Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat

Biological Psychiatry

Volumn 70, Issue 9, 2011, Pages 842-851

  Piontkewitz, Yael ^a   Arad, Michal ^a   Weiner, Ina ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Amphetamine; developmental trajectories; latent inhibition; prenatal poly I:C; rat; schizophrenia; structural brain changes

Indexed keywords

POLYINOSINIC POLYCYTIDYLIC ACID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; FEMALE; GESTATIONAL AGE; HIPPOCAMPUS; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; LOCOMOTION; MALE; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PREFRONTAL CORTEX; PREGNANCY; PRIORITY JOURNAL; PROGENY; RAT; SEX DIFFERENCE;

AGING; AMPHETAMINE; ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; DATA INTERPRETATION, STATISTICAL; DOPAMINE UPTAKE INHIBITORS; FEMALE; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; LATERAL VENTRICLES; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; PHENOTYPE; POLY I-C; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX CHARACTERISTICS; STARTLE REACTION;

EID: 80054007975     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.06.007     Document Type: Article

References (81)

1. N. Gogtay, N.S. Vyas, R. Testa, S.J. Wood, and C. Pantelis Age of onset of schizophrenia: Perspectives from structural neuroimaging studies Schizophr Bull 37 2011 504 513
2. T. Paus, M. Keshavan, and J.N. Giedd Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9 2008 947 957
3. V.A. Mittal, L.M. Ellman, and T.D. Cannon Gene-environment interaction and covariation in schizophrenia: The role of obstetric complications Schizophr Bull 34 2008 1083 1094
4. D.A. Lewis, and P. Levitt Schizophrenia as a disorder of neurodevelopment Annu Rev Neurosci 25 2002 409 432 (Pubitemid 34748023)
5. J. Savitz, and W.C. Drevets Bipolar and major depressive disorder: Neuroimaging the developmental-degenerative divide Neurosci Biobehav Rev 33 2009 699 771
6. T. Tenyi, M. Trixler, and G. Csabi Minor physical anomalies in affective disorders A review of the literature J Affect Disord 112 2009 11 18
7. A.S. Brown, and E.J. Derkits Prenatal infection and schizophrenia: A review of epidemiologic and translational studies Am J Psychiatry 167 2010 261 280
8. P.J. Harrison, and D.R. Weinberger Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence Mol Psychiatry 10 2005 40 68 (Pubitemid 40139588)
9. T.R. Insel Rethinking schizophrenia Nature 468 2010 187 193
10. B.L. Thompson, and P. Levitt The clinical-basic interface in defining pathogenesis in disorders of neurodevelopmental origin Neuron 67 2010 702 712
11. F. Fumagalli, R. Molteni, G. Racagni, and M.A. Riva Stress during development: Impact on neuroplasticity and relevance to psychopathology Prog Neurobiol 81 2007 197 217 (Pubitemid 46498900)
12. M. Weinstock The long-term behavioural consequences of prenatal stress Neurosci Biobehav Rev 32 2008 1073 1086
13. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies Biol Psychiatry 49 2001 1023 1039 (Pubitemid 32595461)
14. R.A. Machon, S.A. Mednick, and M.O. Huttunen Adult major affective disorder after prenatal exposure to an influenza epidemic Arch Gen Psychiatry 54 1997 322 328 (Pubitemid 27171917)
15. A. Sacker, D.J. Done, T.J. Crow, and J. Golding Antecedents of schizophrenia and affective illness Obstetric complications Br J Psychiatry 166 1995 734 741
16. M. Sanches, M.S. Keshavan, P. Brambilla, and J.C. Soares Neurodevelopmental basis of bipolar disorder: A critical appraisal Prog Neuropsychopharmacol Biol Psychiatry 32 2008 1617 1627
17. B.L. Thompson, and P. Levitt Now you see it, now you don'tClosing in on allostasis and developmental basis of psychiatric disorders Neuron 65 2010 437 439
18. T.D. Cannon, T.G. van Erp, C.E. Bearden, R. Loewy, P. Thompson, and A.W. Toga Early and late neurodevelopmental influences in the prodrome to schizophrenia: Contributions of genes, environment, and their interactions Schizophr Bull 29 2003 653 669 (Pubitemid 38181948)
