Neonatal phencyclidine as a model of sex-biased schizophrenia symptomatology in adolescent mice.
Cognition
Neurodevelopment
Postnatal phencyclidine
Psychosis
Sex differences
Social behavior
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
22
04
2023
accepted:
22
07
2023
medline:
19
9
2023
pubmed:
2
8
2023
entrez:
2
8
2023
Statut:
ppublish
Résumé
Sex-biased differences in schizophrenia are evident in several features of the disease, including symptomatology and response to pharmacological treatments. As a neurodevelopmental disorder, these differences might originate early in life and emerge later during adolescence. Considering that the disruption of the glutamatergic system during development is known to contribute to schizophrenia, we hypothesized that the neonatal phencyclidine model could induce sex-dependent behavioral and neurochemical changes associated with this disorder during adolescence. C57BL/6 mice received either saline or phencyclidine (5, 10, or 20 mg/kg) on postnatal days (PN) 7, 9, and 11. Behavioral assessment occurred in late adolescence (PN48-50), when mice were submitted to the open field, social interaction, and prepulse inhibition tests. Either olanzapine or saline was administered before each test. The NMDAR obligatory GluN1 subunit and the postsynaptic density protein 95 (PSD-95) were evaluated in the frontal cortex and hippocampus at early (PN30) and late (PN50) adolescence. Neonatal phencyclidine evoked dose-dependent deficits in all analyzed behaviors and males were more susceptible. Males also had reduced GluN1 expression in the frontal cortex at PN30. There were late-emergent effects at PN50. Cortical GluN1 was increased in both sexes, while phencyclidine increased cortical and decreased hippocampal PSD-95 in females. Olanzapine failed to mitigate most phencyclidine-evoked alterations. In some instances, this antipsychotic aggravated the deficits or potentiated subthreshold effects. These results lend support to the use of neonatal phencyclidine as a sex-biased neurodevelopmental preclinical model of schizophrenia. Olanzapine null effects and deleterious outcomes suggest that its use during adolescence should be further evaluated.
Identifiants
pubmed: 37530885
doi: 10.1007/s00213-023-06434-3
pii: 10.1007/s00213-023-06434-3
doi:
Substances chimiques
Phencyclidine
J1DOI7UV76
Olanzapine
N7U69T4SZR
Antipsychotic Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2111-2129Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abreu-Villaça Y, Correa-Santos M, Dutra-Tavares AC, Paes-Branco D, Nunes-Freitas A, Manhães AC, Filgueiras CC, Ribeiro-Carvalho A (2016) A ten fold reduction of nicotine yield in tobacco smoke does not spare the central cholinergic system in adolescent mice. Int J Dev Neurosci 52:93–103. https://doi.org/10.1016/j.ijdevneu.2016.06.002
doi: 10.1016/j.ijdevneu.2016.06.002
pubmed: 27287270
Amani M, Samadi H, Doosti M-H, Azarfarin M, Bakhtiari A, Majidi-Zolbanin N, Mirza-Rahimi M, Salari A-A (2013) Neonatal NMDA receptor blockade alters anxiety- and depression-related behaviors in a sex-dependent manner in mice. Neuropharmacology 73:87–97. https://doi.org/10.1016/j.neuropharm.2013.04.056
doi: 10.1016/j.neuropharm.2013.04.056
pubmed: 23688920
Anastasio NC, Johnson KM (2008) Atypical anti-schizophrenic drugs prevent changes in cortical N-methyl-D-aspartate receptors and behavior following sub-chronic phencyclidine administration in developing rat pups. Pharmacol Biochem Behav 90(4):569–577. https://doi.org/10.1016/j.pbb.2008.04.017
doi: 10.1016/j.pbb.2008.04.017
pubmed: 18544461
pmcid: 2604119
Apam-Castillejos DJ, Tendilla-Beltrán H, Vázquez-Roque RA, Vázquez-Hernández AJ, Fuentes-Medel E, García-Dolores F, Díaz A, Flores G (2022) Second-generation antipsychotic olanzapine attenuates behavioral and prefrontal cortex synaptic plasticity deficits in a neurodevelopmental schizophrenia-related rat model. J Chem Neuroanat 125:102166. https://doi.org/10.1016/j.jchemneu.2022.102166
doi: 10.1016/j.jchemneu.2022.102166
pubmed: 36156295
Balu DT, Coyle JT (2011) Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Ver 35(3):848–870. https://doi.org/10.1016/j.neubiorev.2010.10.005
doi: 10.1016/j.neubiorev.2010.10.005
Bakker J (2022) The role of steroid hormones in the sexual differentiation of the human brain. J Neuroendocrinol 34(2):e13050. https://doi.org/10.1111/jne.13050
doi: 10.1111/jne.13050
pubmed: 34708466
Barendse MEA, Lara GA, Guyer AE, Swartz JR, Taylor SL, Shirtcliff EA, Lamb ST, Miller C, Ng J, Yu G, Tully LM (2023) Sex and pubertal influences on the neurodevelopmental underpinnings of schizophrenia: a case for longitudinal research on adolescents. Schizophr Res 252:231–241. https://doi.org/10.1016/j.schres.2022.12.011
