Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring

Journal of Psychiatric Research

Volumn 39, Issue 3, 2005, Pages 311-323

  Zuckerman, Lee ^a,b   Weiner, Ina ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Cytokines; Latent inhibition; Maternal immune activation; Neurodevelopment; Poly I:C; Reversal learning; Schizophrenia

Indexed keywords

CLOZAPINE; DIZOCILPINE; NEUROLEPTIC AGENT; POLYINOSINIC POLYCYTIDYLIC ACID; SYNTHETIC PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR; BEHAVIOR DISORDER; CONDITIONING; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; ENVIRONMENTAL EXPOSURE; FEMALE; IMMUNE RESPONSE; IMMUNITY; IMMUNOSTIMULATION; LATENT INHIBITION; LEARNING; LOCOMOTION; MALE; MATERNAL WELFARE; MAZE TEST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROGENY; SCHIZOPHRENIA; VIRUS;

EID: 13844276635     PISSN: 00223956     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2004.08.008     Document Type: Article

References (93)

1. W.M. Abi-Saab, D.C. D'Souza, B. Moghaddam, and J.H. Krystal The NMDAmantagonist model for schizophrenia: promise and pitfalls Pharmacopsychiatry 31 suppl 2 1998 104 109
2. W. Adams, R.E. Kendell, E.H. Hare, and P. Munk-Jorgensen Epidemiological evidence that maternal influenza contributes to the aetiology of schizophrenia. An analysis of Scottish, English, and Danish data British Journal of Psychiatry 163 1993 522 534
3. F. Anscombe The disorder of consciousness in schizophrenia Schizophrenia Bulletin 13 1987 241 260
4. J. Arnt, and T. Skarsfeldt Do novel antipsychotics have similar pharmacological characteristics. A review of the evidence Neuropsychopharmacology 18 2 1998 63 101
5. I. Baruch, D. Hemsley, and J.A.. Gray Differential performance of acute and chronic schizophrenics in a latent inhibition task Journal of Nervous and Mental Disease 176 1988 598 606
6. S.A. Bayer Development of the Hippocampal Region in the Rat - 1. Neurogenisis Examined with 3H-Thymidine Autoradiography Journal of Comparative Neurology 190 1980 87 114
7. S.A. Bayer, and J. Altman Neocortical development 1991 Raven Press New York
8. S.A. Bayer, J. Altman, R.J. Russo, X.F. Dai, and J.A.. Simmons Cell migration in the rat embryonic neocortex Journal of Comparative Neurology 307 3 1991 499 516
9. H. Beckmann Developmental malformations in cerebral structures of schizophrenic patients European Archives of Psychiatry and Clinical Neuroscience 249 Suppl 4 1999 44 47
10. B. Bogerts Recent advances in the neuropathology of schizophrenia Schizophrenia Bulletin 19 2 1993 431 445
11. J. Borrell, J.M. Vela, A. Arevalo-Martin, E. Molina-Holgado, and C. Guaza Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophrenia Neuropsychopharmacology 26 2 2002 204 215
12. A.S. Brown, P. Cohen, J. Harkavy-Friedman, V. Babulas, D. Malaspina, J.M. Gorman, and E.S. Susser Biological Psychiatry 49 6 2001 473 486
13. E. Carboni, A. Imperato, L. Perezzani, and G. Di Chiara Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats Neuroscience 28 3 1989 653 661
14. M. Carlsson, and A. Carlsson The NMDA antagonist MK-801 causes marked locomotor stimulation in monoamine-depleted mice Journal of Neural Transmission 75 3 1989 221 226
15. A. Carlsson, N. Waters, and M.L. Carlsson Neurotransmitter interactions in schizophrenia-therapeutic implications Biological Psychiatry 46 10 1999 1388 1395
16. E. Coutureau, R. Galani, O. Gosselin, M. Majchrzak, and G. Di Scala Entorhinal but not hippocampal or subicular lesions disrupt latent inhibition in rats Neurobiology of Learning and Memory 72 3 1999 143 157
