroscience Research · doi:10.1016/j.neures.2006.06.002 · Cited by 174 · see citing works
Prenosil, G., Gasser, E. M. S., Rudolph, U., Keist, R., Fritschy, J., & Vogt, K. E. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01199.2005 · Cited by 169 · see citing works
Lipina, T. V., Labrie, V., Weiner, I., & Roder, J. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2210-x · Cited by 159 · see citing works
Clinical features of latent inhibition in schizophrenia
Rascle, C., Mazas, O., Vaïva, G., Tournant, M., Raybois, O., Goudemand, M., & Thomas, P. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00162-6 · Cited by 144 · 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
Self-citationMnemonic functions of the hippocampus: A comparison between animals and humans
Kesner, R. P., & Hopkins, R. O. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.004 · Cited by 131 · see citing works
Yan, Q., Reith, M. E. A., Jobe, P. C., & Dailey, J. W. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00568-4 · Cited by 131 · see citing works
French, E. D., Mura, A., & Wang, T. (1993) · Synapse · doi:10.1002/syn.890130203 · Cited by 125 · see citing works
Prazosin inhibits MK-801-induced hyperlocomotion and dopamine release in the nucleus accumbens
Mathé, J. M., Nomikos, G. G., Hildebrand, B. E., Hertel, P., & Svensson, T. H. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00315-9 · Cited by 122 · see citing works
Mathé, J. M., Nomikos, G. G., Blakeman, K. H., & Svensson, T. H. (1999) · Neuropharmacology · doi:10.1016/s0028-3908(98)00163-4 · Cited by 99 · 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
Self-citationDUNCAN, G., MOY, S., LIEBERMAN, J., & KOLLER, B. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.09.017 · Cited by 82 · see citing works
Stability of [123I]IBZM SPECT measurement of amphetamine-induced striatal dopamine release in humans
Kegeles, L. S., Zea‐Ponce, Y., Abi‐Dargham, A., Rodenhiser, J., Wang, T., Weiss, R., Heertum, R. L. V., Mann, J. J., & Laruelle, M. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990315)31:4 · Cited by 80 · see citing works
Duncan, G. E., Moy, S. S., Lieberman, J. A., & Koller, B. H. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0214-1 · Cited by 78 · see citing works
Gaisler‐Salomon, I., & Weiner, I. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1311-z · Cited by 72 · see citing works
Peleg‐Raibstein, D., & Feldon, J. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.002 · Cited by 67 · see citing works
Self-citationPrenosil, G. A. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01199.2006 · Cited by 60 · see citing works
Bast, T., Zhang, W.-N., Heidbreder, C. A., & Feldon, J. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00589-3 · Cited by 58 · see citing works
Self-citationThe relation between latent inhibition and symptom-types in young schizophrenics
Cohen, E., Sereni, N., Kaplan, O., Weizman, A., Kikinzon, L., Weiner, I., & Lubow, R. E. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00221-3 · Cited by 57 · see citing works
Prefrontal D1 and ventral hippocampal N-methyl-d-aspartate regulation of startle gating in rats
Shoemaker, J. M., Marie, R. L. S., Bongiovanni, M. J., Neary, A. C., Tochen, L. S., & Swerdlow, N. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.054 · Cited by 47 · see citing works
Chang, T., Meyer, U., Feldon, J., & Yee, B. K. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0649-z · Cited by 27 · see citing works
Self-citationThe role of medial prefrontal cortical dopamine in spontaneous flexibility in the rat
Lanser, M. G., Ellenbroek, B. A., Zitman, F. G., et al. (2001) · Behavioural Pharmacology · doi:10.1097/00008877-200105000-00002 · Cited by 16 · see citing works
Xiao (1998) · doi:10.1002/(sici)1098-2396(199808)29:4
Flagged first, then by citations
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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
Self-citationThe 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
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
Early-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
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
Common circuit defect of excitatory-inhibitory balance in mouse models of autism
Gogolla, N., LeBlanc, J. J., Quast, K. B., Südhof, T. C., Fagiolini, M., & Hensch, T. K. (2009) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-009-9023-x · Cited by 610 · 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
Self-citationBoksa, P. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.03.005 · Cited by 603 · see citing works
Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice
Krstic, D., Madhusudan, A., Doehner, J., Vogel, P., Notter, T., Imhof, C., Manalastas, A., Hilfiker, M., Pfister, S., Schwerdel, C., et al. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-151 · Cited by 400 · 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
Steullet, P., Cabungcal, J.-H., Coyle, J., Didriksen, M., Gill, K., Grace, A. A., Hensch, T. K., LaMantia, A.-S., Lindemann, L., Maynard, T. M., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.47 · Cited by 360 · see citing works
Self-citationMaternal 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
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
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
Inflammation: A Proposed Intermediary Between Maternal Stress and Offspring Neuropsychiatric Risk
Hantsoo, L., Kornfield, S., Anguera, M. C., & Epperson, C. N. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.018 · Cited by 269 · see citing works
Steullet, P., Cabungcal, J. H., Monin, A., Dwir, D., O'Donnell, P., Cuenod, M., & Do, K. Q. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.021 · Cited by 262 · 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
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Behrens, M. M., Ali, S. S., & Dugan, L. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4457-08.2008 · Cited by 241 · see citing works
Winter, 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
Self-citationBitanihirwe, 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
Canetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., Gordon, J. A., Brown, A., & Kellendonk, C. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.222 · Cited by 201 · see citing works
Garay, P. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00136 · Cited by 217 · see citing works
Steullet, P., Cabungcal, J.-H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T. P., Cuenod, M., & Do, K. Q. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3857-09.2010 · Cited by 202 · see citing works
Sinclair, D., Oranje, B., Razak, K. A., Siegel, S. J., & Schmid, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.029 · Cited by 198 · see citing works
“, 2008), but consistent with VPA models disrupts PPI in the offspring (Howland et al., 2012; Meyer et al., 2008; Vorhees et al., 2015).”