doi: 10.1016/j.schres.2022.12.011
pubmed: 36682313
Bervoets C, Docx L, Sabbe B, Vermeylen S, Van Den Bossche MJ, Morsel A, Morrens M (2014) The nature of the relationship of psychomotor slowing with negative symptomatology in schizophrenia. Cogn Neuropsychiatry 19(1):36–46. https://doi.org/10.1080/13546805.2013.779578
doi: 10.1080/13546805.2013.779578
pubmed: 23725330
Bo Q, Mao Z, Tian Q, Yang N, Li X, Dong F, Zhou F, Li L, Wang C (2021) Impaired sensorimotor gating using the acoustic prepulse inhibition paradigm in individuals at a clinical high risk for psychosis. Schizophr Bull 47(1):128–137. https://doi.org/10.1093/schbul/sbaa102 Erratum in: Schizophr Bull. 2021;47(1):268
doi: 10.1093/schbul/sbaa102
pubmed: 32743658
Boctor SY, Ferguson SA (2009) Neonatal NMDA receptor antagonist treatments have no effects on prepulse inhibition of postnatal day 25 Sprague-Dawley rats. Neurotoxicology 30(1):151–154. https://doi.org/10.1016/j.neuro.2008.10.011
doi: 10.1016/j.neuro.2008.10.011
Boctor SY, Wang C, Ferguson SA (2008) Neonatal PCP is more potent than ketamine at modifying preweaning behaviors of Sprague-Dawley rats. Toxicol Sci 106(1):172–179. https://doi.org/10.1093/toxsci/kfn152
doi: 10.1093/toxsci/kfn152
pubmed: 18667523
pmcid: 2721666
Bosnjak Kuharic D, Kekin I, Hew J, Rojnic Kuzman M, Puljak L (2019) Interventions for prodromal stage of psychosis. Cochrane Database Syst Rev 2019(11):CD012236. https://doi.org/10.1002/14651858.CD012236.pub2
doi: 10.1002/14651858.CD012236.pub2
pubmed: 31689359
pmcid: 6823626
Braff DL (2010) Prepulse inhibition of the startle reflex: a window on the brain in schizophrenia. Curr Top Behav Neurosci 4:349–371. https://doi.org/10.1007/7854_2010_61
doi: 10.1007/7854_2010_61
pubmed: 21312406
Braff DL, Geyer MA (1990) Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatry 47(2):181–188. https://doi.org/10.1001/archpsyc.1990.01810140081011
doi: 10.1001/archpsyc.1990.01810140081011
pubmed: 2405807
Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156(2-3):234–258. https://doi.org/10.1007/s002130100810
doi: 10.1007/s002130100810
pubmed: 11549226
Bubeníková-Valesová V, Horácek J, Vrajová M, Höschl C (2008) Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 32(5):1014–1023. https://doi.org/10.1016/j.neubiorev.2008.03.012
doi: 10.1016/j.neubiorev.2008.03.012
pubmed: 18471877
Căpățînă OO, Micluția IV, Fadgyas-Stănculete M (2021) Current perspectives in treating negative symptoms of schizophrenia: a narrative review. Exp Ther Med 21(3):276. https://doi.org/10.3892/etm.2021.9707
doi: 10.3892/etm.2021.9707
pubmed: 33603883
pmcid: 7851661
Castle DJ, Wessely S, Murray RM (1993) Sex and schizophrenia: effects of diagnostic stringency, and associations with and premorbid variables. Br J Psychiatry 162:658–664. https://doi.org/10.1192/bjp.162.5.658
doi: 10.1192/bjp.162.5.658
pubmed: 8149118
Catts VS, Lai YL, Weickert CS, Weickert TW, Catts SV (2016) A quantitative review of the postmortem evidence for decreased cortical N-methyl-D-aspartate receptor expression levels in schizophrenia: how can we link molecular abnormalities to mismatch negativity deficits? Biol Psychol 116:57–67. https://doi.org/10.1016/j.biopsycho.2015.10.013
doi: 10.1016/j.biopsycho.2015.10.013
pubmed: 26549579
Célia Moreira Borella V, Seeman MV, Carneiro Cordeiro R, Vieira dos Santos J, Matos R, de Souza M, de Sousa N, Fernandes E, Santos Monte A, Maria Mendes Vasconcelos S, Quinn JP, de Lucena DF, Carvalho AF, Macêdo D (2016) Gender and estrous cycle influences on behavioral and neurochemical alterations in adult rats neonatally administered ketamine. Dev Neurobiol 76(5):519–532. https://doi.org/10.1002/dneu.22329
doi: 10.1002/dneu.22329
pubmed: 26215537
Ceskova E, Prikryl R, Libiger J, Svancara J, Jarkovsky J (2015) Gender differences in the treatment of first-episode schizophrenia: results from the european first episode schizophrenia trial. Schizophr Res 169(1-3):303–307. https://doi.org/10.1016/j.schres.2015.10.013
doi: 10.1016/j.schres.2015.10.013
pubmed: 26545298
Chan KN, Chang WC, Ng CM, Lee HC, Chan SI, Chiu SY, Wong CF, Wo SF, Lee HM, Chan KW, Wong MC, Chan KL, Yeung WS, Chan CWH, Choy LW, Chong SY, Siu MW, Lo TL, Yan WC et al (2022) Sex differences in symptom severity, cognition and psychosocial functioning among individuals with at-risk mental state for psychosis. Early Interv Psychiatry 16(1):61–68. https://doi.org/10.1111/eip.13131
doi: 10.1111/eip.13131
pubmed: 33590717