17. E. Coutureau, O. Gosselin, and G. Di Scala Restoration of latent inhibition by olanzapine but not haloperidol in entorhinal cortex-lesioned rats Psychopharmacology (Berl) 150 2 2000 226 232
18. E. Coutureau, I. Lena, V. Dauge, and S.G. Di The entorhinal cortex-nucleus accumbens pathway and latent inhibition: a behavioral and neurochemical study in rats Behavioral Neuroscience 116 1 2002 95 104
19. J. Doukas, A.H. Cutler, and J.P. Mordes Polyinosinic:polycytidylic acid is a potent activator of endothelial cells American Journal of Pathology 145 1 1994 137 147
20. J.P. Druhan, H. Rajabi, and J. Stewart MK-801 increases locomotor activity without elevating extracellular dopamine levels in the nucleus accumbens Synapse 24 2 1996 135 146
21. J.A. Engel, J. Zhang, T. Bergstrom, N. Conradi, C. Forkstam, A. Liljeroth, and L. Svensson Neonatal herpes simplex virus type 1 brain infection affects the development of sensorimotor gating in rats Brain Research 863 1-2 2000 233 240
22. S.H. Fatemi, E.S. Emamian, D. Kist, R.W. Sidwell, K. Nakajima, P. Akhter, A. Shier, S. Sheikh, and K. Bailey Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice Molecular Psychiatry 4 2 1999 145 154
23. E.D. French Effects of phencyclidine on ventral tegmental A10 dopamine neurons in the rat Neuropharmacology 25 3 1986 241 248
24. E.D. French, and A.. Ceci Non-competitive N-methyl-D-aspartate antagonists are potent activators of ventral tegmental A10 dopamine neurons Neuroscience Letters 119 2 1990 159 162
25. M. Gelissen, and A.. Cools Effect of intracaudate haloperidol and apomorphine on switching motor patterns upon current behavior of cats Behavioural Brain Research 29 1988 17 26
26. J.H. Gilmore, and L.F. Jarskog Exposure to infection and brain development: cytokines in the pathogenesis of schizophrenia [letter] Schizophrenia Research 24 3 1997 365 367
27. J.A. Gray, J. Feldon, J.N.P. Rawlins, D.R. Hemsley, and A.D. Smith The neuropsychology of schizophrenia Behavioral and Brain Sciences 14 1991 1 84
28. N.S. Gray, D.R. Hemsley, and J.A.. Gray Abolition of latent inhibition by a single low dose of amphetamine in man Psychopharmacology 107 1992 425 430
29. N.S. Gray, D.R. Hemsley, and J.A. Gray Abolition of latent inhibition in acute, but not chronic schizophrenics Neurology Psychiatry and Brain Research 1 1992 83 89
30. N.S. Gray, A.D. Pickering, D.R. Hemsley, S. Dawling, and J.A.. Gray Abolition of latent inhibition by a single 5 mg dose of d-amphetamine in man Psychopharmacology 107 2-3 1992 425 430
31. W. Holt, and S. Maren Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory Journal of Neuroscience 19 20 1999 9054 9062
32. Y. Izumoto, S. Inoue, and N. Yasuda Schizophrenia and the influenza epidemics of 1957 in Japan Biological Psychiatry 46 1 1999 119 124
33. D.C. Javitt Treatment of negative and cognitive symptoms Current Psychiatry Report 1 1 1999 25 30
34. D.C. Javitt, and S.R. Zukin Recent advances in the phencyclidine model of schizophrenia American Journal of Psychiatry 148 10 1991 1301 1308
35. M.H. Joseph, S.L. Peters, P.M. Moran, G.A. Grigoryan, A.M. Young, and J.A. Gray Modulation of latent inhibition in the rat by altered dopamine transmission in the nucleus accumbens at the time of conditioning Neuroscience 101 4 2000 921 930
36. T. Katafuchi, T. Kondo, T. Yasaka, K. Kubo, S. Take, and M. Yoshimura Prolonged effects of polyriboinosinic:polyribocytidylic acid on spontaneous running wheel activity and brain interferon-alpha mRNA in rats: a model for immunologically induced fatigue Neuroscience 120 3 2003 837 845