19. H. Jaaro-Peled, A. Hayashi-Takagi, S. Seshadri, A. Kamiya, N.J. Brandon, and A. Sawa Neurodevelopmental mechanisms of schizophrenia: Understanding disturbed postnatal brain maturation through neuregulin-1-ErbB4 and DISC1 Trends Neurosci 32 2009 485 495
20. C. Pantelis, M. Yucel, E. Bora, A. Fornito, R. Testa, and W.J. Brewer Neurobiological markers of illness onset in psychosis and schizophrenia: The search for a moving target Neuropsychol Rev 19 2009 385 398
21. R. Smieskova, P. Fusar-Poli, P. Allen, K. Bendfeldt, R.D. Stieglitz, and J. Drewe Neuroimaging predictors of transition to psychosisA systematic review and meta-analysis Neurosci Biobehav Rev 34 2010 1207 1222
22. U. Rao, L.A. Chen, A.S. Bidesi, M.U. Shad, M.A. Thomas, and C.L. Hammen Hippocampal changes associated with early-life adversity and vulnerability to depression Biol Psychiatry 67 2010 357 364
23. M. Berk, F. Kapczinski, A.C. Andreazza, O.M. Dean, F. Giorlando, and M. Maes Pathways underlying neuroprogression in bipolar disorder: Focus on inflammation, oxidative stress and neurotrophic factors Neurosci Biobehav Rev 35 2011 804 817
24. E. Bora, A. Fornito, C. Pantelis, and M. Yucel Gray matter abnormalities in major depressive disorder: A meta-analysis of voxel based morphometry studies [published online ahead of print April 19] J Affect Disord 2011
25. E. Bora, A. Fornito, M. Yucel, and C. Pantelis Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder Biol Psychiatry 67 2010 1097 1105
26. M. Niwa, A. Kamiya, R. Murai, K. Kubo, A.J. Gruber, and K. Tomita Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits Neuron 65 2010 480 489
27. M. Baharnoori, W.G. Brake, and L.K. Srivastava Prenatal immune challenge induces developmental changes in the morphology of pyramidal neurons of the prefrontal cortex and hippocampus in rats Schizophr Res 107 2009 99 109
28. K. Cui, H. Ashdown, G.N. Luheshi, and P. Boksa Effects of prenatal immune activation on hippocampal neurogenesis in the rat Schizophr Res 113 2009 288 297
29. S.H. Fatemi, T.J. Reutiman, T.D. Folsom, H. Huang, K. Oishi, and S. Mori Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: Implications for genesis of neurodevelopmental disorders Schizophr Res 99 2008 56 70
30. E. Romero, C. Guaza, B. Castellano, and J. Borrell Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: Implications for the etiopathology of schizophrenia Mol Psychiatry 15 2010 372 383
31. S. Vuillermot, L. Weber, J. Feldon, and U. Meyer A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia J Neurosci 30 2010 1270 1287
32. B. Abazyan, J. Nomura, G. Kannan, K. Ishizuka, K.L. Tamashiro, and F. Nucifora Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology Biol Psychiatry 68 2010 1172 1181
33. L. Zuckerman, M. Rehavi, R. Nachman, and I. Weiner Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: A novel neurodevelopmental model of schizophrenia Neuropsychopharmacology 28 2003 1778 1789 (Pubitemid 41070843)
34. K. Ozawa, K. Hashimoto, T. Kishimoto, E. Shimizu, H. Ishikura, and M. Iyo 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 2006 546 554 (Pubitemid 43320543)
35. U. Meyer, J. Feldon, M. Schedlowski, and B.K. Yee Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia Neurosci Biobehav Rev 29 2005 913 947 (Pubitemid 41097394)
36. P.H. Patterson Neuroscience Maternal effects on schizophrenia risk Science 318 2007 576 577 (Pubitemid 350017607)
37. U. Meyer, and J. Feldon Epidemiology-driven neurodevelopmental animal models of schizophrenia Prog Neurobiol 90 2010 285 326
38. L. Zuckerman, and I. Weiner Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring J Psychiatr Res 39 2005 311 323 (Pubitemid 40255916)
39. U. Meyer, and J. Feldon Neural basis of psychosis-related behaviour in the infection model of schizophrenia Behav Brain Res 204 2009 322 334