Chavez C, Hollaus M, Scarr E, Pavey G, Gogos A, van den Buuse M (2010) The effect of estrogen on dopamine and serotonin receptor and transporter levels in the brain: an autoradiography study. Brain Res 1321:51–59. https://doi.org/10.1016/j.brainres.2009.12.093
doi: 10.1016/j.brainres.2009.12.093
pubmed: 20079719
Clancy B, Finlay BL, Darlington RB, Anand KJ (2007) Extrapolating brain development from experimental species to humans. Neurotoxicology 28(5):931–937. https://doi.org/10.1016/j.neuro.2007.01.014
doi: 10.1016/j.neuro.2007.01.014
pubmed: 17368774
Coley AA, Gao WJ (2018) PSD95: A synaptic protein implicated in schizophrenia or autism? Prog Neuropsychopharmacol Biol Psychiatry 82:187–194. https://doi.org/10.1016/j.pnpbp.2017.11.016
doi: 10.1016/j.pnpbp.2017.11.016
pubmed: 29169997
Colwell CS, Cepeda C, Crawford C, Levine MS (1998) Postnatal development of glutamate receptor-mediated responses in the neostriatum. Dev Neurosci 20(2-3):154–163. https://doi.org/10.1159/000017310
doi: 10.1159/000017310
pubmed: 9691190
De Koning MB, Bloemen OJ, Van Duin ED, Booij J, Abel KM, De Haan L, Linszen DH, Van Amelsvoort TA (2014) Pre-pulse inhibition and striatal dopamine in subjects at an ultra-high risk for psychosis. J Psychopharmacol 28(6):553–560. https://doi.org/10.1177/0269881113519507
doi: 10.1177/0269881113519507
pubmed: 24526133
du Bois TM, Huang XF, Deng C (2008) Perinatal administration of PCP alters adult behaviour in female Sprague-Dawley rats. Behav Brain Res 188(2):416–419. https://doi.org/10.1016/j.bbr.2007.11.017
doi: 10.1016/j.bbr.2007.11.017
pubmed: 18177952
Duncan GE, Moy SS, Lieberman JA, Koller BH (2006) Typical and atypical antipsychotic drug effects on locomotor hyperactivity and deficits in sensorimotor gating in a genetic model of NMDA receptor hypofunction. Pharmacol Biochem Behav 85(3):481–491. https://doi.org/10.1016/j.pbb.2006.09.017
doi: 10.1016/j.pbb.2006.09.017
pubmed: 17097724
pmcid: 1861823
Farrow TF, Hunter MD, Wilkinson ID, Green RD, Spence SA (2005) Structural brain correlates of unconstrained motor activity in people with schizophrenia. Br J Psychiatry 187:481–482. https://doi.org/10.1192/bjp.187.5.481
doi: 10.1192/bjp.187.5.481
pubmed: 16260826
Galderisi S, Mucci A, Buchanan RW, Arango C (2018) Negative symptoms of schizophrenia: new developments and unanswered research questions. Lancet Psychiatry 5(8):664–677. https://doi.org/10.1016/S2215-0366(18)30050-6
doi: 10.1016/S2215-0366(18)30050-6
pubmed: 29602739
Gogos A, Nathan PJ, Guille V, Croft RJ, van den Buuse M (2006) Estrogen prevents 5-HT1A receptor-induced disruptions of prepulse inhibition in healthy women. Neuropsychopharmacology 31(4):885–889. https://doi.org/10.1038/sj.npp.1300933
doi: 10.1038/sj.npp.1300933
pubmed: 16237386
Gogos A, Sbisa AM, Sun J, Gibbons A, Udawela M, Dean B (2015) A role for estrogen in schizophrenia: clinical and preclinical findings. Int J Endocrinol 2015:615356. https://doi.org/10.1155/2015/615356
doi: 10.1155/2015/615356
pubmed: 26491441
pmcid: 4600562
Grayson B, Barnes SA, Markou A, Piercy C, Podda G, Neill JC (2016) Postnatal phencyclidine (PCP) as a neurodevelopmental animal model of schizophrenia pathophysiology and symptomatology: a review. Curr Top Behav Neurosci 29:403–428. https://doi.org/10.1007/7854_2015_403
doi: 10.1007/7854_2015_403
pubmed: 26510740
Häfner H, an der Heiden W, Behrens S, Gattaz WF, Hambrecht M, Löffler W, Maurer K, Munk-Jørgensen P, Nowotny B, Riecher-Rössler A, Stein A (1998) Causes and consequences of the gender difference in age at onset of schizophrenia. Schizophr Bull 24(1):99–113. https://doi.org/10.1093/oxfordjournals.schbul.a033317
doi: 10.1093/oxfordjournals.schbul.a033317
pubmed: 9502549
Häfner H (2019) From onset and prodromal stage to a life-long course of schizophrenia and its symptom dimensions: how sex, age, and other risk factors influence incidence and course of illness. Psychiatry J 2019:9804836. https://doi.org/10.1155/2019/9804836
doi: 10.1155/2019/9804836
pubmed: 31139639
pmcid: 6500669
Hardingham G (2019) NMDA receptor C-terminal signaling in development, plasticity, and disease. F1000Res 8:1547. https://doi.org/10.12688/f1000research.19925.1
doi: 10.12688/f1000research.19925.1
Harich S, Gross G, Bespalov A (2007) Stimulation of the metabotropic glutamate 2/3 receptor attenuates social novelty discrimination deficits induced by neonatal phencyclidine treatment. Psychopharmacology 192(4):511–519. https://doi.org/10.1007/s00213-007-0742-y
doi: 10.1007/s00213-007-0742-y
pubmed: 17318501
Harvey PD (2014) Assessing disability in schizophrenia: tools and contributors. J Clin Psychiatry 75(10):e27. https://doi.org/10.4088/JCP.13049tx5c