Tye, C., Runicles, A. K., Whitehouse, A. J. O., & Alvares, G. A. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00751 · Cited by 177 · 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
Weber-Stadlbauer, U., Richetto, J., Labouesse, M. A., Bohacek, J., Mansuy, I. M., & Meyer, U. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.41 · Cited by 170 · see citing works
Self-citationPowell, S. B., Sejnowski, T. J., & Behrens, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.049 · Cited by 164 · 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
Self-citationDo, K. Q., Cuenod, M., & Hensch, T. K. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv065 · Cited by 158 · see citing works
Crowley, T., Cryan, J. F., Downer, E. J., & O’Leary, O. F. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.02.001 · Cited by 150 · see citing works
Arrode-Brusés, G., & Brusés, J. L. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-83 · Cited by 146 · see citing works
Richetto, J., Massart, R., Weber-Stadlbauer, U., Szyf, M., Riva, M. A., & Meyer, U. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.010 · Cited by 148 · see citing works
Self-citationParker-Athill, E. C., & Tan, J. (2010) · Neurosignals · doi:10.1159/000319828 · Cited by 140 · see citing works
Early prenatal exposure to LPS results in anxiety- and depression-related behaviors in adulthood
Depino, A. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.065 · Cited by 132 · see citing works
Kirsten, T. B., Chaves‐Kirsten, G. P., Chaible, L. M., Silva, A. C., Martins, D. O., Britto, L. R. G., Dagli, M. L. Z., Torrão, A. S., Palermo‐Neto, J., & Bernardi, M. M. (2012) · Journal of Neuroscience Research · doi:10.1002/jnr.23089 · Cited by 122 · see citing works
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
Self-citationPrenatal maternal immune activation causes epigenetic differences in adolescent mouse brain
Basil, P., Li, Q., Dempster, E. L., Mill, J., Sham, P.-C., Wong, C. C. Y., & McAlonan, G. M. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.80 · Cited by 116 · see citing works
The Autism Birth Cohort: a paradigm for gene–environment–timing research
Stoltenberg, C., Schjølberg, S., Bresnahan, M., Hornig, M., Hirtz, D., Dahl, C., Lie, K. K., Reichborn-Kjennerud, T., Schreuder, P., Alsaker, E., et al. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.143 · Cited by 119 · 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
Yanagi, M., Joho, R. H., Southcott, S. A., Shukla, A. A., Ghose, S., & Tamminga, C. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.49 · Cited by 102 · see citing works
Toward an immune-mediated subtype of autism spectrum disorder
McDougle, C. J., Landino, S. M., Vahabzadeh, A., O’Rourke, J., Zurcher, N. R., Finger, B. C., Palumbo, M. L., Helt, J., Mullett, J. E., Hooker, J. M., et al. (2015) · Brain Research · doi:10.1016/j.brainres.2014.09.048 · Cited by 95 · 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
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
Reelin-mediated signaling in neuropsychiatric and neurodegenerative diseases
Knuesel, I. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.002 · Cited by 89 · see citing works
Self-citationVisceral Inflammation and Immune Activation Stress the Brain
Holzer, P., Farzi, A., Hassan, A. M., Zenz, G., Jačan, A., & Reichmann, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01613 · Cited by 84 · 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
Child neurodevelopmental outcomes following preterm and term birth: what can the placenta tell us?
