Evaluating negative-symptom-like behavioural changes in developmental models of schizophrenia

European Neuropsychopharmacology

Volumn 24, Issue 5, 2014, Pages 774-787

  Moser, Paul ^a  

^a INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

Animal models; Developmental models; Negative symptoms; Schizophrenia

Indexed keywords

GLUTATHIONE; METHYLAZOXYMETHANOL; NERVE GROWTH FACTOR; POLYINOSINIC POLYCYTIDYLIC ACID;

ARTICLE; BEHAVIOR CHANGE; BRAIN DEVELOPMENT; COGNITIVE DEFECT; DISEASE MODEL; FETAL MALNUTRITION; GENOTYPE ENVIRONMENT INTERACTION; HIPPOCAMPUS; INFECTION; NEGATIVE SYNDROME; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; SCHIZOPHRENIA; SOCIAL INTERACTION; SOCIAL ISOLATION; SYMPTOMATOLOGY; ANIMAL; ANIMAL BEHAVIOR; BRAIN; GROWTH, DEVELOPMENT AND AGING; HUMAN; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PSYCHOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; NEUROPSYCHOLOGICAL TESTS; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SOCIAL BEHAVIOR;

EID: 84899893626     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2013.11.004     Document Type: Article

References (107)

1. Abazyan B., Nomura J., Kannan G., Ishizuka K., Tamashiro K.L., Nucifora F., Pogorelov V., Ladenheim B., Yang C., Krasnova I.N., Cadet J.L., Pardo C., Mori S., Kamiya A., Vogel M.W., Sawa A., Ross C.A., Pletnikov M.V. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol. Psychiatry 2010, 68:1172-1181.
2. Becker A., Greksch G., Bernstein H.-G., Höllt V., Bogerts B. Social behaviour in rats lesioned with ibotenic acid in the hippocampus: quantitative and qualitative analysis. Psychopharmacology 1999, 144:333-338.
3. Bitanihirwe B.K.Y., Pelag-Raibstein D., Mouttet F., Feldon J., Meyer U. Late prenatal immune activation in mice leads to behavioural and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 2010, 35:2462-2478.
4. Blas-Valdivia V., Cano-Europa E., Hernandez-Garcia A., Ortiz-Butron R. Neonatal bilateral lidocaine administration into the ventral hippocampus caused postpubertal behavioral changes: an animal model of neurodevelopmental psychopathological disorders. Neuropsychiatric Dis. Treat. 2009, 5:15-22.
5. Boksa P. Animal models of obstetric complications in relation to schizophrenia. Brain Res. Rev. 2004, 45:1-17.
6. Brady A.M., McCallum S.E., Glick S.D., O'Donnell P. Enhanced methamphetamine self-administration in a neurodevelopmental rat model of schizophrenia. Psychopharmacology 2008, 200:205-215.
7. Branchi I., Santucci D., Vitale A., Alleva E. Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Dev. Psychobiol. 1998, 33:249-256.
8. Brandon N.J., Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat. Rev. Neurosci. 2011, 12:707-722.
9. Brenes J.C., Fornaguera J. The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behav. Brain Res. 2009, 198:199-205.
10. Brown A.S., Derkits E.J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 2010, 167:261-280.
11. Brown J.W., Whitehead C.A., Basso A.M., Rueter L.E., Zhang M. Pre-clinical evaluation of non-imidazole histamine H3 receptor antagonists in comparison to atypical antipsychotics for the treatment of cognitive deficits associated with schizophrenia. Int. J. Neuropsychopharmacol. 2012, 21:1-16.
12. Castagné V., Rougemont M., Cuenod M., Do K.Q. Low brain glutathione and ascorbic acid associated with dopamine uptake inhibition during rat's development induce long-term cognitive deficit: relevance to schizophrenia. Neurobiol. Dis. 2004, 15:93-105.