doi: 10.4088/JCP.13049tx5c
pubmed: 25373132
Harvey L, Boksa P (2014) Do prenatal immune activation and maternal iron deficiency interact to affect neurodevelopment and early behavior in rat offspring? Brain Behav Immun 35:144–154. https://doi.org/10.1016/j.bbi.2013.09.009
doi: 10.1016/j.bbi.2013.09.009
pubmed: 24064370
Hayes E, Gavrilidis E, Kulkarni J (2012) The role of oestrogen and other hormones in the pathophysiology and treatment of schizophrenia. Schizophr Res Treat 2012:540273. https://doi.org/10.1155/2012/540273
doi: 10.1155/2012/540273
Hsu HK, Yang RC, Shih HC, Hsieh YL, Chen UY, Hsu C (2001) Prenatal exposure of testosterone prevents SDN-POA neurons of postnatal male rats from apoptosis through NMDA receptor. J Neurophysiol 86(5):2374–2380. https://doi.org/10.1152/jn.2001.86.5.2374
doi: 10.1152/jn.2001.86.5.2374
pubmed: 11698527
Iaccarino HF, Suckow RF, Xie S, Bucci DJ (2013) The effect of transient increases in kynurenic acid and quinolinic acid levels early in life on behavior in adulthood: implications for schizophrenia. Schizophr Res 150(2-3):392–397. https://doi.org/10.1016/j.schres.2013.09.004
doi: 10.1016/j.schres.2013.09.004
pubmed: 24091034
Kaar SJ, Natesan S, McCutcheon R, Howes OD (2020) Antipsychotics: mechanisms underlying clinical response and side-effects and novel treatment approaches based on pathophysiology. Neuropharmacology 172:107704. https://doi.org/10.1016/j.neuropharm.2019.107704
doi: 10.1016/j.neuropharm.2019.107704
pubmed: 31299229
Kahn RS, Sommer IE, Murray RM, Meyer-Lindenberg A, Weinberger DR, Cannon TD, O'Donovan M, Correll CU, Kane JM, van Os J, Insel TR (2015) Schizophrenia. Nat Rev Dis Primers 1:15067. https://doi.org/10.1038/nrdp.2015.67
doi: 10.1038/nrdp.2015.67
pubmed: 27189524
Kapur S, VanderSpek SC, Brownlee BA, Nobrega JN (2003) Antipsychotic dosing in preclinical models is often unrepresentative of the clinical condition: a suggested solution based on in vivo occupancy. J Pharmacol Exp Ther 305(2):625–631. https://doi.org/10.1124/jpet.102.046987
doi: 10.1124/jpet.102.046987
pubmed: 12606608
Karlsen AS, Kaalund SS, Møller M, Plath N, Pakkenberg B (2013) Expression of presynaptic markers in a neurodevelopmental animal model with relevance to schizophrenia. Neuroreport 24(16):928–933. https://doi.org/10.1097/WNR.0000000000000030
doi: 10.1097/WNR.0000000000000030
pubmed: 24045778
Kight KE, McCarthy MM (2020) Androgens and the developing hippocampus. Biol Sex Differ 11(1):30. https://doi.org/10.1186/s13293-020-00307-6
doi: 10.1186/s13293-020-00307-6
pubmed: 32487149
pmcid: 7268439
Kinkead B, Dobner PR, Egnatashvili V, Murray T, Deitemeyer N, Nemeroff CB (2005) Neurotensin-deficient mice have deficits in prepulse inhibition: restoration by clozapine but not haloperidol, olanzapine, or quetiapine. J Pharmacol Exp Ther 315(1):256–264. https://doi.org/10.1124/jpet.105.087437
doi: 10.1124/jpet.105.087437
pubmed: 15987829
Kinon BJ, Roychowdhury SM, Milton DR, Hill AL (2001) Effective resolution with olanzapine of acute presentation of behavioral agitation and positive psychotic symptoms in schizophrenia. J Clin Psychiatry 62(Suppl 2):17–21
pubmed: 11232746
Kishi T, Moriwaki M, Kitajima T, Kawashima K, Okochi T, Fukuo Y, Furukawa O, Naitoh H, Fujita K, Iwata N (2010) Effect of aripiprazole, risperidone, and olanzapine on the acoustic startle response in Japanese chronic schizophrenia. Psychopharmacology 209(2):185–190. https://doi.org/10.1007/s00213-010-1787-x
doi: 10.1007/s00213-010-1787-x
pubmed: 20177883
Kjaerby C, Bundgaard C, Fejgin K, Kristiansen U, Dalby NO (2013) Repeated potentiation of the metabotropic glutamate receptor 5 and the alpha 7 nicotinic acetylcholine receptor modulates behavioural and GABAergic deficits induced by early postnatal phencyclidine (PCP) treatment. Neuropharmacology 72:157–168. https://doi.org/10.1016/j.neuropharm.2013.04.041
doi: 10.1016/j.neuropharm.2013.04.041
pubmed: 23643744
Kjaerby C, Hovelsø N, Dalby NO, Sotty F (2017) Phencyclidine administration during neurodevelopment alters network activity in prefrontal cortex and hippocampus in adult rats. J Neurophysiol 118(2):1002–1011. https://doi.org/10.1152/jn.00081.2017
doi: 10.1152/jn.00081.2017
pubmed: 28539393
pmcid: 5539451
Kristiansen LV, Beneyto M, Haroutunian V, Meador-Woodruff JH (2006) Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia. Mol Psychiatry 11(8):737–705. https://doi.org/10.1038/sj.mp.4001844
doi: 10.1038/sj.mp.4001844
pubmed: 16702973
Laviola G, Marco EM (2011) Passing the knife edge in adolescence: brain pruning and specification of individual lines of development. Neurosci Biobehav Rev 35(8):1631–1633. https://doi.org/10.1016/j.neubiorev.2011.05.011
