{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T13:51:48Z","timestamp":1791899508748,"version":"4.3.4"},"reference-count":93,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2023,1,24]],"date-time":"2023-01-24T00:00:00Z","timestamp":1674518400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,1,24]],"date-time":"2023-01-24T00:00:00Z","timestamp":1674518400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Biol Rep"],"published-print":{"date-parts":[[2023,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Schizophrenia affects millions of people worldwide and is a major challenge for the scientific community. Like most psychotic diseases, it is also considered a complicated mental disorder caused by an imbalance in neurotransmitters. Due to the complexity of neuropathology, it is always a complicated disorder. The lack of proper understanding of the pathophysiology makes the disorder unmanageable in clinical settings. However, due to recent advances in animal models, we hope we can have better therapeutic approaches with more success in clinical settings. Dopamine, glutamate, GABA, and serotonin are the neurotransmitters involved in the pathophysiology of schizophrenia. Various animal models have been put forward based on these neurotransmitters, including pharmacological, neurodevelopmental, and genetic models. Polymorphism of genes such as dysbindin, DICS1, and NRG1 has also been reported in schizophrenia. Hypothesis based on dopamine, glutamate, and serotonin are considered successful models of schizophrenia on which drug therapies have been designed to date. New targets like the orexin system, muscarinic and nicotinic receptors, and cannabinoid receptors have been approached to alleviate the negative and cognitive symptoms. The non-pharmacological models like the post-weaning social isolation model (maternal deprivation), the isolation rearing model etc. have been also\u00a0developed to mimic the symptoms of schizophrenia and to create and test new approaches of drug therapy which is a breakthrough at present in psychiatric disorders. Different behavioral tests have been evaluated in these specific models. This review will highlight the currently available animal models and behavioral tests in psychic disorders concerning schizophrenia.<\/jats:p>","DOI":"10.1007\/s11033-023-08241-7","type":"journal-article","created":{"date-parts":[[2023,1,24]],"date-time":"2023-01-24T16:49:26Z","timestamp":1674578966000},"page":"3767-3785","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["Understanding translational research in schizophrenia: A novel insight into\u00a0animal\u00a0models"],"prefix":"10.1007","volume":"50","author":[{"given":"Jonaid Ahmad","family":"Malik","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zahid","family":"Yaseen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lahari","family":"Thotapalli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sakeel","family":"Ahmed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9865-6224","authenticated-orcid":false,"given":"Mohd Farooq","family":"Shaikh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sirajudheen","family":"Anwar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,1,24]]},"reference":[{"issue":"9","key":"8241_CR1","first-page":"638","volume":"39","author":"KR Patel","year":"2014","unstructured":"Patel KR, Cherian J, Gohil K, Atkinson D (2014) Schizophrenia: overview and treatment options. P T 39(9):638\u2013645","journal-title":"P T"},{"key":"8241_CR2","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/B978-0-12-801829-3.00015-X","volume-title":"The neurobiology of schizophrenia","author":"G Gr\u00fcnder","year":"2016","unstructured":"Gr\u00fcnder G, Cumming P (2016) The dopamine hypothesis of schizophrenia: current status. The neurobiology of schizophrenia. Elsevier, pp 109\u2013124"},{"key":"8241_CR3","doi-asserted-by":"publisher","DOI":"10.3389\/fpsyt.2014.00110","author":"R Brisch","year":"2014","unstructured":"Brisch R et al (2014) The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: old fashioned, but still in vogue. Front Psychiatr. https:\/\/doi.org\/10.3389\/fpsyt.2014.00110","journal-title":"Front Psychiatr"},{"key":"8241_CR4","volume-title":"Clinical handbook of schizophrenia","author":"KT Mueser","year":"2011","unstructured":"Mueser KT, Jeste DV (2011) Clinical handbook of schizophrenia. Guilford Publications"},{"key":"8241_CR5","first-page":"38","volume":"19","author":"R Little","year":"2022","unstructured":"Little R, Dmello D (2022) A cannabinoid hypothesis of schizophrenia: pathways to psychosis\u2014innovations in clinical neuroscience. Innov Clin Neurosci 19:38","journal-title":"Innov Clin Neurosci"},{"issue":"6","key":"8241_CR6","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1016\/j.mehy.2013.03.013","volume":"80","author":"AE Eggers","year":"2013","unstructured":"Eggers AE (2013) A serotonin hypothesis of schizophrenia. Med