13. Castagné V., Cuenod M., Do K.Q. An animal model with relevance to schizophrenia: sex-dependent cognitive deficits in osteogenic disorder-Shionogi rats induced by glutathione synthesis and dopamine uptake inhibition during development. Neuroscience 2004, 123:821-834.
14. Castagné V., Moser P.C., Porsolt R.D. Preclinical behavioural models for predicting antipsychotic activity. Adv. Pharmacol. 2009, 57:381-418.
15. Castagné, V., Moser, P., Roux, S., Porsolt, R.D., 2011. Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Curr. Protoc. Neurosci. Chapter 8:Unit 8.10A.
16. Cattabeni F., Di Luca M. Developmental models of brain dysfunctions induced by targeted cellular ablations with methylazoxymethanol. Physiol. Rev. 1997, 77:199-215.
17. Chabout J., Serreau P., Ey E., Bellier L., Aubin T., Bourgeron T., Granon S. Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS One 2012, 7:e29401.
18. Clarke M.C., Harley M., Cannon M. The role of obstetric events in schizophrenia. Schizophr. Bull. 2006, 32:3-8.
19. Der-Avakian A., Markou A. The neurobiology of anhedonia and other reward related deficits. Trends Neurosci. 2012, 35:68-77.
20. Desbonnet L., O'Tuathaigh C., Clarke G., O'Leary C., Petit E., Clarke N., Tighe O., Lai D., Harvey R., Cryan J.F., Dinan T.G., Waddington J.L. Phenotypic effects of repeated psychosocial stress during adolescence in mice mutant for the schizophrenia risk gene neuregulin-1: A putative model of gene x environment interaction. Brain Behav. Immun. 2012, 26:660-671.
21. Do K.Q., Cabungcal J.H., Frank A., Stuellet P., Cuenod M. Redox dysregulation, neurodevelopment, and schizophrenia. Curr. Op. Neurobiol. 2009, 19:220-230.
22. 308/Y transgenic model of Rett Syndrome. Acta Neuropathol. 2008, 116:425-437.
23. Ellenbroek B.A., Cools A.R. Animal models for the negative symptoms of schizophrenia. Behav. Pharmacol. 2000, 11:223-233.
24. Eyles D., Feldon J., Meyer U. Schizophrenia: do all roads lead to dopamine or is this where they start? Evidence from two epidemiologically informed developmental rodent models. Transl. Psychiatry 2012, 2:e81.
25. Fatemi S.H., Folsom T.D. The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr. Bull. 2009, 35:528-548.
26. File S.E., Hyde J.R. Can social interaction be used to measure anxiety? Br. J. Pharmacol. 1978, 62:19-24.
27. File S.E., Seth P. A review of 25 years of the social interaction test. Eur. J. Pharmacol. 2003, 463:35-53.
28. Flagstad P., Mork A., Glenthoj B.Y., van Beek J., Michael-Titus A.T., Didriksen M. Disruption of neurogenesis on gestational day 17 in the rat causes behavioral changes relevant to positive and negative schizophrenia symptoms and alters amphetamine-induced dopamine release in nucleus accumbens. Neuropsychopharmacology 2004, 29:2052-2064.
29. Fone K.C.F., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-Relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev. 2008, 32:1087-1102.
30. Foussias G., Remington G. Negative symptoms in schizophrenia: Avolition and Occam's razor. Schizophr. Bull. 2010, 36:359-369.
31. Gandal M.J., Edgar J.C., Klook K., Siegal S.J. Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 2012, 62:1504-1518.
32. Geoffroy P.A., Etain B., Houenou J. Gene x environment interactions in schizophrenia and bipolar disorder: evidence from neuroimaging. Front. Psychiat. 2013, 4:136.
33. Gastambide F., Cotel M.C., Gilmour G., O'Neill M.J., Robbins T.J., Tricklebank M.D. Selective remediation of reversal learning deficits in the neurodevelopmental MAM model of schizophrenia by a novel mGlu5 positive allosteric modulator. Neuropsychopharmacology 2012, 37:1057-1066.