doi: 10.1016/j.neubiorev.2011.05.011
pubmed: 21645542
Latysheva NV, Rayevsky KS (2003) Chronic neonatal N-methyl-D-aspartate receptor blockade induces learning deficits and transient hypoactivity in young rats. Prog Neuropsychopharmacol Biol Psychiatry 27(5):787–794. https://doi.org/10.1016/S0278-5846(03)00110-6
doi: 10.1016/S0278-5846(03)00110-6
pubmed: 12921911
Le Pen G, Jay TM, Krebs MO (2011) Effect of antipsychotics on spontaneous hyperactivity and hypersensitivity to MK-801-induced hyperactivity in rats prenatally exposed to methylazoxymethanol. J Psychopharmacol 25(6):822–835. https://doi.org/10.1177/0269881110387839
doi: 10.1177/0269881110387839
pubmed: 21088043
Lewis DA, González-Burgos G (2008) Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology 33(1):141–165. https://doi.org/10.1038/sj.npp.1301563
doi: 10.1038/sj.npp.1301563
pubmed: 17805309
Li C, Tang Y, Yang J, Zhang X, Liu Y, Tang A (2016) Sub-chronic antipsychotic drug administration reverses the expression of neuregulin 1 and ErbB4 in a cultured MK801-induced mouse primary hippocampal neuron or a neurodevelopmental schizophrenia model. Neurochem Res 41(8):2049–2064. https://doi.org/10.1007/s11064-016-1917-x
doi: 10.1007/s11064-016-1917-x
pubmed: 27097547
Lim AL, Taylor DA, Malone DT (2012) A two-hit model: behavioural investigation of the effect of combined neonatal MK-801 administration and isolation rearing in the rat. J Psychopharmacol 26(9):1252–1264. https://doi.org/10.1177/0269881111430751
doi: 10.1177/0269881111430751
pubmed: 22361477
Liu F, Zou X, Sadovova N, Zhang X, Shi L, Guo L, Qian F, Wen Z, Patterson TA, Hanig JP, Paule MG, Slikker W Jr, Wang C (2011) Changes in gene expression after phencyclidine administration in developing rats: a potential animal model for schizophrenia. Int J Dev Neurosci 29(3):351–358. https://doi.org/10.1016/j.ijdevneu.2010.07.234
doi: 10.1016/j.ijdevneu.2010.07.234
pubmed: 20691775
Locklear MN, Cohen AB, Jone A, Kritzer MF (2016) Sex differences distinguish intracortical glutamate receptor-mediated regulation of extracellular dopamine levels in the prefrontal cortex of adult rats. Cereb Cortex 26(2):599–610. https://doi.org/10.1093/cercor/bhu222
doi: 10.1093/cercor/bhu222
pubmed: 25260707
Ludewig K, Geyer MA, Vollenweider FX (2003) Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia. Biol Psychiatry 54(2):121–128. https://doi.org/10.1016/s0006-3223(02)01925-x
doi: 10.1016/s0006-3223(02)01925-x
pubmed: 12873801
Luine V, Serrano P, Frankfurt M (2018) Rapid effects on memory consolidation and spine morphology by estradiol in female and male rodents. Horm Behav 104:111–118. https://doi.org/10.1016/j.yhbeh.2018.04.007
doi: 10.1016/j.yhbeh.2018.04.007
pubmed: 29669258
pmcid: 6274598
Maia TV, Frank MJ (2017) An integrative perspective on the role of dopamine in schizophrenia. Biol Psychiatry 81(1):52–66. https://doi.org/10.1016/j.biopsych.2016.05.021
doi: 10.1016/j.biopsych.2016.05.021
pubmed: 27452791
McGrath J, Saha S, Chant D, Welham J (2008) Schizophrenia: a concise overview of incidence, prevalence, and mortality. Epidemiol Rev 30:67–76. https://doi.org/10.1093/epirev/mxn001
doi: 10.1093/epirev/mxn001
pubmed: 18480098
Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J (2008) Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 22(4):469–486. https://doi.org/10.1016/j.bbi.2007.09.012
doi: 10.1016/j.bbi.2007.09.012
pubmed: 18023140
Mncube K, Harvey BH (2022) Bio-behavioural changes in treatment-resistant socially isolated FSL rats show variable or improved response to combined fluoxetine-olanzapine versus olanzapine treatment. IBRO Neurosci Rep 13:284–298. https://doi.org/10.1016/j.ibneur.2022.08.009
doi: 10.1016/j.ibneur.2022.08.009
pubmed: 36204253
pmcid: 9529672
Mateos-Aparicio P, Rodríguez-Moreno A (2020) Calcium dynamics and synaptic plasticity. Adv Exp Med Biol 1131:965–984. https://doi.org/10.1007/978-3-030-12457-1_38
doi: 10.1007/978-3-030-12457-1_38
pubmed: 31646541
Mendrek A, Mancini-Marïe A (2016) Sex/gender differences in the brain and cognition in schizophrenia. Neurosci Biobehav Rev 67:57–78. https://doi.org/10.1016/j.neubiorev.2015.10.013
doi: 10.1016/j.neubiorev.2015.10.013
pubmed: 26743859
Milenkovic M, Mielnik CA, Ramsey AJ (2014) NMDA receptor-deficient mice display sexual dimorphism in the onset and severity of behavioural abnormalities. Genes Brain Behav 13(8):850–862. https://doi.org/10.1111/gbb.12183
doi: 10.1111/gbb.12183
pubmed: 25327402
