{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T04:48:31Z","timestamp":1793249311045,"version":"4.5.0"},"reference-count":97,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T00:00:00Z","timestamp":1616457600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Czech Science Foundation (GACR)","award":["19-03016S"],"award-info":[{"award-number":["19-03016S"]}]},{"name":"Czech Health Research Council (AZV)","award":["17-30833A"],"award-info":[{"award-number":["17-30833A"]}]},{"name":"Grant agency of the Charles University (GA UK)","award":["172515"],"award-info":[{"award-number":["172515"]}]},{"name":"MH CZ - DRO","award":["National Institute of Mental Health \u2013 NIMH, IN: 00023752"],"award-info":[{"award-number":["National Institute of Mental Health \u2013 NIMH, IN: 00023752"]}]},{"name":"Ministry of Education, Youth and Sports of the Czech Republic","award":["LO1611"],"award-info":[{"award-number":["LO1611"]}]},{"name":"RVO","award":["67985823"],"award-info":[{"award-number":["67985823"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Maternal immune activation (MIA) during pregnancy represents an important environmental factor in the etiology of schizophrenia and autism spectrum disorders (ASD). Our goal was to investigate the impacts of MIA on the brain and behavior of adolescent and adult offspring, as a rat model of these neurodevelopmental disorders. We injected bacterial lipopolysaccharide (LPS, 1 mg\/kg) to pregnant Wistar dams from gestational day 7, every other day, up to delivery. Behavior of the offspring was examined in a comprehensive battery of tasks at postnatal days P45 and P90. Several brain parameters were analyzed at P28. The results showed that prenatal immune activation caused social and communication impairments in the adult offspring of both sexes; males were affected already in adolescence. MIA also caused prepulse inhibition deficit in females and increased the startle reaction in males. Anxiety and hypolocomotion were apparent in LPS-affected males and females. In the 28-day-old LPS offspring, we found enlargement of the brain and decreased numbers of parvalbumin-positive interneurons in the frontal cortex in both sexes. To conclude, our data indicate that sex of the offspring plays a crucial role in the development of the MIA-induced behavioral alterations, whereas changes in the brain apparent in young animals are sex-independent.<\/jats:p>","DOI":"10.3390\/ijms22063274","type":"journal-article","created":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T14:08:16Z","timestamp":1616508496000},"page":"3274","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Behavioral Alterations and Decreased Number of Parvalbumin-Positive Interneurons in Wistar Rats after Maternal Immune Activation by Lipopolysaccharide: Sex Matters"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7029-7936","authenticated-orcid":false,"given":"Iveta","family":"Vojtechova","sequence":"first","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"},{"name":"Laboratory of the Neurophysiology of the Memory, Institute of Physiology of the Czech Academy of Sciences, Videnska 1083, 14220 Prague 4, Czech Republic"},{"name":"First Faculty of Medicine, Charles University, Katerinska 32, 12108 Prague 2, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristyna","family":"Maleninska","sequence":"additional","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"},{"name":"Laboratory of the Neurophysiology of the Memory, Institute of Physiology of the Czech Academy of Sciences, Videnska 1083, 14220 Prague 4, Czech Republic"},{"name":"Faculty of Science, Charles University, Albertov 6, 12800 Prague 2, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Viera","family":"Kutna","sequence":"additional","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ondrej","family":"Klovrza","sequence":"additional","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klara","family":"Tuckova","sequence":"additional","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"},{"name":"Faculty of Science, Charles University, Albertov 6, 12800 Prague 2, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomas","family":"Petrasek","sequence":"additional","affiliation":[{"name":"National Institute of Mental Health, Topolova 748, 25067 Klecany, Czech Republic"},{"name":"Laboratory of the Neurophysiology of the Memory, Institute of Physiology of the Czech Academy of Sciences, Videnska 1083, 14220 Prague 4, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5394-6305","authenticated-orcid":false,"given":"Ales","family":"Stuchlik","sequence":"additional","affiliation":[{"name":"Laboratory of the Neurophysiology of the Memory, Institute of Physiology of the Czech Academy of Sciences, Videnska 1083, 14220 Prague 4, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,3,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1272","DOI":"10.1002\/dneu.22024","article-title":"Epidemiologic Studies of Exposure to Prenatal Infection and Risk of Schizophrenia and Autism","volume":"72","author":"Brown","year":"2012","journal-title":"Dev. Neurobiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1006\/brbi.2001.0644","article-title":"Maternal Cytokine Levels during Pregnancy and Adult Psychosis","volume":"15","author":"Buka","year":"2001","journal-title":"Brain. Behav. Immun."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fnins.2014.00019","article-title":"The Impact of Environmental Factors in Severe Psychiatric Disorders","volume":"8","author":"Schmitt","year":"2014","journal-title":"Front. Neurosci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/s10519-006-9120-5","article-title":"Animal Models Relevant to Schizophrenia and Autism: Validity and Limitations","volume":"37","author":"Tordjman","year":"2007","journal-title":"Behav. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1046\/j.0021-9630.2003.00317.x","article-title":"Autism and Pervasive Developmental Disorders","volume":"45","author":"Volkmar","year":"2004","journal-title":"J. Child Psychol. Psychiatry"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders (DSM-5\u00ae\u00ae), American Psychiatric Association. [5th ed.].","DOI":"10.1176\/appi.books.9780890425596"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/S0140-6736(15)01121-6","article-title":"Schizophrenia","volume":"388","author":"Owen","year":"2016","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kodish, I., and McClellan, J.M. (2016). Early onset schizophrenia. Dulcan\u2019s Textbook of Child and Adolescent Psychiatry, American Psychiatric Publishing, Inc.. [2nd ed.].","DOI":"10.1176\/appi.books.9781615370306.md18"},{"key":"ref_9","first-page":"131","article-title":"Schizophrenic Autism: Clinical Phenomenology and Pathogenetic Implications","volume":"1","author":"Parnas","year":"2002","journal-title":"World Psychiatry"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1192\/apt.bp.115.014720","article-title":"Autism Spectrum Disorder and Schizophrenia: Boundaries and Uncertainties","volume":"22","author":"Parellada","year":"2016","journal-title":"BJPsych Adv."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.biopsych.2010.03.036","article-title":"Cortical Thickness and Subcortical Volumes in Schizophrenia and Bipolar Disorder","volume":"68","author":"Rimol","year":"2010","journal-title":"Biol. Psychiatry"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.tins.2007.12.005","article-title":"Neuroanatomy of Autism","volume":"31","author":"Amaral","year":"2008","journal-title":"Trends Neurosci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1001\/jama.290.3.337","article-title":"Evidence of Brain Overgrowth in the First Year of Life in Autism","volume":"290","author":"Courchesne","year":"2003","journal-title":"JAMA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1093\/cercor\/bhj069","article-title":"Anatomical Differences in the Mirror Neuron System and Social Cognition Network in Autism","volume":"16","author":"Hadjikhani","year":"2006","journal-title":"Cereb. Cortex"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1176\/ajp.2006.163.7.1290","article-title":"An MRI Study of Increased Cortical Thickness in Autism","volume":"163","author":"Hardan","year":"2006","journal-title":"Am. J. Psychiatry"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"6392","DOI":"10.1523\/JNEUROSCI.1297-04.2004","article-title":"The Amygdala Is Enlarged in Children but Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages","volume":"24","author":"Schumann","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/j.biopsych.2015.03.010","article-title":"Alterations in Cortical Network Oscillations and Parvalbumin Neurons in Schizophrenia","volume":"77","author":"Cho","year":"2015","journal-title":"Biol. Psychiatry"},{"key":"ref_18","first-page":"1931","article-title":"The Number of Parvalbumin-Expressing Interneurons Is Decreased in the Prefrontal Cortex in Autism","volume":"27","author":"Hashemi","year":"2017","journal-title":"Cereb. Cortex"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1111\/j.1600-0404.2009.01234.x","article-title":"Parvalbumin-, Calbindin-, and Calretinin-Immunoreactive Hippocampal Interneuron Density in Autism","volume":"121","author":"Lawrence","year":"2010","journal-title":"Acta Neurol. Scand."