37. M. Kimura, L.A. Toth, H. Agostini, A.B. Cady, J.A. Majde, and J.M. Krueger Comparison of acute phase responses induced in rabbits by lipopolysaccharide and double-stranded RNA American Journal of Physiology 267 1994 R1596 R1605
38. D.G. Kirch Infection and autoimmunity as etiologic factors in schizophrenia: a review and reappraisal Schizophrenia Bulletin 19 2 1993 355 370
39. H. Kunugi, S. Nanko, N. Takei, K. Saito, N. Hayashi, and H. Kazamatsuri Schizoprenia following in utero exposure to the 1957 influenza epidemics in Japan American Journal of Psychiatry 152 3 1995 450 452
40. M. Lyon Animal models of mania and schizophrenia P. Willner Behavioral models in psychopharmacology: theoretical, industrial and clinical perspectives 1991 Cambridge University Press Cambridge 253 310
41. P.A. Magaro Cognition in schizophrenia and paranoia: the integration of cognitive processes 1980 Lawrence Erlbaum Hillsdale
42. C.E. Marx, L.F. Jarskog, J.M. Lauder, J.A. Lieberman, and J.H. Gilmore Cytokine effects on cortical neuron MAP-2 immunoreactivity: implications for schizophrenia Biological Psychiatry 50 10 2001 743 749
43. R.J. McDonald, A.L. King, and N.S. Hong Context-specific interference on reversal learning of a stimulus-response habit Behavioural Brain Research 121 1-2 2001 149 165
44. D.W. Miller, and E.D. Abercrombie Effects of MK-801 on spontaneous and amphetamine-stimulated dopamine release in striatum measured with in vivo microdialysis in awake rats Brain Research Bulletin 40 1 1996 57 62
45. B. Moghaddam Bringing order to the glutamate chaos in schizophrenia Neuron 40 5 2003 881 884
46. B. Moghaddam, B. Adams, A. Verma, and D. Daly 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 Journal of Neuroscience 17 8 1997 2921 2927
47. P.C. Moser, J.M. Hitchcock, S. Lister, and P.M. Moran The pharmacology of latent inhibition as an animal model of schizophrenia Brain Research Reviews 33 2-3 2000 275 307
48. R.M. Murray, P. Jones, E. O'Callaghan, N. Takei, and P. Sham Genes, viruses and neurodevelopmental schizophrenia Journal of Psychiatric Research 26 4 1992 225 235
49. H. Nawa, M. Takahashi, and P.H. Patterson Cytokine and growth factor involvement in schizophrenia-support for the developmental model Molecular Psychiatry 5 6 2000 594 603
50. E. O'Callaghan, P.C. Sham, N. Takei, G. Murray, G. Glover, E.H. Hare, and R.M. Murray The relationship of schizophrenic births to 16 infectious diseases British Journal of Psychiatry 165 3 1994 353 356
51. R.D. Oades Attention and schizophrenia: neurobiological bases 1982 Pitman London
52. R.D. Oades The role of noradrenaline in tuning and dopamine in switching between signals in the CNS Neuroscience and Biobehavioral Reviews 9 2 1985 261 282
53. B.D. Pearce Viral mechanisms of schizophrenia M.S. Myslobodsky I Weiner Contemporary issues in modeling psychopathology 2000 Kluwer Academic Publishers New York 79 102
54. B.D. Pearce Schizophrenia and viral infection during neurodevelopment: a focus on mechanisms Molecular Psychiatry 6 6 2001 634 646
55. B.D. Pearce, N.M. Valadi, C.L. Po, and A.H. Miller Viral infection of developing GABAergic neurons in a model of hippocampal disinhibition Neuroreport 11 11 2000 2433 2438
56. S.B. Pruett, R. Fan, and Q. Zheng Acute ethanol administration profoundly alters poly I:C-induced cytokine expression in mice by a mechanism that is not dependent on corticosterone Life Science 72 16 2003 1825 1839