Miller TJ, McGlashan TH, Rosen JL, Cadenhead K, Ventura J, McFarlane W, Perkins DO, Pearlson GD, Woods SW (2003) Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophr Bull 29:703–715. https://doi.org/10.1093/oxfordjournals.schbul.a007040
doi: 10.1093/oxfordjournals.schbul.a007040
pubmed: 14989408
Mizrahi R, Rusjan P, Agid O, Graff A, Mamo DC, Zipursky RB, Kapur S (2007) Adverse subjective experience with antipsychotics and its relationship to striatal and extrastriatal D2 receptors: a PET study in schizophrenia. Am J Psychiatry 164(4):630–637. https://doi.org/10.1176/ajp.2007.164.4.630
doi: 10.1176/ajp.2007.164.4.630
pubmed: 17403977
Moghaddam B (2003) Bringing order to the glutamate chaos in schizophrenia. Neuron 40(5):881–884. https://doi.org/10.1016/s0896-6273(03)00757-8
doi: 10.1016/s0896-6273(03)00757-8
pubmed: 14659087
Möller HJ (2016) The relevance of negative symptoms in schizophrenia and how to treat them with psychopharmaceuticals? Psychiatr Danub 28(4):435–440
pubmed: 27855437
Morrens M, Hulstijn W, Sabbe B (2007) Psychomotor slowing in schizophrenia. Schizophr Bull 33(4):1038–1053. https://doi.org/10.1093/schbul/sbl051
doi: 10.1093/schbul/sbl051
pubmed: 17093141
Nakatani-Pawlak A, Yamaguchi K, Tatsumi Y, Mizoguchi H, Yoneda Y (2009) Neonatal phencyclidine treatment in mice induces behavioral, histological and neurochemical abnormalities in adulthood. Biol Pharm Bull 32(9):1576–1583. https://doi.org/10.1248/bpb.32.1576
doi: 10.1248/bpb.32.1576
pubmed: 19721235
Nudmamud-Thanoi S, Reynolds GP (2004) The NR1 subunit of the glutamate/NMDA receptor in the superior temporal cortex in schizophrenia and affective disorders. Neurosci Lett 372(1-2):173–177. https://doi.org/10.1016/j.neulet.2004.09.035
doi: 10.1016/j.neulet.2004.09.035
pubmed: 15531111
Okamoto M, Katayama T, Suzuki Y, Hoshino K-Y, Yamada H, Matsuoka N, Jodo E (2012) Neonatal administration of phencyclidine decreases the number of putative inhibitory interneurons and increases neural excitability to auditory paired clicks in the hippocampal CA3 region of freely moving adult mice. Neuroscience 224:268–281. https://doi.org/10.1016/j.neuroscience.2012.08.013
doi: 10.1016/j.neuroscience.2012.08.013
pubmed: 22906477
Owen MJ, Sawa A, Mortensen PB (2016) Schizophrenia. Lancet 388(10039):86–97. https://doi.org/10.1016/S0140-6736(15)01121-6
doi: 10.1016/S0140-6736(15)01121-6
pubmed: 26777917
pmcid: 4940219
Pallier PN, Ferrara M, Romagnolo F, Ferretti MT, Soreq H, Cerase A (2022) Chromosomal and environmental contributions to sex differences in the vulnerability to neurological and neuropsychiatric disorders: Implications for therapeutic interventions. Prog Neurobiol 219:102353. https://doi.org/10.1016/j.pneurobio.2022.102353
doi: 10.1016/j.pneurobio.2022.102353
pubmed: 36100191
Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9(12):947–957. https://doi.org/10.1038/nrn2513
doi: 10.1038/nrn2513
pubmed: 19002191
pmcid: 2762785
Pınar N, Akillioglu K, Sefil F, Alp H, Sagir M, Acet A (2015) Effect of clozapine on locomotor activity and anxiety-related behavior in the neonatal mice administered MK-801. Bosn J Basic Med Sci 15(3):74–79. https://doi.org/10.17305/bjbms.2015.472
doi: 10.17305/bjbms.2015.472
pubmed: 26295298
pmcid: 4594329
Quednow BB, Frommann I, Berning J, Kühn KU, Maier W, Wagner M (2008) Impaired sensorimotor gating of the acoustic startle response in the prodrome of schizophrenia. Biol Psychiatry 64(9):766–773. https://doi.org/10.1016/j.biopsych.2008.04.019
doi: 10.1016/j.biopsych.2008.04.019
pubmed: 18514166
Quinn R (2005) Comparing rat's to human's age: how old is my rat in people years? Nutrition 21(6):775–777. https://doi.org/10.1016/j.nut.2005.04.002
doi: 10.1016/j.nut.2005.04.002
pubmed: 15925305
Rajagopal L, Soni D, Meltzer HY (2018) Neurosteroid pregnenolone sulfate, alone, and as augmentation of lurasidone or tandospirone, rescues phencyclidine-induced deficits in cognitive function and social interaction. Behav Brain Res 350:31–43. https://doi.org/10.1016/j.bbr.2018.05.005
doi: 10.1016/j.bbr.2018.05.005
pubmed: 29763637
Rao H, Jean A, Kessler JP (1997) Postnatal ontogeny of glutamate receptors in the rat nucleus tractus solitarii and ventrolateral medulla. J Auton Nerv Syst 65(1):25–32. https://doi.org/10.1016/s0165-1838(97)00031-3
doi: 10.1016/s0165-1838(97)00031-3
pubmed: 9258869
Rasmussen BA, O'Neil J, Manaye KF, Perry DC, Tizabi Y (2007) Long-term effects of developmental PCP administration on sensorimotor gating in male and female rats. Psychopharmacology 190(1):43–49. https://doi.org/10.1007/s00213-006-0584-z
doi: 10.1007/s00213-006-0584-z
pubmed: 17047931