40. U. Meyer, and J. Feldon Prenatal exposure to infection: A primary mechanism for abnormal dopaminergic development in schizophrenia Psychopharmacology (Berl) 206 2009 587 602
41. L. Shi, S.H. Fatemi, R.W. Sidwell, and P.H. Patterson Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring J Neurosci 23 2003 297 302 (Pubitemid 36050430)
42. Y. Piontkewitz, M. Arad, and I. Weiner Risperidone administered during asymptomatic period of adolescence prevents the emergence of brain structural pathology and behavioral abnormalities in an animal model of schizophrenia [published online ahead of print May 3] Schizophr Bull 2010
43. Y. Piontkewitz, Y. Assaf, and I. Weiner Clozapine administration in adolescence prevents postpubertal emergence of brain structural pathology in an animal model of schizophrenia Biol Psychiatry 66 2009 1038 1046
44. L. Zuckerman, and I. Weiner Post-pubertal emergence of disrupted latent inhibition following prenatal immune activation Psychopharmacology (Berl) 169 2003 308 313 (Pubitemid 37255519)
45. I. Weiner The "two-headed" latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment Psychopharmacology (Berl) 169 2003 257 297 (Pubitemid 37264944)
46. M. Laruelle, A. Abi-Dargham, C.H. van Dyck, R. Gil, C.D. D'Souza, and J. Erdos Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects Proc Natl Acad Sci U S A 93 1996 9235 9240
47. C.C. Chen, Y.Y. Tung, and C. Chang A lifespan MRI evaluation of ventricular enlargement in normal aging mice [published online ahead of print February 3] Neurobiol Aging 2010
48. L. Malkova, E. Heuer, and R.C. Saunders Longitudinal magnetic resonance imaging study of rhesus monkey brain development Eur J Neurosci 24 2006 3204 3212 (Pubitemid 44952652)
49. R.C. Knickmeyer, M. Styner, S.J. Short, G.R. Lubach, C. Kang, and R. Hamer Maturational trajectories of cortical brain development through the pubertal transition: Unique species and sex differences in the monkey revealed through structural magnetic resonance imaging Cereb Cortex 20 2010 1053 1063
50. R.K. Lenroot, and J.N. Giedd Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging Neurosci Biobehav Rev 30 2006 718 729 (Pubitemid 44292283)
51. L.P. Spear The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 24 2000 417 463 (Pubitemid 30243061)
52. C.M. McCormick, and I.Z. Mathews Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory Prog Neuropsychopharmacol Biol Psychiatry 34 2010 756 765
53. H.C. Brenhouse, and S.L. Andersen Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes [published online ahead of print May 12] Neurosci Biobehav Rev 2011
54. G.L. Ming, and H. Song Adult neurogenesis in the mammalian central nervous system Annu Rev Neurosci 28 2005 223 250 (Pubitemid 41098905)
55. U. Meyer, M. Nyffeler, A. Engler, A. Urwyler, M. Schedlowski, and I. Knuesel The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology J Neurosci 26 2006 4752 4762 (Pubitemid 44315314)
56. G. Grecksch, H.G. Bernstein, A. Becker, V. Hollt, and B. Bogerts Disruption of latent inhibition in rats with postnatal hippocampal lesions Neuropsychopharmacology 20 1999 525 532 (Pubitemid 29189257)
57. K.Y. Tseng, R.A. Chambers, and B.K. Lipska The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia Behav Brain Res 204 2009 295 305
58. P. Belujon, and A.A. Grace Critical role of the prefrontal cortex in the regulation of hippocampus-accumbens information flow J Neurosci 28 2008 9797 9805
59. D.J. Lodge, and A.A. Grace Developmental pathology, dopamine, stress and schizophrenia Int J Dev Neurosci 29 2011 207 213
60. M.V. Seeman, and M. Lang The role of estrogens in schizophrenia gender differences Schizophr Bull 16 1990 185 194 (Pubitemid 20205356)
61. A.A. Walf, and C.A. Frye A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior Neuropsychopharmacology 31 2006 1097 1111 (Pubitemid 43971828)