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/mp.2016.147","article-title":"Myelination of Parvalbumin Interneurons: A Parsimonious Locus of Pathophysiological Convergence in Schizophrenia","volume":"22","author":"Stedehouder","year":"2017","journal-title":"Mol. Psychiatry"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e13282","DOI":"10.1111\/apha.13282","article-title":"Neural and Neuronal Discoordination in Schizophrenia: From Ensembles through Networks to Symptoms","volume":"226","author":"Krajcovic","year":"2019","journal-title":"Acta Physiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Nakamura, T., Matsumoto, J., Takamura, Y., Ishii, Y., Sasahara, M., Ono, T., and Nishijo, H. (2015). Relationships among Parvalbumin-Immunoreactive Neuron Density, Phase-Locked Gamma Oscillations, and Autistic\/Schizophrenic Symptoms in PDGFR-\u03b2 Knock-out and Control Mice. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0119258"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"14948","DOI":"10.1523\/JNEUROSCI.2204-14.2014","article-title":"Parvalbumin and GAD65 Interneuron Inhibition in the Ventral Hippocampus Induces Distinct Behavioral Deficits Relevant to Schizophrenia","volume":"34","author":"Nguyen","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/s13229-016-0079-7","article-title":"Brinp1 \u2212\/\u2212 Mice Exhibit Autism-like Behaviour, Altered Memory, Hyperactivity and Increased Parvalbumin-Positive Cortical Interneuron Density","volume":"7","author":"Berkowicz","year":"2016","journal-title":"Mol. Autism"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1002\/aur.1264","article-title":"Knockout of NMDA Receptors in Parvalbumin Interneurons Recreates Autism-like Phenotypes","volume":"6","author":"Saunders","year":"2013","journal-title":"Autism Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e525","DOI":"10.1038\/tp.2015.19","article-title":"Lack of Parvalbumin in Mice Leads to Behavioral Deficits Relevant to All Human Autism Core Symptoms and Related Neural Morphofunctional Abnormalities","volume":"5","author":"Orduz","year":"2015","journal-title":"Transl. Psychiatry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1093\/schbul\/sbq098","article-title":"Neonatal Behavioral Changes in Rats with Gestational Exposure to Lipopolysaccharide: A Prenatal Infection Model for Developmental Neuropsychiatric Disorders","volume":"38","author":"Baharnoori","year":"2012","journal-title":"Schizophr. Bull."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.pbb.2010.12.026","article-title":"Prenatal Lipopolysaccharide Treatment Enhances MK-801-Induced Psychotomimetic Effects in Rats","volume":"98","author":"Budziszewska","year":"2011","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.schres.2007.11.018","article-title":"Maternal Infection Leads to Abnormal Gene Regulation and Brain Atrophy in Mouse Offspring: Implications for Genesis of Neurodevelopmental Disorders","volume":"99","author":"Fatemi","year":"2008","journal-title":"Schizophr. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.biopsych.2013.07.011","article-title":"Prenatal Poly(I:C) Exposure and Other Developmental Immune Activation Models in Rodent Systems","volume":"75","author":"Meyer","year":"2014","journal-title":"Biol. Psychiatry"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/j.bbi.2020.10.012","article-title":"Maternal Immune Activation Targeted to a Window of Parvalbumin Interneuron Development Improves Spatial Working Memory: Implications for Autism","volume":"91","author":"Nakamura","year":"2021","journal-title":"Brain. Behav. Immun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.molmed.2011.03.001","article-title":"Maternal Infection and Immune Involvement in Autism","volume":"17","author":"Patterson","year":"2011","journal-title":"Trends Mol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.bbr.2015.11.025","article-title":"Lipopolysaccharide Exposure during Late Embryogenesis Results in Diminished Locomotor Activity and Amphetamine Response in Females and Spatial Cognition Impairment in Males in Adult, but Not Adolescent Rat Offspring","volume":"299","year":"2016","journal-title":"Behav. Brain Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.bbi.2008.09.002","article-title":"Peripheral Lipopolysaccharide (LPS) Challenge Promotes Microglial Hyperactivity in Aged Mice That Is Associated with Exaggerated Induction of Both pro-Inflammatory IL-1\u03b2 and Anti-Inflammatory IL-10 Cytokines","volume":"23","author":"Henry","year":"2009","journal-title":"Brain Behav. Immun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/j.physbeh.2014.10.016","article-title":"Inverse Effects of Lipopolysaccharides on Anxiety in Pregnant Mice and Their Offspring","volume":"139","author":"Solati","year":"2015","journal-title":"Physiol. Behav."