Hypotheses 80(6):791\u2013794","journal-title":"Med Hypotheses"},{"key":"8241_CR7","first-page":"295","volume":"4","author":"S Akhondzadeh","year":"2001","unstructured":"Akhondzadeh S (2001) The 5-HT hypothesis of schizophrenia. IDrugs 4:295","journal-title":"IDrugs"},{"issue":"3","key":"8241_CR8","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1016\/S2215-0366(19)30302-5","volume":"7","author":"AG Dietz","year":"2020","unstructured":"Dietz AG, Goldman SA, Nedergaard M (2020) Glial cells in schizophrenia: a unified hypothesis. The Lancet Psychiatry 7(3):272\u2013281","journal-title":"The Lancet Psychiatry"},{"key":"8241_CR9","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1007\/978-3-319-90365-1_14","volume-title":"Cannabis use disorders","author":"SK Tikka","year":"2019","unstructured":"Tikka SK, D\u2019Souza DC (2019) The association between cannabinoids and psychosis BT. In: Montoya ID, Weiss SRB (eds) Cannabis use disorders. Springer International Publishing, Cham, pp 127\u2013155"},{"key":"8241_CR10","doi-asserted-by":"publisher","first-page":"399","DOI":"10.3389\/fphar.2017.00399","volume":"8","author":"RN Ruggiero","year":"2017","unstructured":"Ruggiero RN, Rossignoli MT, De Ross JB, Hallak JEC, Leite JP, Bueno-Junior LS (2017) Cannabinoids and vanilloids in schizophrenia: neurophysiological evidence and directions for basic research. Front Pharmacol 8:399","journal-title":"Front Pharmacol"},{"issue":"1","key":"8241_CR11","first-page":"88","volume":"10","author":"T Swanton","year":"2019","unstructured":"Swanton T (2019) The dopamine, glutamate, and GABA hypotheses of schizophrenia: glutamate may be the key. ANU Undergrad Res J 10(1):88\u201396","journal-title":"ANU Undergrad Res J"},{"issue":"4","key":"8241_CR12","doi-asserted-by":"publisher","first-page":"349","DOI":"10.31887\/DCNS.2000.2.4\/pharrison","volume":"2","author":"PJ Harrison","year":"2000","unstructured":"Harrison PJ (2000) Postmortem studies in schizophrenia. Dialogues Clin Neurosci 2(4):349\u2013357","journal-title":"Dialogues Clin Neurosci"},{"issue":"6","key":"8241_CR13","doi-asserted-by":"publisher","first-page":"4","DOI":"10.22159\/ajpcr.2018.v11i6.24557","volume":"11","author":"A Arya","year":"2018","unstructured":"Arya A, Sindhwani G, Kadian R (2018) Neurotransmitter and brain parts involved in schizophrenia. Asian J Pharm Clin Res 11(6):4\u201311","journal-title":"Asian J Pharm Clin Res"},{"key":"8241_CR14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpsyt.2018.00713","volume":"9","author":"C Madeira","year":"2018","unstructured":"Madeira C et al (2018) Blood levels of glutamate and glutamine in recent onset and chronic schizophrenia. Front Psychiatr 9:1\u20138","journal-title":"Front Psychiatr"},{"issue":"2","key":"8241_CR15","doi-asserted-by":"publisher","first-page":"144","DOI":"10.2174\/2211556009666200401150756","volume":"9","author":"S Singh","year":"2020","unstructured":"Singh S, Khanna D, Kalra S (2020) Role of neurochemicals in schizophrenia. Curr Psychopharmacol 9(2):144\u2013161","journal-title":"Curr Psychopharmacol"},{"key":"8241_CR16","doi-asserted-by":"publisher","first-page":"118","DOI":"10.3389\/fpsyt.2017.00118","volume":"8","author":"JC de Jonge","year":"2017","unstructured":"de Jonge JC, Vinkers CH, Hulshoff Pol HE, Marsman A (2017) GABAergic mechanisms in schizophrenia: linking postmortem and in vivo studies. Front. Psychiatry 8:118","journal-title":"Front. Psychiatry"},{"issue":"4","key":"8241_CR17","doi-asserted-by":"publisher","first-page":"324","DOI":"10.4103\/0019-5545.58304","volume":"51","author":"CT Ramachandraiah","year":"2009","unstructured":"Ramachandraiah CT, Subramaniam N, Tancer M (2009) The story of antipsychotics: past and present. Indian J Psychiatry 51(4):324\u2013326","journal-title":"Indian J Psychiatry"},{"key":"8241_CR18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpsyt.2019.00049","volume":"10","author":"F Nicoletti","year":"2019","unstructured":"Nicoletti F et al (2019) Targeting mGlu receptors for optimization of antipsychotic activity and disease-modifying effect in schizophrenia. Front Psychiatr 10:1\u201310","journal-title":"Front Psychiatr"},{"issue":"4","key":"8241_CR19","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1093\/ijnp\/pyaa080","volume":"24","author":"SM Perez","year":"2021","unstructured":"Perez SM, Lodge DJ (2021) Orexin modulation of VTA dopamine neuron activity: relevance to schizophrenia. Int J Neuropsychopharmacol 24(4):344","journal-title":"Int J Neuropsychopharmacol"},{"issue":"2","key":"8241_CR20","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1016\/j.bbr.2009.05.004","volume":"204","author":"I Weiner","year":"2009","unstructured":"Weiner I, Arad M (2009) Using the pharmacology of latent inhibition to model domains of pathology in schizophrenia and their treatment. Behav Brain Res 204(2):369\u2013386","journal-title":"Behav Brain