Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring

Brain, Behavior, and Immunity

Volumn 24, Issue 6, 2010, Pages 930-941

  Ito, Hiroshi T ^a   Smith, Stephen E P ^a   Hsiao, Elaine ^a   Patterson, Paul H ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Dopamine; Hippocampus; Poly(I:C); Schizophrenia; Temporoammonic pathway

Indexed keywords

POLYINOSINIC POLYCYTIDYLIC ACID; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; IMMEDIATE EARLY GENE; IMMUNOSTIMULATION; INFORMATION PROCESSING; MOUSE; NONHUMAN; ONCOGENE C FOS; PATHOGENESIS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; TASK PERFORMANCE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED; COGNITION; DRUG EFFECTS; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; HIPPOCAMPAL CA1 REGION; IMMUNITY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; IN VITRO STUDY; MAZE TEST; METABOLISM; NERVE CELL NETWORK; ONCOGENE; PATHOLOGY; PHYSIOLOGY; PREGNANCY; RECOGNITION; SYNAPSE;

ANIMALS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; COGNITION; DOPAMINE; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENES, FOS; HIPPOCAMPUS; IMMUNITY; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MICE; MICE, INBRED C57BL; NERVE NET; POLY I-C; PREGNANCY; PYRAMIDAL CELLS; RECOGNITION (PSYCHOLOGY); SCHIZOPHRENIA; SYNAPSES; IN VITRO TECHNIQUES;

EID: 77954212567     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.03.004     Document Type: Article

References (97)

