Tracing the development of psychosis and its prevention: what can be learned from animal models

Piontkewitz, Yael; Arad, Michal; Weiner, Ina

doi:10.1016/j.neuropharm.2011.04.019

Cited by 108Schizophrenia research and treatmentTryptophan and brain disordersNeurotransmitter Receptor Influence on Behavior

Tracing the development of psychosis and its prevention: what can be learned from animal models

Piontkewitz, Yael, Arad, Michal, Weiner, Ina·2012·Neuropharmacology

DOI 10.1016/j.neuropharm.2011.04.019

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Abstract

Schizophrenia (SCZ) is a neurodevelopmental disorder manifested symptomatically after puberty whose pharmacotherapy remains unsatisfactory. In recent years, longitudinal structural neuroimaging studies have revealed that neuroanatomical aberrations occur in this disorder and in fact precede symptom onset, raising the exciting possibility that SCZ can be prevented. There is some evidence that treatment with atypical antipsychotic drugs (APDs) prior to the development of the full clinical phenotype reduces the risk of transition to psychosis, but results remain controversial. It remains unknown whether progressive structural brain aberrations can be halted. Given the diagnostic, ethical, clinical and methodological problems of pharmacological and imaging studies in patients, getting such information remains a major challenge. Animal neurodevelopmental models of SCZ are invaluable for investigating such questions because they capture the notion that the effects of early brain damage are progressive. In recent years, data derived from such models have converged on key neuropathological and behavioral deficits documented in SCZ attesting to their strong validity, and making them ideal tools for evaluating progression of pathology following in-utero insults as well as its prevention. We review here our recent studies that use longitudinal in vivo structural imaging to achieve this aim in the prenatal immune stimulation model that is based on the association of prenatal infection and increased risk for SCZ. Pregnant rats were injected on gestational day 15 with the viral mimic polyriboinosinic-polyribocytidylic acid (poly I:C) or saline. Male and female offspring were imaged and tested behaviorally on postnatal days (PNDs) 35, 46, 56, 70 and 90. In other experiments, offspring of poly I:C- and saline-treated dams received the atypical antipsychotic drugs (APDs) clozapine or risperidone in two developmental windows: PND 34-47 and PND 48-61, and underwent behavioral testing and imaging at adulthood. Prenatal poly I:C-induced interference with fetal brain development led to aberrant postnatal brain development as manifested in structural abnormalities in the hippocampus, the striatum, the prefrontal cortex and lateral ventricles (LV), as seen in SCZ. The specific trajectories were region-, age- and sex-specific, with females having delayed onset of pathology compared to males. Brain pathology was accompanied by development of behavioral abnormalities phenotypic of SCZ, attentional deficit and hypersensitivity to amphetamine, with same sex difference. Hippocampal volume loss and LV volume expansion as well as behavioral abnormalities were prevented in the offspring of poly I:C mothers who received clozapine or risperidone during the asymptomatic period of adolescence (PND 34-47). Administration at a later window, PNDs 48-61, exerted sex-, region- and drug- specific effects. Our data show that prenatal insult leads to progressive postnatal brain pathology, which gradually gives rise to "symptoms"; that treatment with atypical APDs can prevent both brain and behavioral pathology; and that the earlier the intervention, the more pathological outcomes can be prevented.

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Prenatal poly(I:C) exposure reduced hippocampus volume in adult mice.
“and reduced the volume of the hippocampus in adult mice.”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Piontkewitz et al., 2012
Prenatal poly(I:C) exposure reduced prefrontal cortex volume in adult mice.
“Prenatal exposure to poly(I:C) (Piontkewitz et al., 2012) reduced the volume of the prefrontal cortex”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Piontkewitz et al., 2012