Res"},{"issue":"3","key":"8241_CR21","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1007\/s00213-008-1072-4","volume":"199","author":"NR Swerdlow","year":"2008","unstructured":"Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology 199(3):331","journal-title":"Psychopharmacology"},{"key":"8241_CR22","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1038\/nprot.2008.41","volume":"3","author":"A Bari","year":"2008","unstructured":"Bari A, Dalley J, Robbins T (2008) The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protoc 3:759\u2013767","journal-title":"Nat Protoc"},{"issue":"9","key":"8241_CR23","doi-asserted-by":"publisher","first-page":"2411","DOI":"10.1038\/npp.2016.55","volume":"41","author":"H Eryilmaz","year":"2016","unstructured":"Eryilmaz H et al (2016) Disrupted working memory circuitry in schizophrenia: disentangling fMRI markers of core pathology vs other aspects of impaired performance. Neuropsychopharmacology 41(9):2411\u20132420","journal-title":"Neuropsychopharmacology"},{"issue":"3","key":"8241_CR24","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1037\/0021-843X.111.3.425","volume":"111","author":"MJ Coleman","year":"2002","unstructured":"Coleman MJ et al (2002) Spatial and object working memory impairments in schizophrenia patients: a Bayesian item-response theory analysis. J Abnorm Psychol 111(3):425\u2013435","journal-title":"J Abnorm Psychol"},{"issue":"2","key":"8241_CR25","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.pnpbp.2012.04.018","volume":"38","author":"BA Chindo","year":"2012","unstructured":"Chindo BA, Adzu B, Yahaya TA, Gamaniel KS (2012) Ketamine-enhanced immobility in forced swim test: a possible animal model for the negative symptoms of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 38(2):310\u2013316","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"8241_CR26","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1093\/schbul\/sbj009","volume":"32","author":"WP Horan","year":"2006","unstructured":"Horan WP, Kring AM, Blanchard JJ (2006) Anhedonia in schizophrenia: a review of assessment strategies. Schizophr Bull 32:259","journal-title":"Schizophr Bull"},{"key":"8241_CR27","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/B978-0-12-804078-2.00014-3","volume-title":"Molecular-genetic and statistical techniques for behavioral and neural research","author":"NN Kudryavtseva","year":"2018","unstructured":"Kudryavtseva NN, Kovalenko IL, Smagin DA, Galyamina AG, Babenko VN (2018) Abnormal social behaviors and dysfunction of autism-related genes associated with daily agonistic interactions in mice. Molecular-genetic and statistical techniques for behavioral and neural research. Elsevier, pp 309\u2013344"},{"issue":"1","key":"8241_CR28","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1177\/0706743718773728","volume":"64","author":"IR Winship","year":"2019","unstructured":"Winship IR et al (2019) An overview of animal models related to schizophrenia. Can J Psychiatr 64(1):5\u201317","journal-title":"Can J Psychiatr"},{"key":"8241_CR29","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/B978-0-12-801560-5.00025-2","volume-title":"Network neuroscience","author":"F Fr\u00f6hlich","year":"2016","unstructured":"Fr\u00f6hlich F (2016) Schizophrenia. Network neuroscience. Elseiver, pp 309\u2013318"},{"key":"8241_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpsyt.2020.00868","volume":"11","author":"CL Shen","year":"2020","unstructured":"Shen CL et al (2020) P50, N100, and P200 auditory sensory gating deficits in schizophrenia patients. Front Psychiatr 11:1\u201311","journal-title":"Front Psychiatr"},{"key":"8241_CR31","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/j.schres.2020.02.003","volume":"218","author":"R Freedman","year":"2020","unstructured":"Freedman R, Olsen-Dufour AM, Olincy A (2020) P50 inhibitory sensory gating in schizophrenia: analysis of recent studies. Schizophr Res 218:93\u201398","journal-title":"Schizophr Res"},{"issue":"10","key":"8241_CR32","doi-asserted-by":"publisher","first-page":"2099","DOI":"10.1016\/j.clinph.2018.07.012","volume":"129","author":"T Rosburg","year":"2018","unstructured":"Rosburg T (2018) Auditory N100 gating in patients with schizophrenia: a systematic meta-analysis. Clin Neurophysiol 129(10):2099\u20132111","journal-title":"Clin Neurophysiol"},{"key":"8241_CR33","doi-asserted-by":"publisher","first-page":"e1237","DOI":"10.1038\/tp.2017.198","volume":"7","author":"A Ahnaou","year":"2017","unstructured":"Ahnaou A, Huysmans H, Biermans R, Manyakov NV, Drinkenburg WHIM (2017) Ketamine: differential neurophysiological dynamics in functional networks in the rat brain. Transl Psychiatr 7:e1237","journal-title":"Transl Psychiatr"},{"issue":"4","key":"8241_CR34","doi-asserted-by":"publisher","first-page":"1162","DOI":"10.1111\/j.1476-5381.2011.01386.x","volume":"164","author":"C Jones","year":"2011","unstructured":"Jones C, Watson D, Fone K (2011) Animal models of schizophrenia. Br