1. Anderson M.I., Jeffery K.J. Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 2003, 23:8827-8835.
2. Ang C.W., Carlson G.C., Coulter D.A. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J. Neurosci. 2005, 25:9567-9580.
3. Angrist B., Vankammen D.P. CNS stimulants as tools in the study of schizophrenia. Trends Neurosci. 1984, 7:388-390.
4. Benes F.M., Khan Y., Vincent S.L., Wickramasinghe R. Differences in the subregional and cellular distribution of GABAA receptor binding in the hippocampal formation of schizophrenic brain. Synapse 1996, 22:338-349.
5. Benes F.M., Wickramasinghe R., Vincent S.L., Khan Y., Todtenkopf M. Uncoupling of GABA(A) and benzodiazepine receptor binding activity in the hippocampal formation of schizophrenic brain. Brain Res. 1997, 755:121-129.
6. Bertolino A., Blasi G. The genetics of schizophrenia. Neuroscience 2009, 164:288-299.
7. Boulougouris V., Castane A., Robbins T.W. Dopamine D2/D3 receptor agonist quinpirole impairs spatial reversal learning in rats: investigation of D3 receptor involvement in persistent behavior. Psychopharmacology (Berlin) 2009, 202:611-620.
8. Boyer P., Phillips J.L., Rousseau F.L., Ilivitsky S. Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res. Rev. 2007, 54:92-112.
9. Brown A.S., Vinogradov S., Kremen W.S., Poole J.H., Deicken R.F., Penner J.D., McKeague I.W., Kochetkova A., Kern D., Schaefer C.A. Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am. J. Psychiatry 2009, 166:683-690.
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. Browning M.D., Dudek E.M., Rapier J.L., Leonard S., Freedman R. Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics. Biol. Psychiatry 1993, 34:529-535.
12. Brun V.H., Otnass M.K., Molden S., Steffenach H.A., Witter M.P., Moser M.B., Moser E.I. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296:2243-2246.
13. Burmeister M., McInnis M.G., Zollner S. Psychiatric genetics: progress amid controversy. Nat. Rev. Genet. 2008, 9:527-540.
14. Cajal S.R.Y. Histologie du Systeme nerveux de l'hommes et des vertebres 1911, Maloine, Paris.
15. Cole A.J., Saffen D.W., Baraban J.M., Worley P.F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 1989, 340:474-476.
16. Cotter D., Wilson S., Roberts E., Kerwin R., Everall I.P. Increased dendritic MAP2 expression in the hippocampus in schizophrenia. Schizophr. Res. 2000, 41:313-323.
17. Creese I., Burt D.R., Snyder S.H. Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 1976, 192:481-483.
18. Crider A. Perseveration in schizophrenia. Schizophr. Bull. 1997, 23:63-74.
19. Danion J.M., Rizzo L., Bruant A. Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. Arch. Gen. Psychiatry 1999, 56:639-644.
20. Davidsson P., Gottfries J., Bogdanovic N., Ekman R., Karlsson I., Gottfries C.G., Blennow K. The synaptic-vesicle-specific proteins rab3a and synaptophysin are reduced in thalamus and related cortical brain regions in schizophrenic brains. Schizophr. Res. 1999, 40:23-29.
21. Davis K.L., Kahn R.S., Ko G., Davidson M. Dopamine in schizophrenia: a review and reconceptualization. Am. J. Psychiatry 1991, 148:1474-1486.
22. Davis J.O., Phelps J.A., Bracha H.S. Prenatal development of monozygotic twins and concordance for schizophrenia. Schizophr. Bull. 1995, 21:357-366.
23. Doniger G.M., Foxe J.J., Murray M.M., Higgins B.A., Javitt D.C. Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch. Gen. Psychiatry 2002, 59:1011-1020.
24. Dudman J.T., Tsay D., Siegelbaum S.A. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 2007, 56:866-879.
25. Dvorak-Carbone H., Schuman E.M. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J. Neurophysiol. 1999, 82:3213-3222.
26. Dwork A.J. Postmortem studies of the hippocampal formation in schizophrenia. Schizophr. Bull. 1997, 23:385-402.
27. Eastwood S.L., Harrison P.J. Decreased synaptophysin in the medial temporal lobe in schizophrenia demonstrated using immunoautoradiography. Neuroscience 1995, 69:339-343.
28. El-Ghundi M., Fletcher P.J., Drago J., Sibley D.R., O'Dowd B.F., George S.R. Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur. J. Pharmacol. 1999, 383:95-106.
29. Fey E.T. The performance of young schizophrenics and young normals on the Wisconsin Card Sorting Test. J. Consult. Psychol. 1951, 15:311-319.
30. Floresco S.B., Zhang Y., Enomoto T. Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res. 2008.
31. Gasbarri A., Sulli A., Innocenzi R., Pacitti C., Brioni J.D. Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat. Neuroscience 1996, 74:1037-1044.
32. Gasbarri A., Sulli A., Packard M.G. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 1997, 21:1-22.
33. Golan H.M., Lev V., Hallak M., Sorokin Y., Huleihel M. Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 2005, 48:903-917.
34. Gottesman I.I. Schizophrenia Genesis: The Origins of Madness 1991, W.H. Freeman & Company, NY, New York.
35. Guzowski J.F., Timlin J.A., Roysam B., McNaughton B.L., Worley P.F., Barnes C.A. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 2005, 15:599-606.
36. Hargreaves E.L., Rao G., Lee I., Knierim J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
37. Harrison P.J. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999, 122(Pt 4):593-624.
38. Harrison P.J., Eastwood S.L. Neuropathological studies of synaptic connectivity in the hippocampal formation in schizophrenia. Hippocampus 2001, 11:508-519.
39. Heckers S., Konradi C. Hippocampal neurons in schizophrenia. J. Neural Transm. 2002, 109:891-905.
40. Horvitz J.C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 2000, 96:651-656.
41. Huang Y.Y., Kandel E.R. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc. Natl. Acad. Sci. USA 1995, 92:2446-2450.
42. Ibi D., Nagai T., Kitahara Y., Mizoguchi H., Koike H., Shiraki A., Takuma K., Kamei H., Noda Y., Nitta A., Nabeshima T., Yoneda Y., Yamada K. Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci. Res. 2009, 64:297-305.
43. Ihalainen J.A., Riekkinen P., Feenstra M.G. Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci. Lett. 1999, 277:71-74.
44. Ito H.T., Schuman E.M. Frequency-dependent gating of synaptic transmission and plasticity by dopamine. Front. Neural Circuits 2007, 1:1.
45. Jarsky T., Roxin A., Kath W.L., Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2005, 8:1667-1676.
46. Khan Z.U., Gutierrez A., Martin R., Penafiel A., Rivera A., De La Calle A. Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain. J. Comp. Neurol. 1998, 402:353-371.