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Evaluating Early Preventive Antipsychotic and Antidepressant Drug Treatment in an Infection-Based Neurodevelopmental Mouse Model of Schizophrenia
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Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia
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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
Immune–neural connections: how the immune system’s response to infectious agents influences behavior
McCusker, R. H., & Kelley, K. W. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.073411 · Cited by 429 · see citing works
Negative symptoms of schizophrenia: Clinical characteristics, pathophysiological substrates, experimental models and prospects for improved treatment
Millan, M. J., Fone, K. C. F., Steckler, T., & Horan, W. P. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.03.008 · Cited by 354 · 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
Neuroinflammation as a risk factor for attention deficit hyperactivity disorder
Dunn, G. A., Nigg, J. T., & Sullivan, E. L. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.05.005 · Cited by 299 · see citing works
Maternal immune activation: reporting guidelines to improve the rigor, reproducibility, and transparency of the model
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
An Overview of Animal Models Related to Schizophrenia
Winship, I. R., Dursun, S. M., Baker, G. B., Balista, P. A., Kandratavicius, L., Maia‐de‐Oliveira, J. P., Hallak, J. E. C., & Howland, J. G. (2018) · The Canadian Journal of Psychiatry · doi:10.1177/0706743718773728 · Cited by 247 · see citing works
The Poly(I:C)-induced maternal immune activation model in preclinical neuropsychiatric drug discovery
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
Minocycline rescues decrease in neurogenesis, increase in microglia cytokines and deficits in sensorimotor gating in an animal model of schizophrenia
Mattei, D., Djodari-Irani, A., Hadar, R., Pelz, A., de Cossío, L. F., Goetz, T., Matyash, M., Kettenmann, H., Winter, C., & Wolf, S. A. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.019 · Cited by 188 · see citing works
Targeting Oxidative Stress and Aberrant Critical Period Plasticity in the Developmental Trajectory to Schizophrenia
Do, K. Q., Cuenod, M., & Hensch, T. K. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv065 · Cited by 158 · 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
Maternal Immune Activation during Gestation Interacts withDisc1Point Mutation to Exacerbate Schizophrenia-Related Behaviors in Mice
Lipina, T. V., Zai, C. C. H., Hlousek, D., Roder, J., & Wong, A. H. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0091-13.2013 · Cited by 146 · see citing works
Prenatal immune activation causes hippocampal synaptic deficits in the absence of overt microglia anomalies
Giovanoli, S., Weber‐Stadlbauer, U., Schedlowski, M., Meyer, U., & Engler, H. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.015 · Cited by 139 · see citing works
Isolated Mitochondria Transfer Improves Neuronal Differentiation of Schizophrenia-Derived Induced Pluripotent Stem Cells and Rescues Deficits in a Rat Model of the Disorder
Robicsek, O., Ene, H. M., Karry, R., Ytzhaki, O., Asor, E., McPhie, D. L., Cohen, B. M., Ben-Yehuda, R., Weiner, I., & Ben‐Shachar, D. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx077 · Cited by 134 · see citing works
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Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy
Howland, J. G., Cazakoff, B. N., & Zhang, Y. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.011 · Cited by 127 · see citing works
Adolescence as a period of vulnerability and intervention in schizophrenia: Insights from the MAM model
Gomes, F. V., Rincón‐Cortés, M., & Grace, A. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.030 · Cited by 128 · see citing works
Maternal immune activation, central nervous system development and behavioral phenotypes
Minakova, E., & Warner, B. B. (2018) · Birth Defects Research · doi:10.1002/bdr2.1416 · Cited by 108 · see citing works
Preliminary evidence of neuropathology in nonhuman primates prenatally exposed to maternal immune activation
Weir, R. K., Forghany, R., Smith, S. E. P., Patterson, P. H., McAllister, A. K., Schumann, C. M., & Bauman, M. D. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.03.009 · Cited by 86 · see citing works