57. C. Rascle, O. Mazas, G. Vaiva, M. Tournant, O. Raybois, M. Goudemand, and P. Thomas Clinical features of latent inhibition in schizophrenia Schizophrenia Research 51 2-3 2001 149 161
58. D.M. Rothschild, M. O'Grady, and L. Wecker Neonatal cytomegalovirus exposure decreases prepulse inhibition in adult rats: implications for schizophrenia Journal of Neuroscience Research 57 4 1999 429 434
59. S.A. Rubin, P. Sylves, M. Vogel, M. Pletnikov, T.H. Moran, G.J. Schwartz, and K.M. Carbone Borna disease virus-induced hippocampal dentate gyrus damage is associated with spatial learning and memory deficits Brain Research Bulletin 48 1 1999 23 30
60. E. Shadach, J. Feldon, and I. Weiner Clozapine-induced potentiation of latent inhibition is due to its action in the conditioning stage: implications for the mechanism of action of antipsychotic drugs International Journal of Neuropsychopharmacology 2 1999 283 291
61. E. Shadach, I. Gaisler, D. Schiller, and I. Weiner The latent inhibition model dissociates between clozapine, haloperidol, and ritanserin Neuropsychopharmacology 23 2 2000 151 161
62. L. Shi, S.H. Fatemi, R.W. Sidwell, and P.H. Patterson Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring Journal of Neuroscience 23 1 2003 297 302
63. J.C. Snell, O. Chernyshev, D.L. Gilbert, and C.A. Colton Polyribonucleotides induce nitric oxide production by human monocyte-derived macrophages Journal of Leukocyte Biology 62 3 1997 369 373
64. N.R. Swerdlow, and G.F. Koob Dopamine, schizophrenia, mania and depression: toward a unified hypothesis of cortico-striato-pallido-thalamic function Behavioural Brain Research 10 1987 215 217
65. C.A. Tamminga Schizophrenia and glutamatergic transmission Critical Reviews in Neurobiology 12 1-2 1998 21 36
66. J.C. Thornton, S. Dawe, C. Lee, C. Capstick, P.J. Corr, P. Cotter, S. Frangou, N.S. Gray, M.A. Russell, and J.A. Gray Effects of nicotine and amphetamine on latent inhibition in human subjects Psychopharmacology (Berl) 127 2 1996 164 173
67. E.F. Torrey, R. Rawlings, and I.N. Waldman Schizophrenic births and viral diseases in two states Schizophrenia Research 1 1 1988 73 77
68. F.D. Toth, C. Juhl, N. Norskov-Lauritsen, P. Mosborg Petersen, and P. Ebbesen Interferon production by cultured human trophoblast induced with double stranded polyribonucleotide Journal of Reproductive Immunology 17 3 1990 217 227
69. D. Vaitl, and V. Lipp Latent inhibition and autonomic responses: a psycholophysiological approach Behavioral Brain Research 88 1997 85 94
70. D. Vaitl, O. Lipp, U. Bauer, G. Schuler, R. Stark, M. Zimmermann, and P. Kirsch Latent inhibition and schizophrenia: pavlovian conditioning of autonomic responses Schizophrenia Research 55 1-2 2002 147 158
71. R. Van den Bos, and A.R. Cools The involvement of the nucleus accumbens in the ability of rats to switch to cue-directed behaviors Life Science 44 1989 1697 1704
72. R.Wd. Waltrip, D.R. Carrigan, and W.T. Carpenter Jr. Immunopathology and viral reactivation. A general theory of schizophrenia Journal of Nervous and Mental Disease 178 12 1990 729 738
73. C.G. Watson, T. Kucala, C. Tilleskjor, and L. Jacobs Schizophrenic birth seasonality in relation to the incidence of infectious diseases and temperature extremes Archives of General Psychiatry 41 1 1984 85 90
74. D.R. Weinberger From neuropathology to neurodevelopment Lancet 346 8974 1995 552 557