Rietschel L, Lambert M, Karow A, Zink M, Müller H, Heinz A, de Millas W, Janssen B, Gaebel W, Schneider F, Naber D, Juckel G, Krüger-Özgürdal S, Wobrock T, Wagner M, Maier W, Klosterkötter J, Bechdolf A, PREVENT study group (2017) Clinical high risk for psychosis: gender differences in symptoms and social functioning. Early Interv Psychiatry 11(4):306–313. https://doi.org/10.1111/eip.12240
doi: 10.1111/eip.12240
pubmed: 25808791
Rodríguez G, Neugebauer NM, Yao KL, Meltzer HY, Csernansky JG, Dong H (2017) Δ9-tetrahydrocannabinol (Δ9-THC) administration after neonatal exposure to phencyclidine potentiates schizophrenia-related behavioral phenotypes in mice. Pharmacol Biochem Behav 159:6–11. https://doi.org/10.1016/j.pbb.2017.06.010
doi: 10.1016/j.pbb.2017.06.010
pubmed: 28648819
Rueter LE, Ballard ME, Gallagher KB, Basso AM, Curzon P, Kohlhaas KL (2004) Chronic low dose risperidone and clozapine alleviate positive but not negative symptoms in the rat neonatal ventral hippocampal lesion model of schizophrenia. Psychopharmacology 176(3-4):312–319. https://doi.org/10.1007/s00213-004-1897-4
doi: 10.1007/s00213-004-1897-4
pubmed: 15179541
Sams-Dodd F (1998) Effects of continuous D-amphetamine and phencyclidine administration on social behaviour, stereotyped behaviour, and locomotor activity in rats. Neuropsychopharmacology 19(1):18–25. https://doi.org/10.1016/S0893-133X(97)00200-5
doi: 10.1016/S0893-133X(97)00200-5
pubmed: 9608573
Sams-Dodd F (1999) Phencyclidine in the social interaction test: an animal model of schizophrenia with face and predictive validity. Rev Neurosci 10(1):59–90. https://doi.org/10.1515/revneuro.1999.10.1.59
doi: 10.1515/revneuro.1999.10.1.59
pubmed: 10356992
Sano W, Nakamura T, Yoshiuchi K, Kitajima T, Tsuchiya A, Esaki Y, Yamamoto Y, Iwata N (2012) Enhanced persistency of resting and active periods of locomotor activity in schizophrenia. PloS One 7(8):e43539. https://doi.org/10.1371/journal.pone.0043539
doi: 10.1371/journal.pone.0043539
pubmed: 22952701
pmcid: 3429496
Sinclair D, Purves-Tyson TD, Allen KM, Weickert CS (2014) Impacts of stress and sex hormones on dopamine neurotransmission in the adolescent brain. Psychopharmacology 231(8):1581–1599. https://doi.org/10.1007/s00213-013-3415-z
doi: 10.1007/s00213-013-3415-z
pubmed: 24481565
pmcid: 3967083
Selemon LD, Zecevic N (2015) Schizophrenia: a tale of two critical periods for prefrontal cortical development. Transl Psychiatry 5(8):e623. https://doi.org/10.1038/tp.2015.115
doi: 10.1038/tp.2015.115
pubmed: 26285133
pmcid: 4564568
Snedocor GW, Cochran WC (1967) Statistical Methods, 6th edn. Iowa State University Press
Spear LP (2013) Adolescent neurodevelopment. J Adolesc Health 52(2 Suppl 2):S7–S13. https://doi.org/10.1016/j.jadohealth.2012.05.006
doi: 10.1016/j.jadohealth.2012.05.006
pubmed: 23332574
pmcid: 3982854
Snyder MA, Gao WJ (2020) NMDA receptor hypofunction for schizophrenia revisited: Perspectives from epigenetic mechanisms. Schizophr Res 217:60–70. https://doi.org/10.1016/j.schres.2019.03.010
doi: 10.1016/j.schres.2019.03.010
Swerdlow NR, Hartman PL, Auerbach PP (1997) Changes in sensorimotor inhibition across the menstrual cycle: implications for neuropsychiatric disorders. Biol Psychiatry 41(4):452–460. https://doi.org/10.1016/S0006-3223(96)00065-0
doi: 10.1016/S0006-3223(96)00065-0
pubmed: 9034539
Tandon R, Nasrallah HA, Keshavan MS (2009) Schizophrenia, “just the facts” 4. Clinical features and conceptualization. Schizophr Res 110:1–23. https://doi.org/10.1016/j.schres.2009.03.005
doi: 10.1016/j.schres.2009.03.005
pubmed: 19328655
Tendilla-Beltrán H, Meneses-Prado S, Vázquez-Roque RA, Tapia-Rodríguez M, Vázquez-Hernández AJ, Coatl-Cuaya H, Martín-Hernández D, MacDowell KS, Garcés-Ramírez L, Leza JC, Flores G (2019) Risperidone ameliorates prefrontal cortex neural atrophy and oxidative/nitrosative stress in brain and peripheral blood of rats with neonatal ventral hippocampus lesion. J Neurosci 39(43):8584–8599. https://doi.org/10.1523/JNEUROSCI.1249-19.2019
doi: 10.1523/JNEUROSCI.1249-19.2019
pubmed: 31519825
pmcid: 6807277
Togay B, Çıkrıkçılı U, Bayraktaroglu Z, Uslu A, Noyan H, Üçok A (2020) Lower prepulse inhibition in clinical high-risk groups but not in familial risk groups for psychosis compared with healthy controls. Early Interv Psychiatry 14(2):196–202. https://doi.org/10.1111/eip.12845
doi: 10.1111/eip.12845
pubmed: 31264797
Turetsky BI, Calkins ME, Light GA, Olincy A, Radant AD, Swerdlow NR (2007) Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull 33(1):69–94. https://doi.org/10.1093/schbul/sbl060
doi: 10.1093/schbul/sbl060
pubmed: 17135482
Uno Y, Coyle JT (2019) Glutamate hypothesis in schizophrenia. Psychiatry Clin Neurosci 73(5):204–215. https://doi.org/10.1111/pcn.12823