J Pharmacol 164(4):1162","journal-title":"Br J Pharmacol"},{"key":"8241_CR35","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-800212-4.00026-1","volume-title":"Amphetamine-induced psychosis","author":"V Farnia","year":"2016","unstructured":"Farnia V, Golshani S (2016) Amphetamine-induced psychosis. Elsevier Inc"},{"issue":"1","key":"8241_CR36","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1177\/2045125314557797","volume":"5","author":"H Steeds","year":"2015","unstructured":"Steeds H, Carhart-Harris RL, Stone JM (2015) Drug models of schizophrenia. Ther Adv Psychopharmacol 5(1):43\u201358","journal-title":"Ther Adv Psychopharmacol"},{"issue":"6","key":"8241_CR37","doi-asserted-by":"publisher","first-page":"1172","DOI":"10.1093\/schbul\/sbx116","volume":"43","author":"N Kanyuch","year":"2017","unstructured":"Kanyuch N, Anderson S (2017) Animal models of developmental neuropathology in schizophrenia. Schizophr Bull 43(6):1172\u20131175","journal-title":"Schizophr Bull"},{"issue":"4","key":"8241_CR38","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1038\/sj.npp.1301179","volume":"32","author":"LD Selemon","year":"2007","unstructured":"Selemon LD, Begovi\u0107 A, Goldman-Rakic PS, Castner SA (2007) Amphetamine sensitization alters dendritic morphology in prefrontal cortical pyramidal neurons in the non-human primate. Neuropsychopharmacology 32(4):919\u2013931","journal-title":"Neuropsychopharmacology"},{"issue":"8","key":"8241_CR39","doi-asserted-by":"publisher","first-page":"1556","DOI":"10.1016\/j.pnpbp.2007.08.025","volume":"31","author":"RE Featherstone","year":"2007","unstructured":"Featherstone RE, Kapur S, Fletcher PJ (2007) The amphetamine-induced sensitized state as a model of schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatr 31(8):1556\u20131571","journal-title":"Prog Neuro-Psychopharmacol Biol Psychiatr"},{"issue":"10","key":"8241_CR40","doi-asserted-by":"publisher","first-page":"2074","DOI":"10.1038\/sj.npp.1301352","volume":"32","author":"R Kozak","year":"2007","unstructured":"Kozak R, Martinez V, Young D, Brown H, Bruno JP, Sarter M (2007) Toward a neuro-cognitive animal model of the cognitive symptoms of schizophrenia: disruption of cortical cholinergic neurotransmission following repeated amphetamine exposure in attentional task-performing, but not non-performing, rats. Neuropsychopharmacology 32(10):2074\u20132086","journal-title":"Neuropsychopharmacology"},{"key":"8241_CR41","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3390\/brainsci11070917","volume":"11","author":"S Estaphan","year":"2021","unstructured":"Estaphan S et al (2021) Combined low dose of ketamine and social isolation: A possible model of induced chronic schizophrenia-like symptoms in male albino rats. Brain Sci 11:7","journal-title":"Brain Sci"},{"issue":"8","key":"8241_CR42","doi-asserted-by":"publisher","first-page":"2921","DOI":"10.1523\/JNEUROSCI.17-08-02921.1997","volume":"17","author":"B Moghaddam","year":"1997","unstructured":"Moghaddam B, Adams B, Verma A, Daly D (1997) Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17(8):2921\u20132927","journal-title":"J Neurosci"},{"key":"8241_CR43","doi-asserted-by":"publisher","first-page":"11","DOI":"10.3390\/ijms23115968","volume":"23","author":"M Bia\u0142o\u0144","year":"2022","unstructured":"Bia\u0142o\u0144 M, W\u0105sik A (2022) Advantages and limitations of animal schizophrenia models. Int J Mol Sci 23:11","journal-title":"Int J Mol Sci"},{"key":"8241_CR44","doi-asserted-by":"publisher","first-page":"5968","DOI":"10.1371\/journal.pone.0059395","volume":"8","author":"J Genius","year":"2013","unstructured":"Genius J et al (2013) Glutamatergic dysbalance and oxidative stress in in vivo and in vitro models of psychosis based on chronic NMDA receptor antagonism. PLoS ONE 8:5968","journal-title":"PLoS ONE"},{"issue":"1","key":"8241_CR45","doi-asserted-by":"publisher","first-page":"3","DOI":"10.5507\/crj.2015.001","volume":"4","author":"M Svojanovsk\u00e1","year":"2015","unstructured":"Svojanovsk\u00e1 M, Stuchl\u00edk A (2015) Animal models of schizophrenia with a focus on models targeting NMDA receptors. Cogn Remediat J 4(1):3\u201318","journal-title":"Cogn Remediat J"},{"key":"8241_CR46","doi-asserted-by":"publisher","first-page":"185","DOI":"10.3389\/fnmol.2019.00185","volume":"12","author":"G Lee","year":"2019","unstructured":"Lee G, Zhou Y (2019) NMDAR hypofunction animal models of schizophrenia. Front Mol Neurosci 12:185","journal-title":"Front Mol Neurosci"},{"issue":"7","key":"8241_CR47","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1080\/17460441.2021.1877657","volume":"16","author":"MG Sotiropoulos","year":"2021","unstructured":"Sotiropoulos MG, Poulogiannopoulou E, Delis F, Dalla C, Antoniou K, Kokras N (2021) Innovative screening models for the discovery of new schizophrenia drug therapies: an integrated approach. Expert Opin Drug Discov 16(7):791\u2013806","journal-title":"Expert