75. I. Weiner The latent inhibition model of schizophrenia M.S. Myslobodsky I. Weiner Contemporary issues in modeling psychopathology 2000 Kluwer Academic Publishers New York 197 230
76. I. Weiner The two-headed latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment Psychopharmacology (Berl) 169 3-4 2003 257 297
77. I. Weiner, and J. Feldon Reversal and nonreversal shifts under amphetamine Psychopharmacology (Berl) 89 3 1986 355 359
78. I. Weiner, and D. Joel Dopamine in schizophrenia: dysfunctional information processing in basal ganglia-thalamocortical split circuits G. Di Chiara Handbook of experimental pharmacology. Dopamine in the CNS II 2002 Springer-Verlag Berlin 417 472
79. I. Weiner, R.E. Lubow, and J. Feldon Chronic amphetamine and latent inhibition Behavioural Brain Research 2 1981 285 286
80. I. Weiner, R.E. Lubow, and J. Feldon Abolition of the expression but not the acquisition of latent inhibition by chronic amphetamine in rats Psychopharmacology 83 1984 194 199
81. I. Weiner, E. Ben Horin, and J. Feldon Amphetamine and the overtraining reversal effect Pharmacology Biochemistry and Behavior 24 6 1986 1539 1542
82. I. Weiner, J. Feldon, and O. Ben-Shahar Simultaneous brightness discrimination and reversal: the effects of amphetamine administration in the two stages Pharmacology Biochemistry and Behavior 25 5 1986 939 942
83. I. Weiner, R.E. Lubow, and J. Feldon Disruption of latent inhibition by acute administration of low doses of amphetamine Pharmacology Biochemistry and Behavior 30 1988 871 878
84. I. Weiner, E. Shadach, R. Tarrasch, R. Kidron, and J. Feldon The latent inhibition model of schizophrenia: further validation using the atypical neuroleptic, clozapine Biological Psychiatry 40 9 1996 834 843
85. I. Weiner, E. Shadach, R. Barkai, and J. Feldon Haloperidol- and clozapine-induced enhancement of latent inhibition with extended conditioning: implications for the mechanism of action of neuroleptic drugs Neuropsychopharmacology 16 1 1997 42 50
86. R.F. Westbrook, M.L. Jones, G.K. Bailey, and J.A. Harris Contextual control over conditioned responding in a latent inhibition paradigm Journal of Experimental Psychology - Animal Behavior Process 26 2 2000 157 173
87. P. Wright, M. Gill, and R.M. Murray Schizophrenia: genetics and the maternal immune response to viral infection American Journal of Medical Genetics 48 1 1993 40 46
88. B.K. Yee, J. Feldon, and J.N.P. Rawlins Latent inhibition in rats is abolished by NMDA-induced neuronal loss in the retrohippocampal region but this lesion effect can be prevented by systemic haloperidol treatment Behavioral Neuroscience 109 1995 227 240
89. B.K. Yee, and J.N. Rawlins A comparison between the effects of medial septal lesions and entorhinal cortex lesions on performance of nonspatial working memory tasks and reversal learning Behavioural Brain Research 94 2 1998 281 300
90. H. Yogev, U. Hadar, Y. Gutman, and P. Sirota Perseveration and over-switching in schizophrenia Schizophrenia Research 61 2-3 2003 315 321
91. L. Zuckerman, S. Ben-Eliyahu, and I. Weiner Maternal Immune stimulation leads to cognitive deficits in the adult offspring which are alleviated by antipsychotic treatment: a novel neurodevelopmental model of schizophrenia in the rat European Neuropsychopharmacology 11 3 2001 246
92. 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 10 2003 1778 1789
93. L. Zuckerman, and I. Weiner Post-pubertal emergence of disrupted latent inhibition following prenatal immune activation Psychopharmacology (Berl) 169 3-4 2003 308 313