Early, time-dependent disturbances of hippocampal synaptic transmission and plasticity after in utero immune challenge

Biological Psychiatry

Volumn 70, Issue 10, 2011, Pages 992-999

  Escobar, Marion ^a   Crouzin, Nadine ^a   Cavalier, Mélanie ^a   Quentin, Julie ^a   Roussel, Julien ^a   Lanté, Fabien ^a   Batista Novais, Aline Rideau ^a   Cohen Solal, Catherine ^a   De Jesus Ferreira, Marie Céleste ^a   Guiramand, Janique ^a   Barbanel, Gérard ^a   Vignes, Michel ^a  

^a CNRS   (France)

Author keywords

CA1; long term depression (LTD); N methyl D aspartate (NMDA); neurodevelopmental disease; prenatal lipopolysaccharide (LPS); schizophrenia

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; LIPOPOLYSACCHARIDE; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; CEREBRAL PALSY; CONTROLLED STUDY; INFECTION; LEARNING DISORDER; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MENTAL DISEASE; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NEWBORN; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; RISK FACTOR; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LONG-TERM SYNAPTIC DEPRESSION; MALE; PATCH-CLAMP TECHNIQUES; POLYSACCHARIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PYRIDINES; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; VALINE;

EID: 80054946444     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.01.009     Document Type: Article

References (44)