Opin Drug Discov"},{"key":"8241_CR48","doi-asserted-by":"publisher","first-page":"101889","DOI":"10.1016\/j.jchemneu.2020.101889","volume":"111","author":"I Camacho-Abrego","year":"2021","unstructured":"Camacho-Abrego I, Gonz\u00e1lez-Cano SI, Aguilar-Alonso P, Brambila E, de la Cruz F, Flores G (2021) Changes in nitric oxide, zinc and metallothionein levels in limbic regions at pre-pubertal and post-pubertal ages presented in an animal model of schizophrenia. J Chem Neuroanat 111:101889","journal-title":"J Chem Neuroanat"},{"issue":"1","key":"8241_CR49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12991-021-00353-3","volume":"20","author":"S Ahn","year":"2021","unstructured":"Ahn S et al (2021) Effects of comorbid alcohol use disorder on the clinical outcomes of first-episode schizophrenia: a nationwide population-based study. Ann Gen Psychiatry 20(1):1\u20138","journal-title":"Ann Gen Psychiatry"},{"key":"8241_CR50","doi-asserted-by":"publisher","first-page":"108","DOI":"10.3390\/biom12010108","volume":"12","author":"T Stark","year":"2022","unstructured":"Stark T et al (2022) Early blockade of CB1 receptors ameliorates schizophrenia-like alterations in the neurodevelopmental MAM model of schizophrenia. Biomolecules 12:108","journal-title":"Biomolecules"},{"key":"8241_CR51","volume-title":"Decreases in the frontal cortical areas following a developmental disruption model of schizophrenia","author":"A Healy","year":"2021","unstructured":"Healy A (2021) Decreases in the frontal cortical areas following a developmental disruption model of schizophrenia. Bridgewater State University"},{"key":"8241_CR52","doi-asserted-by":"publisher","first-page":"e10","DOI":"10.35430\/nab.2020.e10","volume":"2","author":"V Menne","year":"2020","unstructured":"Menne V, Chesworth R (2020) Schizophrenia and drug addiction comorbidity: recent advances in our understanding of behavioural susceptibility and neural mechanisms. Neuroanat Behav 2:e10","journal-title":"Neuroanat Behav"},{"key":"8241_CR53","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.pnpbp.2018.06.013","volume":"88","author":"DJ Clarke","year":"2019","unstructured":"Clarke DJ et al (2019) Nrg1 deficiency modulates the behavioural effects of prenatal stress in mice. Prog Neuro-Psychopharmacol Biol Psychiatr 88:86\u201395","journal-title":"Prog Neuro-Psychopharmacol Biol Psychiatr"},{"key":"8241_CR54","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnmol.2018.00423","volume":"11","author":"F Matrisciano","year":"2018","unstructured":"Matrisciano F, Dong E, Nicoletti F, Guidotti A (2018) Epigenetic alterations in prenatal stress mice as an endophenotype model for schizophrenia: role of metabotropic glutamate 2\/3 receptors. Front Mol Neurosci 11:1\u20138","journal-title":"Front Mol Neurosci"},{"issue":"6","key":"8241_CR55","doi-asserted-by":"publisher","first-page":"1574","DOI":"10.3892\/ijmm.2015.2161","volume":"35","author":"H Lee","year":"2015","unstructured":"Lee H et al (2015) Changes in Dpysl2 expression are associated with prenatally stressed rat offspring and susceptibility to schizophrenia in humans. Int J Mol Med 35(6):1574\u20131586","journal-title":"Int J Mol Med"},{"key":"8241_CR56","doi-asserted-by":"publisher","DOI":"10.15406\/mojap.2018.05.00211","author":"N Rodriguez","year":"2018","unstructured":"Rodriguez N, Liaudat AC, Mayer NI, Vivas A, Romanini MC, Bosch P (2018) Attenuation effects of prenatal stress by early postnatal stimulation in different research models. MOJ Anat Physiol. https:\/\/doi.org\/10.15406\/mojap.2018.05.00211","journal-title":"MOJ Anat Physiol"},{"issue":"1","key":"8241_CR57","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.bandc.2009.06.003","volume":"72","author":"CM McCormick","year":"2010","unstructured":"McCormick CM, Mathews IZ, Thomas C, Waters P (2010) Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn 72(1):73\u201385","journal-title":"Brain Cogn"},{"issue":"6","key":"8241_CR58","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1016\/j.neubiorev.2008.03.003","volume":"32","author":"KCF Fone","year":"2008","unstructured":"Fone KCF, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32(6):1087\u20131102","journal-title":"Neurosci Biobehav Rev"},{"key":"8241_CR59","doi-asserted-by":"crossref","first-page":"394","DOI":"10.55782\/ane-2013-1946","volume":"73","author":"M Aksi\u0107","year":"2013","unstructured":"Aksi\u0107 M et al (2013) Long-term effects of the maternal deprivation on the volume and number of neurons in the rat neocortex and hippocampus. Acta Neurobiol Exp 73:394","journal-title":"Acta Neurobiol Exp"},{"issue":"2","key":"8241_CR60","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1007\/s00213-010-2128-9","volume":"215","author":"K Fabricius","year":"2011","unstructured":"Fabricius K, Helboe L, Fink-Jensen A, W\u00f6rtwein G, Steiniger-Brach B (2011) Pharmacological characterization of social isolation-induced