Developmental disruption of perineuronal nets in the medial prefrontal cortex after maternal immune activation
Paylor, J. W., Lins, B. R., Greba, Q., Moen, N., de Moraes, R. S., Howland, J. G., & Winship, I. R. (2016) · Scientific Reports · doi:10.1038/srep37580 · Cited by 79 · see citing works
Alteration of imprinted Dlk1-Dio3 miRNA cluster expression in the entorhinal cortex induced by maternal immune activation and adolescent cannabinoid exposure
Hollins, S. L., Zavitsanou, K., Walker, F. R., & Cairns, M. J. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.99 · Cited by 78 · see citing works
Evolution of structural abnormalities in the rat brain following in utero exposure to maternal immune activation: a longitudinal in vivo MRI study
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
Early or Late Gestational Exposure to Maternal Immune Activation Alters Neurodevelopmental Trajectories in Mice: An Integrated Neuroimaging, Behavioral, and Transcriptional Study
Guma, E., Bordignon, P. D. C., Devenyi, G. A., Gallino, D., Anastassiadis, C., Cvetkovska, V., Barry, A., Snook, E., Germann, J., Greenwood, C. M. T., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.03.017 · Cited by 75 · see citing works
Using a maternal immune stimulation model of schizophrenia to study behavioral and neurobiological alterations over the developmental course
Hadar, R., Soto‐Montenegro, M. L., Götz, T., Wieske, F., Sohr, R., Desco, M., Hamani, C., Weiner, I., Pascau, J., & Winter, C. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.05.010 · Cited by 71 · see citing works
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Behavioral alterations in rat offspring following maternal immune activation and ELR-CXC chemokine receptor antagonism during pregnancy: Implications for neurodevelopmental psychiatric disorders
Ballendine, S. A., Greba, Q., Dawicki, W., Zhang, X., Gordon, J., & Howland, J. G. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.11.002 · Cited by 71 · see citing works
Maternal Immune Activation during Pregnancy Alters Postnatal Brain Growth and Cognitive Development in Nonhuman Primate Offspring
Vlasova, R., Iosif, A., Ryan, A. M., Funk, L. H., Murai, T., Chen, S., Lesh, T. A., Rowland, D. J., Bennett, J., Hogrefe, C. E., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-21.2021 · Cited by 70 · see citing works
Translational opportunities in the prenatal immune environment: Promises and limitations of the maternal immune activation model
Bauman, M. D., & de Water, J. V. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104864 · Cited by 64 · see citing works
Systemic maternal inflammation promotes ASD via IL-6 and IFN-γ
Majerczyk, D., Ayad, E., Brewton, K. L., Saing, P., & Hart, P. C. (2022) · Bioscience Reports · doi:10.1042/bsr20220713 · Cited by 62 · see citing works
Deep brain stimulation improves behavior and modulates neural circuits in a rodent model of schizophrenia
Bikovski, L., Hadar, R., Soto‐Montenegro, M. L., Klein, J., Weiner, I., Desco, M., Pascau, J., Winter, C., & Hamani, C. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.06.012 · Cited by 59 · see citing works
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What Does Immunology Have to Do With Normal Brain Development and the Pathophysiology Underlying Tourette Syndrome and Related Neuropsychiatric Disorders?
Martino, D., Johnson, I. N. S., & Leckman, J. F. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.567407 · Cited by 59 · see citing works
Prospective Analysis of the Effects of Maternal Immune Activation on Rat Cytokines during Pregnancy and Behavior of the Male Offspring Relevant to Schizophrenia
Lins, B. R., Hurtubise, J. L., Roebuck, A. J., Marks, W. N., Zabder, N. K., Scott, G. A., Greba, Q., Dawicki, W., Zhang, X., Rudulier, C. D., et al. (2018) · eNeuro · doi:10.1523/eneuro.0249-18.2018 · Cited by 59 · see citing works
Olanzapine treatment of adolescent rats causes enduring specific memory impairments and alters cortical development and function
Milstein, J. A., Elnabawi, A., Vinish, M., Swanson, T., Enos, J. K., Bailey, A. M., Kolb, B., & Frost, D. O. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057308 · Cited by 57 · see citing works
Attenuated psychosis and the schizophrenia prodrome: current status of risk identification and psychosis prevention
Tandon, N., Shah, J. L., Keshavan, M. S., & Tandon, R. (2012) · Neuropsychiatry · doi:10.2217/npy.12.36 · Cited by 57 · see citing works