34. Ghajarnia M., Moore H., Grace A.A. Enhanced behavioural effects of phencyclidine in rats with developmental abnormalities of the temporal lobe. Soc. Neurosci. Abstr. 1998, 24:2177.
35. Gorbachevskaya N., Bashina V., Gratchev V., Iznak A. Cerebrolysin therapy in Rett Syndrome: clinical and EEG mapping. Brain Dev. 2001, 23:S90-S93.
36. Gourevitch R., Rocher C., Le Pen G., Krebs M.O., Jay T.M. Working memory deficits in adult rats after prenatal disruption of neurogenesis. Behav. Pharmacol. 2004, 15:287-292.
37. Grabrucker A.M. Environmental factors in autism. Front. Psychiatr. 2012, 3:118.
38. Guillemot J., Lukaszewski M.A., Montel V., Delahaye F., Mayeur S., Laborie C., Dickes-Coopman A., Dutriez-Casteloot I., Lesage J., Breton C., Vieau D. Influence of prenatal undernutrition on the effects of clozapine and aripiprazole in the adult male rats: relevance to a neurodevelopmental origin of schizophrenia? Eur. J. Pharmacol. 2011, 667:402-409.
39. Harms L.R., Eyles D.W., McGrath J.J., Mackay-Sim A., Burne T.H.J. Developmental vitamin D deficiency alters adult behaviour in 129/SvJ and C57BL/6J mice. Behav. Brain Res. 2008, 187:343-350.
40. Harrison P.J. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999, 122:593-624.
41. Hermes G., Li N., Duman C., Duman R. Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol. Behav. 2011, 104:354-359.
42. Hida H., Mouri A., Noda Y. Behavioral phenotypes in schizophrenic animal models with multiple combinations of genetic and environmental factors. J. Pharmacol. Sci. 2013, 121:185-191.
43. Ibi D., Nagai T., Koike H., Kitahara Y., Mizoguchu H., Niwa M., Jaaro-Peled H., Nitta A., Yoneda Y., Nabeshima T., Sawa A., Yamada K. Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav. Brain Res. 2010, 206:32-37.
44. Ishihama T., Ago Y., Shintani N., Hashimoto H., Baba A., Takuma K., Matsuda T. Environmental factors during early developmental period influence psychobehavioral abnormalities in adult PACAP-deficient mice. Behav. Brain Res. 2010, 209:274-280.
45. Jaaro-Peled H., Hayashi-Takagi A., Seshadri S., Kamiya A., Brandon N.J., Sawa A. Neurodevelopmental mechanisms of schizophrenia: understanding disturbed postnatal brain maturation through neuregulin-1-ErbB4 and DISC1. TiNS 2009, 32:485-495.
46. Kirsten T.B., Taricano M., Maiorka P.C., Palermo-Neto J., Bernardi M.M. Prenatal lipopolysaccharide reduces social behaviour in male offspring. Neuroimmunomodulation 2010, n17:240-251.
47. Kirsten T.B., Chaves-Kirsten G.P., Chaible L.M., Silva A.C., Martine D.O., Britto L.R.G., Dagli M.L.Z., Torrão A.S., Palermo-Neto J., Bernardi M.M. Hypoactivity of the central dopaminergic system and autistic-like behaviour induced by a single early prenatal exposure to lipopolysaccharide. J. Neurosci. Res. 2012, 90:1903-1912.
48. Koike H., Ibi D., Mizoguchi H., Nagai T., Nitta A., Takuma K., Nabeshima T., Yoneda Y., Yamada K. Behavioral abnormality and pharmacologic response in social isolation-reared mice. Behav. Brain Res. 2009, 202:114-121.
49. Kulak A., Cuenod M., Do K.Q. Behavioral phenotyping of glutathione-deficient mice: relevance to schizophrenia and bipolar disorder. Behav. Brain Res. 2012, 226:563-570.
50. Landauer M.R., Balster R.L. A new test of social investigation in mice: effects of d-amphetamine. Psychopharmacology 1978, 78:322-325.
51. Lahvis G.P., Alleva E., Scattoni M.L. Translating mouse vocalisations: prosody and frequency modulation. Genes Brain Behav. 2011, 10:4-16.