1. T.L. Bale Is mom too sensitive? Impact of maternal stress during gestation Front Neuroendocrinol 26 2005 41 49 (Pubitemid 40602846)
2. T.L. Bale, T.Z. Baram, A.S. Brown, J.M. Goldstein, T.R. Insel, and M.M. McCarthy Early life programming and neurodevelopmental disorders Biol Psychiatry 68 2010 314 319
3. K.L. Brunson, E. Kramar, B. Lin, Y. Chen, L.L. Colgin, and T.K. Yanagihara Mechanisms of late-onset cognitive decline after early-life stress J Neurosci 25 2005 9328 9338 (Pubitemid 41464745)
4. 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
5. 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 2002 204 215 (Pubitemid 34093083)
6. M.E. Fortier, R. Joober, G.N. Luheshi, and P. Boksa Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring J Psychiatr Res 38 2004 335 345 (Pubitemid 38299172)
7. M.E. Fortier, G.N. Luheshi, and P. Boksa Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy Behav Brain Res 181 2007 270 277 (Pubitemid 46898665)
8. E. Romero, C. Ali, E. Molina-Holgado, B. Castellano, C. Guaza, and J. Borrell Neurobehavioral and immunological consequences of prenatal immune activation in rats. influence of antipsychotics Neuropsychopharmacology 32 2006 1791 1804 (Pubitemid 47076375)
9. 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
10. F. Lante, J. Meunier, J. Guiramand, M.C. De Jesus Ferreira, G. Cambonie, and R. Aimar Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation Hippocampus 18 2008 602 609 (Pubitemid 351832747)
11. F. Lanté, J. Meunier, J. Guiramand, T. Maurice, M. Cavalier, and M.C. de Jesus Ferreira Neurodevelopmental damage after prenatal infection: Role of oxidative stress in the fetal brain Free Radic Biol Med 42 2007 1231 1245 (Pubitemid 46437362)
12. G.C. Lowe, G.N. Luheshi, and S. Williams Maternal infection and fever during late gestation are associated with altered synaptic transmission in the hippocampus of juvenile offspring rats Am J Physiol Regul Integr Comp Physiol 295 2008 R1563 R1571
13. A. Roumier, O. Pascual, C. Bechade, S. Wakselman, J.C. Poncer, and E. Real Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function PLoS ONE 3 2008 e2595
14. G.H. Son, D. Geum, S. Chung, E.J. Kim, J.H. Jo, and C.M. Kim Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity J Neurosci 26 2006 3309 3318
15. G.L. Collingridge, S. Peineau, J.G. Howland, and Y.T. Wang Long-term depression in the CNS Nat Rev Neurosci 11 2010 459 473
16. N. Kemp, and Z.I. Bashir Long-term depression: A cascade of induction and expression mechanisms Prog Neurobiol 65 2001 339 365 (Pubitemid 32781668)
17. R.M. Mulkey, and R.C. Malenka Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus Neuron 9 1992 967 975
18. K.M. Huber, M.S. Kayser, and M.F. Bear Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression Science 288 2000 1254 1257
19. N. Kemp, and Z.I. Bashir NMDA receptor-dependent and -independent long-term depression in the CA1 region of the adult rat hippocampus in vitro Neuropharmacology 36 1997 397 399 (Pubitemid 27200974)
20. N. Kemp, J. McQueen, S. Faulkes, and Z.I. Bashir Different forms of LTD in the CA1 region of the hippocampus: Role of age and stimulus protocol Eur J Neurosci 12 2000 360 366 (Pubitemid 30068441)
21. V.Y. Bolshakov, and S.A. Siegelbaum Postsynaptic induction and presynaptic expression of hippocampal long-term depression Science 264 1994 1148 1152
22. S.H. Oliet, R.C. Malenka, and R.A. Nicoll Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells Neuron 18 1997 969 982 (Pubitemid 27274615)
23. F. Lanté, M. Cavalier, C. Cohen-Solal, J. Guiramand, and M. Vignes Developmental switch from LTD to LTP in low frequency-induced plasticity Hippocampus 16 2006 981 989 (Pubitemid 44857655)
24. H.Y. Ku, Y.F. Huang, P.H. Chao, C.C. Huang, and K.S. Hsu Neonatal isolation delays the developmental decline of long-term depression in the CA1 region of rat hippocampus Neuropsychopharmacology 33 2008 2847 2859
25. K. Yashiro, and B.D. Philpot Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity Neuropharmacology 55 2008 1081 1094
26. K. Williams, S.L. Russell, Y.M. Shen, and P.B. Molinoff Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro Neuron 10 1993 267 278 (Pubitemid 23079548)
27. M. Kollen, A. Stephan, A. Faivre-Bauman, C. Loudes, P.M. Sinet, and J. Alliot Preserved memory capacities in aged Lou/C/Jall rats Neurobiol Aging 31 2010 129 142
28. K. Nakazawa, M.C. Quirk, R.A. Chitwood, M. Watanabe, M.F. Yeckel, and L.D. Sun Requirement for hippocampal CA3 NMDA receptors in associative memory recall Science 297 2002 211 218 (Pubitemid 34761276)
29. S.M. Dudek, and M.F. Bear Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade Proc Natl Acad Sci U S A 89 1992 4363 4367
30. J. Zhong, D.P. Carrozza, K. Williams, D.B. Pritchett, and P.B. Molinoff Expression of mRNAs encoding subunits of the NMDA receptor in developing rat brain J Neurochem 64 1995 531 539
31. J.L. Brigman, T. Wright, G. Talani, S. Prasad-Mulcare, S. Jinde, and G.K. Seabold Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning J Neurosci 30 2010 4590 4600
32. V. Cheli, M. Adrover, C. Blanco, C. Ferrari, A. Cornea, and F. Pitossi Knocking-down the NMDAR1 subunit in a limited amount of neurons in the rat hippocampus impairs learning J Neurochem 97 2006 68 73
33. U. Meyer, M. Nyffeler, B.K. Yee, I. Knuesel, and J. Feldon Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice Brain Behav Immun 22 2008 469 486 (Pubitemid 351451821)
34. C.G. Lau, and R.S. Zukin NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders Nat Rev Neurosci 8 2007 413 426 (Pubitemid 46789232)
35. R.J. Wenthold, K. Prybylowski, S. Standley, N. Sans, and R.S. Petralia Trafficking of NMDA receptors Annu Rev Pharmacol Toxicol 43 2003 335 358 (Pubitemid 37372645)
36. F. Lante, N. Crouzin, and M. Vignes Unveiling novel forms of hippocampal synaptic plasticity with microelectrode arrays J Integr Neurosci 7 2008 249 270
37. F. Lanté, M.C. de Jesus Ferreira, J. Guiramand, M. Recasens, and M. Vignes Low-frequency stimulation induces a new form of LTP, metabotropic glutamate (mGlu(5)) receptor- and PKA-dependent, in the CA1 area of the rat hippocampus Hippocampus 16 2006 345 360 (Pubitemid 43805440)
38. Y.Y. Huang, and E.R. Kandel Low-frequency stimulation induces a pathway-specific late phase of LTP in the amygdala that is mediated by PKA and dependent on protein synthesis Learn Mem 14 2007 497 503 (Pubitemid 47204848)
39. Z.A. Bortolotto, and G.L. Collingridge Characterisation of LTP induced by the activation of glutamate metabotropic receptors in area CA1 of the hippocampus Neuropharmacology 32 1993 1 9 (Pubitemid 23016192)
40. D. Habib, and H.C. Dringenberg Low-frequency-induced synaptic potentiation: A paradigm shift in the field of memory-related plasticity mechanisms? Hippocampus 20 2010 29 35
41. G. Cambonie, L. Laplanche, J.M. Kamenka, and G. Barbanel NMDA but not glutamate induces the release of hydroxyl radicals in the neonatal rat: Modulation by group I metabotropic glutamate receptors J Neurosci Res 62 2000 84 90
42. G. Cambonie, H. Hirbec, M. Michaud, J.-M. Kamenka, and G. Barbanel Prenatal infection obliterates the glutamate-related protection against free hydroxyl radicals in neonatal rat brain J Neurosci Res 75 2004 125 132 (Pubitemid 38049413)
43. J. Perroy, F. Raynaud, V. Homburger, M.C. Rousset, L. Telley, J. Bockaert, and L. Fagni Direct interaction enables cross-talk between ionotropic and group I metabotropic glutamate receptors J Biol Chem 283 2008 6799 6805
44. J.A. Gordon Testing the glutamate hypothesis of schizophrenia Nat Neurosci 13 2010 2 4