Gestational cytokine concentrations and neurocognitive development at 7 years
Ghassabian, A., Albert, P. S., Hornig, M., Yeung, E. H., Cherkerzian, S., Goldstein, R. B., Buka, S. L., Goldstein, J. M., & Gilman, S. E. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0112-z · Cited by 56 · see citing works
Maternal immune activation produces neonatal excitability defects in offspring hippocampal neurons from pregnant rats treated with poly I:C
Patrich, E., Piontkewitz, Y., Peretz, A. S., Weiner, I., & Attali, B. (2016) · Scientific Reports · doi:10.1038/srep19106 · Cited by 54 · see citing works
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Maternal immune activation during pregnancy in rats impairs working memory capacity of the offspring
Murray, B. G., Davies, D. A., Molder, J. J., & Howland, J. G. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.04.005 · Cited by 55 · see citing works
Variability in PolyIC induced immune response: Implications for preclinical maternal immune activation models
Careaga, M., Taylor, S. L., Chang, C., Chiang, A., Ku, K. M., Berman, R. F., de Water, J. V., & Bauman, M. D. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.06.014 · Cited by 51 · see citing works
Effects of early or late prenatal immune activation in mice on behavioral and neuroanatomical abnormalities relevant to schizophrenia in the adulthood
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
Antipsychotic-induced sensitization and tolerance: Behavioral characteristics, developmental impacts, and neurobiological mechanisms
Li, M. (2016) · Journal of Psychopharmacology · doi:10.1177/0269881116654697 · Cited by 51 · see citing works
Deep brain stimulation during early adolescence prevents microglial alterations in a model of maternal immune activation
Hadar, R., Dong, L., Del-Valle-Anton, L., Güneykaya, D., Voget, M., Edemann-Callesen, H., Schweibold, R., Djodari-Irani, A., Goetz, T., Ewing, S. G., et al. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.003 · Cited by 50 · see citing works
Maternal Immune Activation during Pregnancy Alters the Behavior Profile of Female Offspring of Sprague Dawley Rats
Lins, B. R., Marks, W. N., Zabder, N. K., Greba, Q., & Howland, J. G. (2019) · eNeuro · doi:10.1523/eneuro.0437-18.2019 · Cited by 50 · see citing works
Effects of Maternal Psychological Stress During Pregnancy on Offspring Brain Development: Considering the Role of Inflammation and Potential for Preventive Intervention
Graham, A. M., Doyle, O. J., Tilden, E. L., Sullivan, E. L., Gustafsson, H., Marr, M. C., Allen, M. C., & Seghete, K. L. M. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.10.012 · Cited by 54 · see citing works
Age-related changes in neuroinflammation and prepulse inhibition in offspring of rats treated with Poly I:C in early gestation
Ding, S., Hu, Y., Luo, B., Cai, Y., Hao, K., Yang, Y., Zhang, Y., Wang, X., Ding, M., Zhang, H., et al. (2019) · Behavioral and Brain Functions · doi:10.1186/s12993-019-0154-2 · Cited by 47 · see citing works
Effect of maternal immune activation on the kynurenine pathway in preadolescent rat offspring and on MK801-induced hyperlocomotion in adulthood: amelioration by COX-2 inhibition
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
Early neuromodulation prevents the development of brain and behavioral abnormalities in a rodent model of schizophrenia
Hadar, R., Bikovski, L., Soto‐Montenegro, M. L., Schimke, J., Maier, P., Ewing, S. G., Voget, M., Wieske, F., Götz, T., Desco, M., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.52 · Cited by 46 · see citing works
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Prevention of the Phencyclidine-Induced Impairment in Novel Object Recognition in Female Rats by Co-Administration of Lurasidone or Tandospirone, a 5-HT1A Partial Agonist
Horiguchi, M., Hannaway, K. E., Adelekun, A. E., Jayathilake, K., & Meltzer, H. Y. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.64 · Cited by 44 · see citing works
Altered dopamine ontogeny in the developmentally vitamin D deficient rat and its relevance to schizophrenia
Kesby, J., Cui, X.-Y., Burne, T., & Eyles, D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00111 · Cited by 49 · see citing works
Differential effects of early or late exposure to prenatal maternal immune activation on mouse embryonic neurodevelopment