52. Lazar N.L., Rajakumar N., Cain D.P. Injections of NGF into neonatal frontal cortex decreases social interaction as adults: a rat model of schizophrenia. Schizophr. Bull. 2008, 34:127-136.
53. Le Pen G., Gaudet L., Mortas P., Mory L., Moreau J.-L. Deficits in reward sensitivity in a neurodevelopmental rat model of schizophrenia. Psychopharmacology 2002, 161:434-441.
54. Le Pen G., Gourevitch R., Hazane F., Hoareau C., Jay T.M., Krebs M.-O. Peri-pubertal maturation after developmental disturbance: a model for psychosis onset in the rat. Neuroscience 2006, 143:395-405.
55. Lipska B.K. Using animal models to test a neurodevelopmental hypothesis of schizophrenia. Rev. Psychiatr. Neurosci. 2004, 29:282-286.
56. Lipska B.K., Weinberger D.R. Delayed effects of neonatal hippocampal damage on haloperidol-induced catalepsy and apomorphine induced stereotypic behaviors in the rat. Brain Res. Dev. Brain Res. 1993, 75:213-222.
57. Lipska B.K., Halim N.D., Segal P.N., Weinberger D.R. Effects of reversible inactivation of the neonatal ventral hippocampus on behaviour in the adult rat. J. Neurosci. 2002, 22:2835-2842.
58. Lodge D.J., Grace A.A. Gestational methylazoxymethanol acetate administration: a developmental disruption model of schizophrenia. Behav. Brain Res. 2009, 204:306-312.
59. Lukasz B., O'Sullivan N., Loscher J.S., Pickering M., Regan C.M., Murphy K.J. Peripubertal viral-like challenge and social isolation mediate overlapping but distinct effects on behaviour and brain interferon regulatory factor 7 expression in the adult Wistar rat. Brain Behav. Immun. 2013, 27:71-79.
60. Lukkes J.L., Watt M.J., Lowry C.A., Forster G.L. Consequences of post-weaning social isolation on anxiety behaviour and related neural circuits in rodents. Front Behav. Neurosci. 2009, 3:18.
61. Markou A., Salamone J.D., Bussey T.J., Mar A.C., Brunner D., Gilmour G., Balsam P. Measuring reinforcement learning and motivation constructs in experimental animals: relevance to the negative symptoms of schizophrenia. Neurosci. Biobehav. Rev. 2013, 37:2149-2165.
62. 6 receptors. Neuropharmacol 2011, 61:400-407.
63. McGrath J.J., Burne T.H., Feron F., Mackay-Sim A., Eyles D.W. Developmental vitamin D deficiency and risk of schizophrenia: a 10-year update. Schizphr. Bull. 2010, 36:1073-1078.
64. Meng Q., Li N., Han X., Shao F., Wang W. Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neurosci. Lett. 2010, 480:25-29.
65. Meyer U. Developmental neuroinflammation and schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 42:20-34.
66. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog. Neurobiol. 2010, 90:285-326.
67. Millan M.J. An epigenetic framework for neurodevelopmental disorders: from pathogenesis to potential therapy. Neuropharmacology 2013, 68:2-82.
68. Miller B.J., Culpepper N., Rapoport M.H., Buckley P. Prenatal inflammation and neurodevelopment in schizophrenia: a review of human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 42:92-100.
69. Mittal V.A., Ellman L.M., Cannon T.D. Gene-environment interactions and covariation in schizophrenia. The role of obstetric complications. Schizophr. Bull. 2008, 34:1083-1094.
70. Miyamoto S., Miyake N., Jarskog L.F., Fleischhacker W.W., Lieberman J.A. Pharmacological treatment of schizophrenia: a critical review of the pharmacology and clinical effects of current and future therapeutic agents. Mol. Psychiatry 2012, 17:1206-1227.
71. Murray R.M., Lappin J., Di Forti M. Schizophrenia: From developmental deviance to dopamine dysregulation. Eur. Neuropsychopharmacol. 2008, 18:S129-S134.