47. Kim S.M., Frank L.M. Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS One 2009, 4:e5494.
48. Knierim J.J., Lee I., Hargreaves E.L. Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 2006, 16:755-764.
49. Knight R. Contribution of human hippocampal region to novelty detection. Nature 1996, 383:256-259.
50. Law A.J., Weickert C.S., Hyde T.M., Kleinman J.E., Harrison P.J. Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines. Am. J. Psychiatry 2004, 161:1848-1855.
51. Li S., Cullen W.K., Anwyl R., Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat. Neurosci. 2003, 6:526-531.
52. Lieberman J.A., Kane J.M., Alvir J. Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology (Berlin) 1987, 91:415-433.
53. Lipska B.K., Jaskiw G.E., Weinberger D.R. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 1993, 9:67-75.
54. Lisman J.E., Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005, 46:703-713.
55. Manns J.R., Eichenbaum H. Evolution of declarative memory. Hippocampus 2006, 16:795-808.
56. Meador-Woodruff J.H., Grandy D.K., Van Tol H.H., Damask S.P., Little K.Y., Civelli O., Watson S.J. Dopamine receptor gene expression in the human medial temporal lobe. Neuropsychopharmacology 1994, 10:239-248.
57. Mednick S.A., Machon R.A., Huttunen M.O., Bonett D. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch. Gen. Psychiatry 1988, 45:189-192.
58. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., Yee B.K., Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 2006, 26:4752-4762.
59. Meyer U., Feldon J. Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia. Psychopharmacology (Berlin) 2009, 206:587-602.
60. Meyer U., Feldon J., Fatemi S.H. In vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33. 2009, 1061-1079.
61. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 1991, 14:421-451.
62. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 1984, 11:47-60.
63. Nakashiba T., Young J.Z., McHugh T.J., Buhl D.L., Tonegawa S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319:1260-1264.
64. Nelson M.D., Saykin A.J., Flashman L.A., Riordan H.J. Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch. Gen. Psychiatry 1998, 55:433-440.
65. Nolan J.D. A within-subjects analysis of discrimination shift behavior in schizophrenics. J. Abnorm. Psychol. 1974, 83:497-511.
66. Okubo Y., Suhara T., Suzuki K., Kobayashi K., Inoue O., Terasaki O., Someya Y., Sassa T., Sudo Y., Matsushima E., Iyo M., Tateno Y., Toru M. Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET. Nature 1997, 385:634-636.
67. Otmakhova N.A., Lisman J.E. D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 1996, 16:7478-7486.
68. Otmakhova N.A., Lisman J.E. Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J. Neurosci. 1999, 19:1437-1445.
69. Ozawa K., Hashimoto K., Kishimoto T., Shimizu E., Ishikura H., Iyo M. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol. Psychiatry 2006, 59:546-554.
70. Patterson P.H. Maternal effects on schizophrenia risk. Science 2007, 318:576-577.
71. Patterson P.H. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav. Brain Res. 2009, 204:313-324.
72. Redish A.D., Touretzky D.S. The role of the hippocampus in solving the Morris water maze. Neural Comput. 1998, 10:73-111.
73. Remondes M., Schuman E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416:736-740.
74. Remondes M., Schuman E.M. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 2004, 431:699-703.
75. Rizzo L., Danion J.M., Van Der Linden M., Grangé D., Rohmer J.G. Impairment of memory for spatial context in schizophrenia. Neuropsychology 1996, 10:376-384.
76. Rossato J.I., Bevilaqua L.R., Izquierdo I., Medina J.H., Cammarota M. Dopamine controls persistence of long-term memory storage. Science 2009, 325:1017-1020.
77. Rutishauser U., Mamelak A.N., Schuman E.M. Single-trial learning of novel stimuli by individual neurons of the human hippocampus-amygdala complex. Neuron 2006, 49:805-813.
78. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 1998, 80:1-27.
79. Shi L., Fatemi S.H., Sidwell R.W., Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003, 23:297-302.
80. Smith S.E., 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.
81. Steward O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 1976, 167:285-314.
82. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
83. Swanson L. The limbic region I. The Septohippocampal System. Handbook of Chemical Neuroanatomy 1987, Elsevier, Amsterdam, pp. 125-227.
84. Talamini L.M., Meeter M. Dominance of objects over context in a mediotemporal lobe model of schizophrenia. PLoS One 2009, 4:e6505.
85. Tamamaki N., Nojyo Y. Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats. J. Comp. Neurol. 1995, 353:379-390.
86. Toda M., Abi-Dargham A. Dopamine hypothesis of schizophrenia: making sense of it all. Curr. Psychiatry Rep. 2007, 9:329-336.
87. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
88. Ungerleider L.G., Haxby J.V. 'What' and 'where' in the human brain. Curr. Opin. Neurobiol. 1994, 4:157-165.
89. van Groen T., Miettinen P., Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 2003, 13:133-149.
90. Vuillermot S., Weber L., Feldon J., Meyer U. A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J. Neurosci. 2010, 30:1270-1287.
91. Wamsley J.K., Gehlert D.R., Filloux F.M., Dawson T.M. Comparison of the distribution of D-1 and D-2 dopamine receptors in the rat brain. J. Chem. Neuroanat. 1989, 2:119-137.
92. Weinberger D., Laruelle M. Neurochemical and neuropharmacological imaging in schizophrenia. Neuropsychopharmacology 2001, Lippincott Williams & Wilkins, Philadelphia.
93. Whishaw I.Q., Tomie J.A. Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus 1997, 7:361-370.
94. Witter M.P., Amaral D.G. Hippocampal formation. The Rat Nervous System 2004, Elsevier Academic Press, Amsterdam.
95. Wynn J.K., Green M.F., Engel S., Korb A., Lee J., Glahn D., Nuechterlein K.H., Cohen M.S. Increased extent of object-selective cortex in schizophrenia. Psychiatry Res. 2008, 164:97-105.
96. Young C.E., Arima K., Xie J., Hu L., Beach T.G., Falkai P., Honer W.G. SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cereb. Cortex 1998, 8:261-268.
97. Zuckerman L., Weiner I. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J. Psychiatr. Res. 2005, 39:311-323.