Guma, E., Bordeleau, M., Ibáñez, F. G., Picard, K., Snook, E., Desrosiers-Grégoire, G., Spring, S., Lerch, J. P., Nieman, B. J., Devenyi, G. A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114545119 · Cited by 43 · see citing works
Increased extracellular free-water in adult male rats following in utero exposure to maternal immune activation
Biase, M. A. D., Katabi, G., Piontkewitz, Y., Karayumak, S. C., Weiner, I., & Pasternak, O. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.09.010 · Cited by 41 · see citing works
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Preliminary evidence of increased striatal dopamine in a nonhuman primate model of maternal immune activation
Bauman, M. D., Lesh, T. A., Rowland, D. J., Schumann, C. M., Smucny, J., Kukis, D. L., Cherry, S. R., McAllister, A. K., & Carter, C. S. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0449-y · Cited by 41 · see citing works
Pre-clinical models of neurodevelopmental disorders: focus on the cerebellum
Shevelkin, A. V., Ihenatu, C., & Pletnikov, M. V. (2014) · Reviews in the Neurosciences · doi:10.1515/revneuro-2013-0049 · Cited by 40 · see citing works
Behavioral Animal Models of Antipsychotic Drug Actions
Peleg‐Raibstein, D., Feldon, J., & Meyer, U. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25761-2_14 · Cited by 37 · see citing works
Stress, depression, and hippocampus: from biochemistry to electrophysiology
Idunkova, A., Lacinová, Ľ., & Hoppanová, L. (2023) · General Physiology and Biophysics · doi:10.4149/gpb_2023001 · Cited by 36 · see citing works
Longitudinal in vivo maturational changes of metabolites in the prefrontal cortex of rats exposed to polyinosinic–polycytidylic acid in utero
Vernon, A. C., So, P., Lythgoe, D. J., Chege, W., Cooper, J. D., Williams, S., & Kapur, S. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.09.022 · Cited by 35 · see citing works
Impact of Maternal Immune Activation on Nonhuman Primate Prefrontal Cortex Development: Insights for Schizophrenia
Hanson, K. L., Grant, S. E., Funk, L. H., Schumann, C. M., & Bauman, M. D. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.04.004 · Cited by 30 · see citing works
Animal Models of Schizophrenia
Yanagi, M., Southcott, S. A., Lister, J. M., & Tamminga, C. A. (2011) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394596-9.00012-3 · Cited by 31 · see citing works
Heightened fear in response to a safety cue and extinguished fear cue in a rat model of maternal immune activation
Sangha, S., Greba, Q., Robinson, P., Ballendine, S., & Howland, J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00168 · Cited by 33 · see citing works
Investigating the “two-hit hypothesis”: Effects of prenatal maternal immune activation and adolescent cannabis use on neurodevelopment in mice
Guma, E., Cupo, L., Ma, W., Gallino, D., Moquin, L., Gratton, A. P., Devenyi, G. A., & Chakravarty, M. M. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110642 · Cited by 28 · see citing works
Alteration of transcriptional networks in the entorhinal cortex after maternal immune activation and adolescent cannabinoid exposure
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Authors: Piontkewitz, Y., Arad, M., & Weiner, I.
Affiliations: Tel Aviv University (IL)
Corresponding author: Weiner, Ina
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2012-03
Volume: 62
Issue: 3
Pages: 1273-1289
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2011.04.019
OpenAlex: W1979322945
Cited by: 108
References: 271
Citations by year: 2026: 2 · 2025: 2 · 2023: 5 · 2022: 7 · 2021: 9 · 2020: 8 · 2019: 7 · 2018: 15 · 2017: 7 · 2016: 12 · 2015: 11 · 2014: 9 · 2013: 5 · 2012: 7
FWCI: 0.96
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: United States-Israel Binational Science Foundation (BSF 2007188)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: schizophrenia, neurodevelopmental model, poly(I:C), atypical antipsychotics, clozapine, risperidone, psychosis prevention, hippocampal atrophy, lateral ventricle enlargement, sex differences, attention deficits, prenatal infection, structural neuroimaging, longitudinal brain development, striatum, prefrontal cortex
MeSH terms: Age Factors, Animals, Disease Models, Animal, Female, Hippocampus, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects, Psychotic Disorders, Early Diagnosis, Rats

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Tracing the development of psychosis and its prevention: what can be learned from animal models

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