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1128\/CMR.16.3.379-414.2003","article-title":"Receptors, Mediators, and Mechanisms Involved in Bacterial Sepsis and Septic Shock","volume":"16","author":"Kuiper","year":"2003","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1203\/00006450-200001000-00013","article-title":"Cytokine Induction in Fetal Rat Brains and Brain Injury in Neonatal Rats after Maternal Lipopolysaccharide Administration","volume":"47","author":"Cai","year":"2000","journal-title":"Pediatr. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1038\/mp.2008.44","article-title":"Ontogeny of Sensorimotor Gating and Immune Impairment Induced by Prenatal Immune Challenge in Rats: Implications for the Etiopathology of Schizophrenia","volume":"15","author":"Romero","year":"2010","journal-title":"Mol. Psychiatry"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/j.bbi.2010.03.005","article-title":"Effects of Prenatal Infection on Brain Development and Behavior: A Review of Findings from Animal Models","volume":"24","author":"Boksa","year":"2010","journal-title":"Brain Behav. Immun."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"McPartland, J.C., Law, K., and Dawson, G. (2016). Autism Spectrum Disorder. Encyclopedia of Mental Health, Elsevier.","DOI":"10.1016\/B978-0-12-397045-9.00230-5"},{"key":"ref_41","first-page":"1","article-title":"Gender Differences in Schizophrenia and First-Episode Psychosis: A Comprehensive Literature Review","volume":"2012","author":"Ochoa","year":"2012","journal-title":"Schizophr. Res. Treat."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1097\/WCO.0b013e32835ee548","article-title":"Sex Differences in Autism Spectrum Disorders","volume":"26","author":"Werling","year":"2013","journal-title":"Curr. Opin. Neurol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.neuropharm.2018.11.023","article-title":"Evaluation of Ultrasonic Vocalizations in a Neurodevelopmental Model of Schizophrenia during the Early Life Stages of Rats","volume":"146","author":"Potasiewicz","year":"2019","journal-title":"Neuropharmacology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.neuroscience.2014.12.013","article-title":"Prenatal Administration of Lipopolysaccharide Induces Sex-Dependent Changes in Glutamic Acid Decarboxylase and Parvalbumin in the Adult Rat Brain","volume":"287","author":"Trojan","year":"2015","journal-title":"Neuroscience"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.pnpbp.2014.10.004","article-title":"Prenatal LPS-Exposure\u2014A Neurodevelopmental Rat Model of Schizophrenia\u2014Differentially Affects Cognitive Functions, Myelination and Parvalbumin Expression in Male and Female Offspring","volume":"57","author":"Wischhof","year":"2015","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1176\/appi.ajp.2015.14081031","article-title":"In Vivo Measurement of GABA Transmission in Healthy Subjects and Schizophrenia Patients","volume":"172","author":"Frankle","year":"2015","journal-title":"Am. J. Psychiatry"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1176\/appi.ajp.2011.11010052","article-title":"Cortical Deficits of Glutamic Acid Decarboxylase 67 Expression in Schizophrenia: Clinical, Protein, and Cell Type-Specific Features","volume":"168","author":"Curley","year":"2011","journal-title":"Am. J. Psychiatry"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/mp.2013.152","article-title":"Altered Parvalbumin Basket Cell Inputs in the Dorsolateral Prefrontal Cortex of Schizophrenia Subjects","volume":"19","author":"Glausier","year":"2014","journal-title":"Mol. Psychiatry"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.schres.2011.06.007","article-title":"Hippocampal Interneurons are Abnormal in Schizophrenia","volume":"131","author":"Konradi","year":"2011","journal-title":"Schizophr. Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/s11920-010-0124-8","article-title":"Alterations of Cortical GABA Neurons and Network Oscillations in Schizophrenia","volume":"12","author":"Hashimoto","year":"2010","journal-title":"Curr. Psychiatry Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.tins.2011.10.004","article-title":"Cortical Parvalbumin Interneurons and Cognitive Dysfunction in Schizophrenia","volume":"35","author":"Lewis","year":"2012","journal-title":"Trends Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1159\/000290040","article-title":"Prenatal Lipopolysaccharide Reduces Social Behavior in Male Offspring","volume":"17","author":"Kirsten","year":"2010","journal-title":"Neuroimmunomodulation"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"11706","DOI":"10.1523\/JNEUROSCI.0730-12.2012","article-title":"Lipopolysaccharide-Induced Microglial Activation and Neuroprotection against Experimental Brain Injury Is Independent of Hematogenous TLR4","volume":"32","author":"Chen","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e0164403","DOI":"10.1371\/journal.pone.0164403","article-title":"Early Postnatal Lipopolysaccharide Exposure Leads to Enhanced Neurogenesis and Impaired Communicative Functions in Rats","volume":"11","author":"Pang","year":"2016","journal-title":"PLoS ONE"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1212\/WNL.57.2.245","article-title":"Unusual Brain Growth Patterns in Early Life in Patients with Autistic Disorder: An MRI Study","volume":"57","author":"Courchesne","year":"2001","journal-title":"Neurology"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.biopsych.2006.07.016","article-title":"Rate of Head Growth Decelerates and Symptoms Worsen in the Second Year of Life in Autism","volume":"61","author":"Dawson","year":"2007","journal-title":"Biol. Psychiatry"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.pediatrneurol.2004.08.005","article-title":"Accelerated Head Growth in Early Development of Individuals with Autism","volume":"32","author":"Dementieva","year":"2005","journal-title":"Pediatr. Neurol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.bbr.2006.01.009","article-title":"Volumetric Structural Brain Abnormalities in Men with Schizophrenia or Antisocial Personality Disorder","volume":"169","author":"Barkataki","year":"2006","journal-title":"Behav. Brain Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.ijdevneu.2014.04.001","article-title":"Sexually Dimorphic Effects of Prenatal Exposure to Propionic Acid and Lipopolysaccharide on Social Behavior in Neonatal, Adolescent, and Adult Rats: Implications for Autism Spectrum Disorders","volume":"39","author":"Foley","year":"2014","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.bbr.2018.05.001","article-title":"Neonatal Immune Activation by Lipopolysaccharide Causes Inadequate Emotional Responses to Novel Situations but No Changes in Anxiety or Cognitive Behavior in Wistar Rats","volume":"349","author":"Vojtechova","year":"2018","journal-title":"Behav. Brain Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1093\/oxfordjournals.schbul.a006889","article-title":"Speech Disorder in Schizophrenia: Review of the Literature and Exploration of Its Relation to the Uniquely Human Capacity for Language","volume":"27","author":"DeLisi","year":"2001","journal-title":"Schizophr. Bull."},{"key":"ref_62","unstructured":"McKenna, P.J., Oh, T.M., and Oh, T. (2005). Schizophrenic Speech: Making Sense of Bathroots and Ponds That Fall in Doorways, Cambridge University Press."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/0091-3057(95)02126-4","article-title":"A Review of the Validity and Variability of the Elevated Plus-Maze as an Animal Model of Anxiety","volume":"54","author":"Hogg","year":"1996","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.tips.2008.07.005","article-title":"Animal Models of Anxiety: Do I Need Multiple Tests?","volume":"29","author":"Ramos","year":"2008","journal-title":"Trends Pharmacol. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.neuroscience.2015.04.065","article-title":"Early Prenatal Exposure to LPS Results in Anxiety- and Depression-Related Behaviors in Adulthood","volume":"299","author":"Depino","year":"2015","journal-title":"Neuroscience"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1016\/j.bbi.2011.12.003","article-title":"Prenatal Lipopolysaccharide Exposure Increases Anxiety-like Behaviors and Enhances Stress-Induced Corticosterone Responses in Adult Rats","volume":"26","author":"Lin","year":"2012","journal-title":"Brain Behav. Immun."