72. Naert A., Gantois I., Laeremans A., Vreysen S., Van den Bergh G., Arckens L., Callaerts-Vegh Z., D'Hooge R. Behavioural alterations relevant to developmental brain disorders in mice with neonatally induced ventral hippocampal lesions. Brain Res. Bull. 2013, 94:71-81.
73. Nagai T., Kitahara Y., Ibi D., Nabeshima T., Sawa A., Yamada K. Effects of antipsychotics on the behavioral deficits in human dominant-negative DISC1 transgenic mice with neonatal polyI:C treatment. Behav. Brain Res. 2011, 225:305-310.
74. Nagai T., Yu J., Kitahara Y., Nabeshima T., Yamada K. D-serine ameliorates neonatal polyI:C treatment-induced emotional and cognitive impairments in adult mice. J. Pharmacol. Sci. 2012, 120:213-227.
75. Nipa Haque F., Lipina T.V., Roder J.C., Wong A.H.C. Social defeat interacts with Disc-1 mutations in the mouse to affect behaviour. Behav. Brain Res. 2012, 233:337-344.
76. Niwa M., Matsumoto M., Mouri A., Ozaki N., Nabeshima T. Vulnerability in early life to changes in the rearing environment plays a crucial role in the aetiopathology of psychiatric disorders. Int. J. Neuropsychopharmacol. 2011, 14:459-477.
77. O'Donnell P. Cortical disinhibition in the neonatal ventral hippocampal lesion model of schizophrenia: New vistas on possible therapeutic approaches. Pharmacol. Ther. 2012, 133:19-25.
78. Olivier B., Mos J. Rodent models of aggressive behaviour and serotonergic drugs. Prog. Neuropsychopharmacol. Biol. Psychiatry 1992, 16:847-870.
79. Oliver P.L. Challenges of analysing gene-environment interactions in mouse models of schizophrenia. Scientific World 2011, 11:1411-1420.
80. O'Tuathaigh C.M.P., Desbonnet L., Waddington J.L. Mutant mouse models in evaluating novel approaches to antipsychotic treatment. Novel antipsychotic treatments. Handbook Exp. Pharmacol. 2012, 213:113-154.
81. O'Tuathaigh C.M.P., Kirby B.P., Moran P.M., Waddington J.L. Mutant mouse models: genotype-phenotype relationships to negative symptoms in schizophrenia. Schizophr. Bull. 2010, 36:271-288.
82. Rajakumar N., Leung L.S., Ma J., Rajakumar B., Rushlow W. Altered neurotrophin receptor function in the developing prefrontal cortex leads to adult-onset dopaminergic hyperresponsivity and impaired prepulse inhibition of acoustic startle. Biol. Psychiatry 2004, 55:797-803.
83. Rapoport J.L., Giedd J.N., Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol. Psychiatry 2012, 17:1228-1238.
84. Rehn A.E., Van Den Buuse M., Copolov D., Briscoe T., Lambert G., Rees S. An animal model of chronic placental insufficiency: relevance to neurodevelopmental disorders including schizophrenia. Neuroscience 2004, 129:381-391.
85. Rueter L.E., Ballard M.E., Gallagher K.B., Basso A.M., Curzon P., Kohlhass K.L. Chronic low dose risperidone and clozapine alleviate positive but not negative symptoms in the rat neonatal ventral hippocampal lesion model of schizophrenia. Psychopharmacology 2004, 176:312-319.
86. Sams-Dodd F., Lipska B.K., Weinberger D.R. Neonatal lesions of the ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology 1997, 132:303-310.
87. Scattoni M.L., Crawley J., Ricceri L. Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci. Biobehav. Rev. 2009, 33:508-515.
88. Schwendener S., Meyer U., Feldon J. Deficient maternal care resulting from immunological stress during pregnancy is associated with a sex-dependent enhancement of conditioned fear in the offspring. J. Neurodev. Disord. 2009, 1:15-32.