hyperactivity. Psychopharmacology 215(2):257\u2013266","journal-title":"Psychopharmacology"},{"issue":"4","key":"8241_CR61","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1017\/S1461145711000435","volume":"15","author":"DJG Watson","year":"2012","unstructured":"Watson DJG, Marsden CA, Millan MJ, Fone KCF (2012) Blockade of dopamine D3 but not D2 receptors reverses the novel object discrimination impairment produced by post-weaning social isolation: implications for schizophrenia and its treatment. Int J Neuropsychopharmacol 15(4):471\u2013484","journal-title":"Int J Neuropsychopharmacol"},{"issue":"6","key":"8241_CR62","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1016\/0006-3223(93)90180-L","volume":"34","author":"MA Geyer","year":"1993","unstructured":"Geyer MA, Wilkinson LS, Humby T, Robbins TW (1993) Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol Psychiatry 34(6):361\u2013372","journal-title":"Biol Psychiatry"},{"key":"8241_CR63","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/B978-0-12-800981-9.00009-2","volume":"23","author":"SB Powell","year":"2016","unstructured":"Powell SB, Swerdlow NR (2016) Social isolation rearing and sensorimotor gating in rat models of relevance to schizophrenia: what we know, and what we do not know. Handb Behav Neurosci 23:125\u2013138","journal-title":"Handb Behav Neurosci"},{"issue":"1","key":"8241_CR64","doi-asserted-by":"publisher","first-page":"388","DOI":"10.3758\/s13415-013-0204-4","volume":"14","author":"N Amitai","year":"2014","unstructured":"Amitai N, Young JW, Higa K, Sharp RF, Geyer MA, Powell SB (2014) Isolation rearing effects on probabilistic learning and cognitive flexibility in rats. Cogn Affect Behav Neurosci 14(1):388\u2013406","journal-title":"Cogn Affect Behav Neurosci"},{"key":"8241_CR65","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/j.bbi.2012.12.011","volume":"30","author":"M M\u00f6ller","year":"2013","unstructured":"M\u00f6ller M, Du Preez JL, Viljoen FP, Berk M, Emsley R, Harvey BH (2013) Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioural deficits in rats, and is reversed by clozapine or N-acetyl cysteine. Brain Behav Immun 30:156\u2013167","journal-title":"Brain Behav Immun"},{"issue":"3","key":"8241_CR66","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1590\/S0100-879X2012007500031","volume":"45","author":"DS Mac\u00eado","year":"2012","unstructured":"Mac\u00eado DS et al (2012) Animal models of prenatal immune challenge and their contribution to the study of schizophrenia: a systematic review. Brazilian J Med Biol Res 45(3):179","journal-title":"Brazilian J Med Biol Res"},{"issue":"3","key":"8241_CR67","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1176\/appi.ajp.2009.09030361","volume":"167","author":"AS Brown","year":"2010","unstructured":"Brown AS, Derkits EJ (2010) Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 167(3):261","journal-title":"Am J Psychiatry"},{"issue":"6","key":"8241_CR68","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1016\/j.biopsych.2005.07.031","volume":"59","author":"K Ozawa","year":"2006","unstructured":"Ozawa K, Hashimoto K, Kishimoto T, Shimizu E, Ishikura H, Iyo M (2006) Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol Psychiatry 59(6):546\u2013554","journal-title":"Biol Psychiatry"},{"issue":"4","key":"8241_CR69","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1017\/S1461145708009206","volume":"12","author":"C Winter","year":"2009","unstructured":"Winter C et al (2009) Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: implications for brain disorders of neurodevelopmental origin such as schizophrenia. Int J Neuropsychopharmacol 12(4):513\u2013524","journal-title":"Int J Neuropsychopharmacol"},{"issue":"6","key":"8241_CR70","doi-asserted-by":"publisher","first-page":"1054","DOI":"10.1093\/schbul\/sbn096","volume":"34","author":"AS Brown","year":"2008","unstructured":"Brown AS, Susser ES (2008) Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull 34(6):1054","journal-title":"Schizophr Bull"},{"key":"8241_CR71","doi-asserted-by":"crossref","first-page":"472","DOI":"10.55782\/ane-2013-1953","volume":"73","author":"P Ratajczak","year":"2013","unstructured":"Ratajczak P, Wo\u017aniak A, Nowakowska E (2013) Animal models of schizophrenia: developmental preparation in rats. Acta Neurobiol Exp 73:472","journal-title":"Acta Neurobiol Exp"},{"issue":"2","key":"8241_CR72","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.brainres.2003.09.077","volume":"996","author":"AA Palmer","year":"2004","unstructured":"Palmer AA, Printz DJ, Butler PD, Dulawa SC, Printz MP (2004) Prenatal protein deprivation in rats induces changes in prepulse inhibition and NMDA receptor binding. Brain Res 996(2):193\u2013201","journal-title":"Brain Res"},{"issue":"3","key":"8241_CR73","doi-asserted-by":"publisher","first-page":"24","DOI":"10.3390\/brainsci6030024","volume":"6","author":"MG Morgese","year":"2016","unstructured":"Morgese