62. C.L. Sisk, and J.L. Zehr Pubertal hormones organize the adolescent brain and behavior Front Neuroendocrinol 26 2005 163 174 (Pubitemid 41772653)
63. M. Arad, and I. Weiner Contrasting effects of increased and decreased dopamine transmission on latent inhibition in ovariectomized rats and their modulation by 17beta-estradiol: An animal model of menopausal psychosis? Neuropsychopharmacology 35 2010 1570 1582
64. M. Arad, and I. Weiner Sex-dependent antipsychotic capacity of 17β-estradiol in the latent inhibition model: A typical antipsychotic drug in both sexes, atypical antipsychotic drug in males Neuropsychopharmacology 35 2010 2179 2192
65. M.S. Keshavan, K.M. Prasad, and G. Pearlson Are brain structural abnormalities useful as endophenotypes in schizophrenia? Int Rev Psychiatry 19 2007 397 406
66. S.J. Borgwardt, P.K. McGuire, J. Aston, U. Gschwandtner, M.O. Pfluger, and R.D. Stieglitz Reductions in frontal, temporal and parietal volume associated with the onset of psychosis Schizophr Res 106 2008 108 114
67. P. Fusar-Poli, S. Borgwardt, A. Crescini, G. D'Este, M. Kempton, and S. Lawrie Neuroanatomy of vulnerability to psychosis: A voxel-based meta-analysis Neurosci Biobehav Rev 35 2010 1175 1185
68. D.E. Job, H.C. Whalley, E.C. Johnstone, and S.M. Lawrie Grey matter changes over time in high risk subjects developing schizophrenia Neuroimage 25 2005 1023 1030 (Pubitemid 40591646)
69. A.M. McIntosh, D.C. Owens, W.J. Moorhead, H.C. Whalley, A.C. Stanfield, and J. Hall Longitudinal volume reductions in people at high genetic risk of schizophrenia as they develop psychosis Biol Psychiatry 69 2011 953 958
70. D. Sun, L. Phillips, D. Velakoulis, A. Yung, P.D. McGorry, and S.J. Wood Progressive brain structural changes mapped as psychosis develops in "at risk" individuals Schizophr Res 108 2009 85 92
71. V.A. Mittal, M. Daley, M.F. Shiode, C.E. Bearden, J. O'Neill, and T.D. Cannon Striatal volumes and dyskinetic movements in youth at high-risk for psychosis Schizophr Res 123 2010 68 70
72. J.M. Stone, O.D. Howes, A. Egerton, J. Kambeitz, P. Allen, and D.J. Lythgoe Altered relationship between hippocampal glutamate levels and striatal dopamine function in subjects at ultra high risk of psychosis Biol Psychiatry 68 2010 599 602
73. P. Fusar-Poli, O.D. Howes, P. Allen, M. Broome, I. Valli, and M.C. Asselin Abnormal frontostriatal interactions in people with prodromal signs of psychosis: A multimodal imaging study Arch Gen Psychiatry 67 2010 683 691
74. S.M. Lawrie, A.M. McIntosh, J. Hall, D.G. Owens, and E.C. Johnstone Brain structure and function changes during the development of schizophrenia: The evidence from studies of subjects at increased genetic risk Schizophr Bull 34 2008 330 340 (Pubitemid 351323338)
75. L.M. Ellman, R.F. Deicken, S. Vinogradov, W.S. Kremen, J.H. Poole, and D.M. Kern Structural brain alterations in schizophrenia following fetal exposure to the inflammatory cytokine interleukin-8 Schizophr Res 121 2010 46 54
76. S.H. Fatemi, and T.D. Folsom The neurodevelopmental hypothesis of schizophrenia, revisited Schizophr Bull 35 2009 528 548
77. S.H. Fatemi, T.D. Folsom, T.J. Reutiman, H. Huang, K. Oishi, and S. Mori Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring Eur Neuropsychopharmacol 19 2009 648 653
78. P. Boksa Effects of prenatal infection on brain development and behavior: A review of findings from animal models Brain Behav Immun 24 2010 881 897
79. S.J. Short, G.R. Lubach, A.I. Karasin, C.W. Olsen, M. Styner, and R.C. Knickmeyer Maternal influenza infection during pregnancy impacts postnatal brain development in the rhesus monkey Biol Psychiatry 67 2010 965 973
80. Q. Li, C. Cheung, R. Wei, E.S. Hui, J. Feldon, and U. Meyer Prenatal immune challenge is an environmental risk factor for brain and behavior change relevant to schizophrenia: evidence from MRI in a mouse model PloS One 24 4 2009 e6354
81. R.K. Lenroot, and J.N. Giedd Sex differences in the adolescent brain Brain Cogn 72 2010 46 55