89. Shi L., Fatemi S.H., Sidwell R.W., Patterson P.H. Maternal influenza infection causes marked behavioural and pharmacological changes in the offspring. J. Neurosci. 2003, 23:297-302.
90. Silva-Gomez A.B., Bermudez M., Quirion R., Srivastava L.K., Picazo O., Flores G. Comparative behavioral changes between male and female postpubertal rats following neonatal excitotoxic lesions of the ventral hippocampus. Brain Res. 2003, 973:285-292.
91. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nature Rev. Neurosci. 2010, 11:490-502.
92. Smith S.E.P., Li J., Garbett K., Mirnics K., Patterson P.H. Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 2007, 27:10695-10702.
93. Susser E., Neugebauer R., Hoek H.W., Brown A.S., Lin S., Labovitz D., Gorman J.M. Schizophrenia after prenatal famine. Further evidence. Arch. Gen. Psychiatry 1996, 53:25-31.
94. Svrakic D.M., Zorumski C.F., Svrakic N.M., Zwir I., Cloninger C.R. Risk architecture of schizophrenia: the role of epigenetics. Curr. Op. Psychiatry 2013, 26:188-195.
95. Swanson J.W., Swartz M.S., Van Dorn R.A., Elbogen E.B., Wagner H.R., Rosenheck R.A., Stroup T.S., McEvoy J.P., Lieberman J.A. A national study of violent behavior in persons with schizophrenia. Arch. Gen. Psychiatry 2006, 63:490-499.
96. Talamini L.M., Koch T., Ter Horst G.J., Korf J. Methylazoxymethanol acetate induced abnormalities in the entorhinal cortex of the rat; parallels with morphological findings in schizophrenia. Brain Res. 1998, 789:293-306.
97. Tandon R., Keshaven M.S., Nasrallah H.A. Schizophrenia, "just the facts" what we know in 2008. 2. Epidemiology and etiology. Schizophr. Res. 2008, 102:1-18.
98. Tseng K.Y., Chambers R.A., Lipska B.K. The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav. Brain Res. 2009, 204:295-305.
99. Tsuang M.T., Stone W.S., Faraone S.V. Genes, environment and schizophrenia. Br. J. Psychiatry 2001, 40:s18-s24.
100. Vazquez-Roque R.A., Ramos B., Tecuatl C., Juarez I., Adame A., de la Cruz F., Zamudio S., Mena R., Rockenstein E., Masliah E., Flores G. Chronic administration of the neurotrophic agent cerebrolysin ameliorates the behavioural and morphological changes induced by neonatal ventral hippocampus lesion in a rat model of schizophrenia. J. Neurosci. Res. 2012, 90:288-306.
101. Verdoux H. Perinatal risk factors for schizophrenia: how specific are they?. Curr. Psychiatry Rep. 2004, 6:162-167.
102. Wan R.Q., Giovanni A., Kafka S.H., Corbett R. Neonatal ventral hippocampal lesions induced hyperresponsiveness to amphetamine: behavioural and in vivo microdialysis studies. Behav. Brain Res. 1996, 78:211-223.
103. Wöhr M., Schwarting R.K. Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res. 2013, 354:81-97.
104. Workman A.D., Charvet C.J., Clancy B., Darlington R.B., Finlay B.L. Modeling transformations of neurodevelopmental sequences across mammalian species. J. Neurosci. 2013, 33:7368-7383.
105. Yao J.K., Keshaven M.S. Antioxidants, redox signalling and pathophysiology in schizophrenia: an integrative view. Antiox. Redox Signal 2011, 15:2011-2035.
106. Yee N., Schwarting R.K.W., Fuchs E., Wöhr M. Increased affective ultrasonic communication during fear learning in adult male rats exposed to maternal immune activation. J. Psychiatric Res. 2012, 46:1199-1205.
107. Zamberletti E., Vigano D., Guidali C., Rubino T., Parolaro D. Long-lasting recovery of psychotic-like symptoms in isolation-reared rats after chronic but not acute treatment with the cannabinoid antagonist AM251. Int. J. Neeuropsychopharmacol. 2012, 15:267-280.