Hodyl, N. A., Aboustate, N., Bianco-Miotto, T., Roberts, C. T., Clifton, V. L., & Stark, M. J. (2017) · Placenta · doi:10.1016/j.placenta.2017.06.009 · Cited by 76 · see citing works
Crum, W. R., Sawiak, S. J., Chege, W., Cooper, J. D., Williams, S. C. R., & Vernon, A. C. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.008 · Cited by 76 · see citing works
Ratnayake, U., Quinn, T. A., Castillo-Melendez, M., Dickinson, H., & Walker, D. W. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.08.011 · Cited by 75 · see citing works
The major histocompatibility complex and autism spectrum disorder
Needleman, L. A., & McAllister, A. K. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22046 · Cited by 66 · see citing works
Kirsten, T. B., Chaves-Kirsten, G. P., Bernardes, S., Scavone, C., Sarkis, J. E., Bernardi, M. M., & Felicio, L. F. (2015) · PLOS ONE · doi:10.1371/journal.pone.0134565 · Cited by 65 · see citing works
Soumiya, H., Fukumitsu, H., & Furukawa, S. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22704 · Cited by 58 · see citing works
Straley, M. E., Van Oeffelen, W., Theze, S., Sullivan, A. M., O’Mahony, S. M., Cryan, J. F., & O’Keeffe, G. W. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.06.002 · Cited by 52 · see citing works
da Silveira, V. T., de Castro Medeiros, D., Ropke, J., Guidine, P. A., Rezende, G. H., Moraes, M. F. D., Mendes, E. M. A. M., Macedo, D., Moreira, F. A., & de Oliveira, A. C. P. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.01.009 · Cited by 51 · see citing works
Nelson, P. A., Sage, J. R., Wood, S. C., Davenport, C. M., Anagnostaras, S. G., & Boulanger, L. M. (2013) · Learning & Memory · doi:10.1101/lm.031351.113 · Cited by 49 · see citing works
Immunologic and neurodevelopmental susceptibilities of autism
Pessah, I. N., Seegal, R. F., Lein, P. J., LaSalle, J., Yee, B. K., Van De Water, J., & Berman, R. F. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2008.02.006 · Cited by 51 · see citing works
Self-citationWang, X., Pinto-Duarte, A., Sejnowski, T. J., & Behrens, M. M. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4907 · Cited by 46 · see citing works
Zavitsanou, K., Lim, C. K., Purves-Tyson, T., Karl, T., Kassiou, M., Banister, S. D., Guillemin, G. J., & Weickert, C. S. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.05.011 · Cited by 46 · see citing works
Rahman, T., Zavitsanou, K., Purves-Tyson, T., Harms, L. R., Meehan, C., Schall, U., Todd, J., Hodgson, D. M., Michie, P. T., & Weickert, C. S. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00077 · Cited by 39 · see citing works
Maternal Immune Activation Increases Neonatal Mouse Cortex Thickness and Cell Density
Smith, S. E. P., Elliott, R. M., & Anderson, M. P. (2012) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9372-1 · Cited by 34 · see citing works
- Authors
- Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., & Feldon, J.
- Affiliations
- ETH Zurich (CH)
- Corresponding author
- Feldon, Joram
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 22
- Issue
- 4
- Pages
- 469-486
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2022230955
- Cited by
- 457
- References
- 77
- Citations by year
- 2026: 10 · 2025: 7 · 2024: 23 · 2023: 11 · 2022: 20 · 2021: 28 · 2020: 28 · 2019: 20 · 2018: 29 · 2017: 21 · 2016: 30 · 2015: 37 · 2014: 30 · 2013: 32 · 2012: 42
- FWCI
- 6.03
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Branco Weiss Fellowship – Society in Science
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Eidgenössische Technische Hochschule Zürich
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- prenatal immune activation, maternal infection, poly(I:C), schizophrenia, autism spectrum disorder, pregnancy timing, sensorimotor gating, dopamine D1 receptor, prefrontal cortex, working memory, MK-801, NMDA receptor, hippocampus, amphetamine sensitivity, reelin, parvalbumin, neurodevelopmental disorders, neuroimmunology
- MeSH terms
- Reelin Protein, Acoustic Stimulation, Age Factors, Amphetamines, Central Nervous System Stimulants, Animals, Autistic Disorder, Brain, Female, gamma-Aminobutyric Acid, Interferon Inducers, Male, Mice, Inbred C57BL, Nerve Tissue Proteins, Parvalbumins, Poly I-C, Pregnancy, Prenatal Exposure Delayed Effects, Schizophrenia, Serine Endopeptidases, Specific Pathogen-Free Organisms, Reflex, Startle, Cell Adhesion Molecules, Neuronal, Receptors, N-Methyl-D-Aspartate, Dizocilpine Maleate, Extracellular Matrix Proteins, Receptors, Dopamine D1, Excitatory Amino Acid Antagonists, Mice
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