MG, Trabace L (2016) Maternal malnutrition in the etiopathogenesis of psychiatric diseases: role of polyunsaturated fatty acids. Brain Sci 6(3):24","journal-title":"Brain Sci"},{"key":"8241_CR74","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2013.00111","author":"JP Kesby","year":"2013","unstructured":"Kesby JP, Cui X, Burne THJ, Eyles DW (2013) Altered dopamine ontogeny in the developmentally vitamin D deficient rat and its relevance to schizophrenia. Front Cell Neurosci. https:\/\/doi.org\/10.3389\/fncel.2013.00111","journal-title":"Front Cell Neurosci"},{"issue":"9","key":"8241_CR75","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/S0166-2236(00)01886-5","volume":"24","author":"RR Gainetdinov","year":"2001","unstructured":"Gainetdinov RR, Mohn AR, Caron MG (2001) Genetic animal models: focus on schizophrenia. Trends Neurosci 24(9):527\u2013533","journal-title":"Trends Neurosci"},{"issue":"12","key":"8241_CR76","first-page":"139","volume":"176","author":"K Schaumberg","year":"2017","unstructured":"Schaumberg K, Weich E, Breithaupt L, Hubel C, Baker J, Munn-Chernoff M (2017) \u4e73\u9f20\u5fc3\u808c\u63d0\u53d6 HHS public access. Physiol Behav 176(12):139\u2013148","journal-title":"Physiol Behav"},{"issue":"12","key":"8241_CR77","doi-asserted-by":"publisher","first-page":"2091","DOI":"10.4103\/1673-5374.241453","volume":"13","author":"D Leo","year":"2018","unstructured":"Leo D, Sukhanov I, Gainetdinov RR (2018) Novel translational rat models of dopamine transporter deficiency. Neural Regen Res 13(12):2091\u20132093","journal-title":"Neural Regen Res"},{"issue":"2","key":"8241_CR78","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1002\/ajmg.b.32578","volume":"177","author":"A Salatino-Oliveira","year":"2018","unstructured":"Salatino-Oliveira A, Rohde LA, Hutz MH (2018) The dopamine transporter role in psychiatric phenotypes. Am. J. Med. Genet. Part B Neuropsychiatr. Genet. 177(2):211\u2013231","journal-title":"Am. J. Med. Genet. Part B Neuropsychiatr. Genet."},{"issue":"4","key":"8241_CR79","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1590\/1516-4446-2016-1987","volume":"39","author":"CT Matsuzaka","year":"2017","unstructured":"Matsuzaka CT et al (2017) Catechol-O-methyltransferase (COMT) polymorphisms modulate working memory in individuals with schizophrenia and healthy controls. Rev Bras Psiquiatr 39(4):302\u2013308","journal-title":"Rev Bras Psiquiatr"},{"issue":"3","key":"8241_CR80","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1007\/s00406-005-0583-9","volume":"255","author":"W Maier","year":"2005","unstructured":"Maier W, H\u00f6fgen B, Zobel A, Rietschel M (2005) Genetic models of schizophrenia and bipolar disorder: overlapping inheritance or discrete genotypes? Eur Arch Psychiatry Clin Neurosci 255(3):159\u2013166","journal-title":"Eur Arch Psychiatry Clin Neurosci"},{"issue":"4","key":"8241_CR81","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1016\/j.pharep.2018.01.009","volume":"70","author":"A Nikiforuk","year":"2018","unstructured":"Nikiforuk A (2018) Assessment of cognitive functions in animal models of schizophrenia. Pharmacol Reports 70(4):639\u2013649","journal-title":"Pharmacol Reports"},{"issue":"1","key":"8241_CR82","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1080\/00207144.2018.1396120","volume":"66","author":"ZI Storozheva","year":"2018","unstructured":"Storozheva ZI, Kirenskaya AV, Gordeev MN, Kovaleva ME, Novototsky-Vlasov VY (2018) COMT genotype and sensory and sensorimotor gating in high and low hypnotizable subjects. Int J Clin Exp Hypn 66(1):83\u2013105","journal-title":"Int J Clin Exp Hypn"},{"key":"8241_CR83","volume-title":"Gene models of schizophrenia: DISC1 mouse models","author":"H Jaaro-Peled","year":"2009","unstructured":"Jaaro-Peled H (2009) Gene models of schizophrenia: DISC1 mouse models. Elsevier"},{"key":"8241_CR84","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.neuroscience.2015.12.061","volume":"321","author":"T Tomoda","year":"2016","unstructured":"Tomoda T, Sumitomo A, Jaaro-Peled H, Sawa A (2016) Utility and validity of DISC1 mouse models in biological psychiatry. Neuroscience 321:99\u2013107","journal-title":"Neuroscience"},{"key":"8241_CR85","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fphar.2019.01638","volume":"10","author":"JL Waddington","year":"2020","unstructured":"Waddington JL, Zhen X, O\u2019Tuathaigh CMP (2020) Developmental genes and regulatory proteins, domains of cognitive impairment in schizophrenia spectrum psychosis and implications for antipsychotic drug discovery: the example of dysbindin-1 isoforms and beyond. Front Pharmacol 10:1\u201312","journal-title":"Front Pharmacol"},{"key":"8241_CR86","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1016\/j.schres.2018.04.042","volume":"201","author":"GT Konopaske","year":"2018","unstructured":"Konopaske GT, Balu DT, Presti KT, Chan G, Benes FM, Coyle JT (2018) Dysbindin-1 contributes to prefrontal cortical dendritic arbor pathology in schizophrenia. Schizophr Res 201:270\u2013277","journal-title":"Schizophr Res"},{"issue":"1","key":"8241_CR87","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1080\/15622975.2018.1523562","volume":"21","author":"KE Schoonover","year":"2018","unstructured":"Schoonover KE, Queern SL, Lapi SE, Roberts RC (2018) Impaired copper transport in schizophrenia results in a copper-deficient brain state: a new side to the dysbindin story. World J Biol 21(1):13\u201328. https:\/\/doi.org\/10.1080\/15622975.2018.1523562","journal-title":"World J Biol"},{"key":"8241_CR88","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbr.2021.113166","author":"S Guerra","year":"2021","unstructured":"Guerra S, Chesworth R, Weickert CS, Karl T (2021) Effects of handling on the behavioural phenotype of the neuregulin 1 type III transgenic mouse model for schizophrenia. Behav Brain Res. https:\/\/doi.org\/10.1016\/j.bbr.2021.113166","journal-title":"Behav Brain Res"},{"issue":"5","key":"8241_CR89","doi-asserted-by":"publisher","first-page":"417","DOI":"10.3109\/09540261.2010.515205","volume":"22","author":"KM Abel","year":"2010","unstructured":"Abel KM, Drake R, Goldstein JM (2010) Sex differences in schizophrenia. Int Rev Psychiatry 22(5):417\u2013428","journal-title":"Int Rev Psychiatry"},{"key":"8241_CR90","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.neuropharm.2018.10.026","volume":"144","author":"K Chalkiadaki","year":"2019","unstructured":"Chalkiadaki K et al (2019) Development of the MAM model of schizophrenia in mice: Sex similarities and differences of hippocampal and prefrontal cortical function. Neuropharmacology 144:193\u2013207","journal-title":"Neuropharmacology"},{"issue":"1","key":"8241_CR91","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1038\/s41386-018-0179-5","volume":"44","author":"NM Grissom","year":"2019","unstructured":"Grissom NM, Reyes TM (2019) Let\u2019s call the whole thing off: evaluating gender and sex differences in executive function. Neuropsychopharmacology 44(1):86\u201396","journal-title":"Neuropsychopharmacology"},{"key":"8241_CR92","doi-asserted-by":"publisher","first-page":"703","DOI":"10.3389\/fpsyt.2020.00703","volume":"11","author":"V Langova","year":"2020","unstructured":"Langova V, Vales K, Horka P, Horacek J (2020) The role of zebrafish and laboratory rodents in schizophrenia research. Front Psychiatry 11:703","journal-title":"Front Psychiatry"},{"issue":"2","key":"8241_CR93","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1007\/s10561-020-09888-3","volume":"22","author":"B Larijani","year":"2021","unstructured":"Larijani B et al (2021) Stem cell-based models and therapies: a key approach into schizophrenia treatment. Cell Tissue Bank 22(2):207\u2013223","journal-title":"Cell Tissue Bank"}],"updated-by":[{"DOI":"10.1007\/s11033-023-08352-1","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T00:00:00Z","timestamp":1680739200000}}],"container-title":["Molecular Biology Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11033-023-08241-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11033-023-08241-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11033-023-08241-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,5]],"date-time":"2023-12-05T14:35:43Z","timestamp":1701786943000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11033-023-08241-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,24]]},"references-count":93,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2023,4]]}},"alternative-id":["8241"],"URL":"https:\/\/doi.org\/10.1007\/s11033-023-08241-7","relation":{"correction":[{"id-type":"doi","id":"10.1007\/s11033-023-08352-1","asserted-by":"object"}]},"ISSN":["0301-4851","1573-4978"],"issn-type":[{"value":"0301-4851","type":"print"},{"value":"1573-4978","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,24]]},"assertion":[{"value":"6 July 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 January 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 January 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 March 2023","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Update","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Missing Open Access funding information has been added in the Funding Note.","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 April 2023","order":7,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Correction","order":8,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"A Correction to this paper has been published:","order":9,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"https:\/\/doi.org\/10.1007\/s11033-023-08352-1","URL":"https:\/\/doi.org\/10.1007\/s11033-023-08352-1","order":10,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors have no\u00a0conflict of interest with anybody\u00a0or any competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}