doi: 10.1111/pcn.12823
pubmed: 30666759
Van den Eynde K, Missault S, Fransen E, Raeymaekers L, Willems R, Drinkenburg W, Timmermans JP, Kumar-Singh S, Dedeurwaerdere S (2014) Hypolocomotive behaviour associated with increased microglia in a prenatal immune activation model with relevance to schizophrenia. Behav Brain Res 258:179–186. https://doi.org/10.1016/j.bbr.2013.10.005
doi: 10.1016/j.bbr.2013.10.005
pubmed: 24129217
Van den Buuse M, Low JK, Kwek P, Martin S, Gogos A (2017) Selective enhancement of NMDA receptor-mediated locomotor hyperactivity by male sex hormones in mice. Psychopharmacology 234(18):2727–2735. https://doi.org/10.1007/s00213-017-4668-8
doi: 10.1007/s00213-017-4668-8
pubmed: 28674745
Van Rijn S, Aleman A, de Sonneville L, Sprong M, Ziermans T, Schothorst P, van Engeland H, Swaab H (2011) Neuroendocrine markers of high risk for psychosis: salivary testosterone in adolescent boys with prodromal symptoms. Psychol Med 41(9):1815–1822. https://doi.org/10.1017/S0033291710002576
doi: 10.1017/S0033291710002576
pubmed: 21251344
Walder DJ, Holtzman CW, Addington J, Cadenhead K, Tsuang M, Cornblatt B, Cannon TD, McGlashan TH, Woods SW, Perkins DO, Seidman LJ, Heinssen R, Walker EF (2013) Sexual dimorphisms and prediction of conversion in the NAPLS psychosis prodrome. Schizophr Res 144(1-3):43–50. https://doi.org/10.1016/j.schres.2012.11.039
doi: 10.1016/j.schres.2012.11.039
pubmed: 23340377
pmcid: 4045468
Wadenberg ML, Soliman A, VanderSpek SC, Kapur S (2001) Dopamine D(2) receptor occupancy is a common mechanism underlying animal models of antipsychotics and their clinical effects. Neuropsychopharmacology 25(5):633–641. https://doi.org/10.1016/S0893-133X(01)00261-5
doi: 10.1016/S0893-133X(01)00261-5
pubmed: 11682246
Wang C, McInnis J, West JB, Bao J, Anastasio N, Guidry JA, Ye Y, Salvemini D, Johnson KM (2003) Blockade of phencyclidine-induced cortical apoptosis and deficits in prepulse inhibition by M40403, a superoxide dismutase mimetic. J Pharmacol Exp Ther 304(1):266–271. https://doi.org/10.1124/jpet.102.041798
doi: 10.1124/jpet.102.041798
pubmed: 12490600
Wang JX, Furukawa H (2019) Dissecting diverse functions of NMDA receptors by structural biology. Curr Opin Struct Biol 54:34–42. https://doi.org/10.1016/j.sbi.2018.12.009
doi: 10.1016/j.sbi.2018.12.009
pubmed: 30703613
pmcid: 6592722
Wang X, Bell IM, Uslaner JM (2020) Activators of α7 nAChR as potential therapeutics for cognitive impairment. Curr Top Behav Neurosci 45:209–245. https://doi.org/10.1007/7854_2020_140
doi: 10.1007/7854_2020_140
pubmed: 32451955
Wang Y, Ma Y, Hu J, Cheng W, Jiang H, Zhang X, Li M, Ren J, Li X (2015) Prenatal chronic mild stress induces depression-like behavior and sex-specific changes in regional glutamate receptor expression patterns in adult rats. Neuroscience 301:363–374. https://doi.org/10.1016/j.neuroscience.2015.06.008
doi: 10.1016/j.neuroscience.2015.06.008
pubmed: 26071959
Wegrzyn D, Juckel G, Faissner A (2022) Structural and functional deviations of the hippocampus in schizophrenia and schizophrenia animal models. Int J Mol Sci 23(10):5482. https://doi.org/10.3390/ijms23105482
doi: 10.3390/ijms23105482
pubmed: 35628292
pmcid: 9143100
Weinberger DR (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44(7):660–669. https://doi.org/10.1001/archpsyc.1987.01800190080012
doi: 10.1001/archpsyc.1987.01800190080012
pubmed: 3606332
Wickens MM, Bangasser DA, Briand LA (2018) Sex differences in psychiatric disease: a focus on the glutamate system. Front Mol Neurosci 11:197. https://doi.org/10.3389/fnmol.2018.00197
doi: 10.3389/fnmol.2018.00197
pubmed: 29922129
pmcid: 5996114
Wu YC, Hill RA, Gogos A, van den Buuse M (2013) Sex differences and the role of estrogen in animal models of schizophrenia: interaction with BDNF. Neuroscience 239:67–83. https://doi.org/10.1016/j.neuroscience.2012.10.024
doi: 10.1016/j.neuroscience.2012.10.024
pubmed: 23085218
Zhang T, Wang J, Xu L, Wei Y, Tang X, Hu Y, Cui H, Tang Y, Li C, Ling Z, Wang J (2022) Further evidence that antipsychotic medication does not prevent long-term psychosis in higher-risk individuals. Eur Arch Psychiatry Clin Neurosci 272(4):591–602. https://doi.org/10.1007/s00406-021-01331-2
doi: 10.1007/s00406-021-01331-2
pubmed: 34536114
Ziermans TB, Schothorst PF, Sprong M, Magnée MJ, van Engeland H, Kemner C (2012) Reduced prepulse inhibition as an early vulnerability marker of the psychosis prodrome in adolescence. Schizophr Res 134(1):10–15. https://doi.org/10.1016/j.schres.2011.10.009
doi: 10.1016/j.schres.2011.10.009
pubmed: 22085828