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Foley, K.A., Ossenkopp, K.-P., Kavaliers, M., and MacFabe, D.F. (2014). Pre- and Neonatal Exposure to Lipopolysaccharide or the Enteric Metabolite, Propionic Acid, Alters Development and Behavior in Adolescent Rats in a Sexually Dimorphic Manner. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0087072"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1111\/j.1600-0447.2007.01067.x","article-title":"Anxiety Symptoms in Schizophrenia Spectrum Disorders: Associations with Social Function, Positive and Negative Symptoms, Hope and Trauma History","volume":"116","author":"Lysaker","year":"2007","journal-title":"Acta Psychiatr. Scand."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.cpr.2009.01.003","article-title":"Anxiety in Children and Adolescents with Autism Spectrum Disorders","volume":"29","author":"White","year":"2009","journal-title":"Clin. Psychol. Rev."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1016\/j.neubiorev.2008.03.012","article-title":"Models of Schizophrenia in Humans and Animals Based on Inhibition of NMDA Receptors","volume":"32","author":"Horacek","year":"2008","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/s11011-011-9234-1","article-title":"Behavioral Changes and Mitochondrial Dysfunction in a Rat Model of Schizophrenia Induced by Ketamine","volume":"26","author":"Fraga","year":"2011","journal-title":"Metab. Brain Dis."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"94","DOI":"10.9758\/cpn.2012.10.2.94","article-title":"Effects of the Antioxidant Sulforaphane on Hyperlocomotion and Prepulse Inhibition Deficits in Mice after Phencyclidine Administration","volume":"10","author":"Shirai","year":"2012","journal-title":"Clin. Psychopharmacol. Neurosci."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.ejphar.2008.11.036","article-title":"Repeated Antipsychotic Treatment Progressively Potentiates Inhibition on Phencyclidine-Induced Hyperlocomotion, but Attenuates Inhibition on Amphetamine-Induced Hyperlocomotion: Relevance to Animal Models of Antipsychotic Drugs","volume":"602","author":"Sun","year":"2009","journal-title":"Eur. J. Pharmacol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.bbr.2016.03.020","article-title":"Dizocilpine (MK-801) Impairs Learning in the Active Place Avoidance Task but Has No Effect on the Performance during Task\/Context Alternation","volume":"305","author":"Vojtechova","year":"2016","journal-title":"Behav. Brain Res."},{"key":"ref_75","first-page":"12","article-title":"Effect of perinatal inflammatory reaction on the induction of psychotic-like behaviour: Experimental study","volume":"11","author":"Tejkalova","year":"2007","journal-title":"Psychiatrie"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1016\/j.ijdevneu.2013.10.003","article-title":"Inflammatory Response and Oxidative Stress in Developing Rat Brain and Its Consequences on Motor Behavior Following Maternal Administration of LPS and Perinatal Anoxia","volume":"31","author":"Stigger","year":"2013","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1093\/schbul\/sbn094","article-title":"Negative Symptoms in Schizophrenia: Avolition and Occam\u2019s Razor","volume":"36","author":"Foussias","year":"2010","journal-title":"Schizophr. Bull."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.bbr.2014.09.032","article-title":"Sexually Dimorphic Effects of Prenatal Exposure to Lipopolysaccharide, and Prenatal and Postnatal Exposure to Propionic Acid, on Acoustic Startle Response and Prepulse Inhibition in Adolescent Rats: Relevance to Autism Spectrum Disorders","volume":"278","author":"Foley","year":"2015","journal-title":"Behav. Brain Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1016\/j.bbr.2007.04.016","article-title":"Effects of Prenatal Infection on Prepulse Inhibition in the Rat Depend on the Nature of the Infectious Agent and the Stage of Pregnancy","volume":"181","author":"Fortier","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0920-9964(00)00139-0","article-title":"Impact of Prepulse Characteristics on the Detection of Sensorimotor Gating Deficits in Schizophrenia","volume":"49","author":"Braff","year":"2001","journal-title":"Schizophr. Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s002130100811","article-title":"Pharmacological Studies of Prepulse Inhibition Models of Sensorimotor Gating Deficits in Schizophrenia: A Decade in Review","volume":"156","author":"Geyer","year":"2001","journal-title":"Psychopharmacology"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.jpsychires.2012.11.018","article-title":"Prepulse Inhibition in Psychiatric Disorders\u2014Apart from Schizophrenia","volume":"47","author":"Kohl","year":"2013","journal-title":"J. Psychiatr. Res."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1002\/aur.1337","article-title":"Increased Prepulse Inhibition and Sensitization of the Startle Reflex in Autistic Children: Sensorimotor Gating in Autistic Children","volume":"7","author":"Madsen","year":"2014","journal-title":"Autism Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1016\/j.biopsych.2005.09.025","article-title":"Sensorimotor Gating Deficits in Adults with Autism","volume":"61","author":"Perry","year":"2007","journal-title":"Biol. Psychiatry"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Kohl, S., Wolters, C., Gruendler, T.O.J., Vogeley, K., Klosterk\u00f6tter, J., and Kuhn, J. (2014). Prepulse Inhibition of the Acoustic Startle Reflex in High Functioning Autism. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0092372"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"26R","DOI":"10.1203\/PDR.0b013e318212c196","article-title":"Schizophrenia and Autism: Both Shared and Disorder-Specific Pathogenesis via Perinatal Inflammation?","volume":"69","author":"Meyer","year":"2011","journal-title":"Pediatr. Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1590\/S1519-69842002000400008","article-title":"Determination of the Estrous Cycle Phases of Rats: Some Helpful Considerations","volume":"62","author":"Marcondes","year":"2002","journal-title":"Braz. J. Biol."},{"key":"ref_88","unstructured":"Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates, Elsevier. [6th ed.]."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1289\/ehp.6088","article-title":"Diminished Experience-Dependent Neuroanatomical Plasticity: Evidence for an Improved Biomarker of Subtle Neurotoxic Damage to the Developing Rat Brain","volume":"111","author":"Wallace","year":"2003","journal-title":"Environ. Health Perspect."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/1742-2094-8-147","article-title":"Post-Traumatic Hypoxia Exacerbates Neurological Deficit, Neuroinflammation and Cerebral Metabolism in Rats with Diffuse Traumatic Brain Injury","volume":"8","author":"Yan","year":"2011","journal-title":"J. Neuroinflammation"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1073\/pnas.94.1.343","article-title":"Place Cells and Place Navigation","volume":"94","author":"Bures","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"11493","DOI":"10.1073\/pnas.95.19.11493","article-title":"Both Here and There: Simultaneous Expression of Autonomous Spatial Memories in Rats","volume":"95","author":"Fenton","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_93","first-page":"S1","article-title":"Place Avoidance Tasks as Tools in the Behavioral Neuroscience of Learning and Memory","volume":"62","author":"Dockery","year":"2013","journal-title":"Physiol. Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1111\/2041-210X.12584","article-title":"BORIS: A Free, Versatile Open-Source Event-Logging Software for Video\/Audio Coding and Live Observations","volume":"7","author":"Friard","year":"2016","journal-title":"Methods Ecol. Evol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/209223a0","article-title":"Behavioural Correlates of the Oestrous Cycle in the Rat","volume":"209","author":"Burke","year":"1966","journal-title":"Nature"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.drugalcdep.2006.12.017","article-title":"Plasma Progesterone Levels and Cocaine-Seeking in Freely Cycling Female Rats across the Estrous Cycle","volume":"89","author":"Feltenstein","year":"2007","journal-title":"Drug Alcohol Depend."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1159\/000346579","article-title":"Maternal Exposure to Lipopolysaccharide Leads to Transient Motor Dysfunction in Neonatal Rats","volume":"35","author":"Rousset","year":"2013","journal-title":"Dev. Neurosci."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/6\/3274\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:39:46Z","timestamp":1760161186000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/6\/3274"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,23]]},"references-count":97,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,3]]}},"alternative-id":["ijms22063274"],"URL":"https:\/\/doi.org\/10.3390\/ijms22063274","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,23]]}}}