Early-life programming of later-life brain and behavior: A critical role for the immune system

Frontiers in Behavioral Neuroscience

Volumn 3, Issue AUG, 2009, Pages

  Bilbo, Staci D ^a   Schwarz, Jaclyn M ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Anxiety; Cytokines; Depression; Infection; Interleukin 1; Memory; Microglia; Schizophrenia

Indexed keywords

EID: 77649139342     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.08.014.2009     Document Type: Review

References (176)

1. Abraham, W. C., and Williams, J. M. (2003). Properties and mechanisms of LTP maintenance. Neuroscientist 9, 463-474.
2. Adams-Chapman, I., and Stoll, B. J. (2006). Neonatal infection and longterm neurodevelopmental outcome in the preterm infant. Curr. Opin. Infect. Dis. 19, 290-297.
3. Armitage, J. A., Poston, L., and Taylor, P. D. (2008). Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front. Horm. Res. 36, 73-84.
4. Bakos, J., Duncko, R., Makatsori, A., Pirnik, Z., Kiss, A., and Jezova, D. (2004). Prenatal immune challenge affects growth, behavior, and brain dopamine in offspring. Ann. N. Y. Acad. Sci. 1018, 281-287.
5. Barres, B. A. (2008). The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60, 430-440.
6. Barrientos, R. M., Higgins, E. A., Sprunger, D. B., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2002). Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav. Brain Res. 134, 291-298.
7. Barrientos, R. M., Sprunger, D. B., Campeau, S., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2004). BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J. Neuroimmunol. 155, 119-126.
8. Bauman, M. L., Filipek, P. A., and Kemper, T. L. (1997). Early infantile autism. Int. Rev. Neurobiol. 41, 367-386.
9. Bayer, S. A., Altman, J., Russo, R. J., and Zhang, X. (1993). Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14, 83-144.
10. Bennet, L., and Gunn, A. (2006). The fetal origins of adult mental illness. In Early Life Origins of Health and Disease (Advances in Experimental Medicine and Biology), M. Wintour-Coghlan and J. Owens, eds (New York, Springer), pp. 204-211.
11. Bilbo, S. D., Barrientos, R. M., Eads, A. S., Northcutt, A., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2008a). Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav. Immun. 22, 451-455.
12. Bilbo, S. D., Yirmiya, R., Amat, J., Paul, E. D., Watkins, L. R., and Maier, S. F. (2008b). Bacterial infection early in life protects against stressorinduced depressive-like symptoms in adult rats. Psychoneuroendocrinology 33, 261-269.
13. Bilbo, S. D., Biedenkapp, J. C., Der-Avakian, A., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2005a). Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J. Neurosci. 25, 8000-8009.
14. Bilbo, S. D., Levkoff, L. H., Mahoney, J. H., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2005b). Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav. Neurosci. 119, 293-301.
15. Bilbo, S. D., Newsum, N. J., Sprunger, D. B., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2007). Differential effects of neonatal handling on early life infection-induced alterations in cognition in adulthood. Brain Behav. Immun. 21, 332-342.
16. Bilbo, S. D., Rudy, J. W., Watkins, L. R., and Maier, S. F. (2006). A behavioural characterization of neonatal infection-facilitated memory impairment in adult rats. Behav. Brain Res. 169, 39-47.
17. Billiards, S. S., Haynes, R. L., Folkerth, R. D., Trachtenberg, F. L., Liu, L. G., Volpe, J. J., and Kinney, H. C. (2006). Development of microglia in the cerebral white matter of the human fetus and infant. J. Comp. Neurol. 497, 199-208.
18. Boisse, L., Spencer, S. J., Mouihate, A., Vergnolle, N., and Pittman, Q. J. (2005). Neonatal immune challenge alters nociception in the adult rat. Pain 119, 133-141.
19. Breivik, T., Stephan, M., Brabant, G. E., Straub, R. H., Pabst, R., and von Horsten, S. (2002). Postnatal lipopolysaccharide-induced illness predisposes to periodontal disease in adulthood. Brain Behav. Immun. 16, 421-438.
20. Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M., Babulas, V. P., and Susser, E. S. (2004). Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 61, 774-780.
21. Bufford, J. D., and Gern, J. E. (2005). The hygiene hypothesis revisited. Immunol. Allergy Clin. North Am. 25, 247-262, v-vi.
22. Butovsky, O., Talpalar, A. E., Ben-Yaakov, K., and Schwartz, M. (2005). Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol. Cell Neurosci. 29, 381-393.
23. Cai, Z., Pan, Z. L., Pang, Y., Evans, O. B., and Rhodes, P. G. (2000). Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47, 64-72.
24. Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., and Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U.S.A. 95, 5335-5340.
25. Champagne, F. A. (2008). Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 29, 386-397.
26. Choy, K. H., de Visser, Y. P., and van den Buuse, M. (2009). The effect of 'two hit' neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density. Br. J. Pharmacol. 156, 388-396.
27. Combrinck, M. I., Perry, V. H., and Cunningham, C. (2002). Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease. Neuroscience 112, 7-11.
28. Coyle, P., Tran, N., Fung, J. N., Summers, B. L., and Rofe, A. M. (2009). Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy. Behav. Brain Res. 197, 210-218.
29. Cui, K., Ashdown, H., Luheshi, G. N., and Boksa, P. (2009). Effects of prenatal immune activation on hippocampal neurogenesis in the rat. Schizophr. Res. (in press).
30. Cunningham, A. J., Murray, C. A., O'Neill, L. A., Lynch, M. A., and O'Connor, J. J. (1996). Interleukin-1 beta (IL-1 beta) and TNF inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci. Lett. 203, 17-20.
31. Cunningham, C., Wilcockson, D. C., Campion, S., Lunnon, K., and Perry, V. H. (2005). Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J. Neurosci. 25, 9275-9284.
32. Cunningham, E. T., Jr., and De Souza, E. B. (1993). Interleukin 1 receptors in the brain and endocrine tissues. Immunol. Today 14, 171-176.
33. Dantzer, R., and Kelley, K. W. (2007). Twenty years of research on cytokineinduced sickness behavior. Brain Behav. Immun. 21, 153-160.
34. Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., and Kelley, K. W. (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-56.
35. de Boo, H. A., and Harding, J. E. (2006). The developmental origins of adult disease (Barker) hypothesis. Aust. N. Z. J. Obstet. Gynaecol. 46, 4-14.
36. Deguchi, K., Mizuguchi, M., and Takashima, S. (1996). Immunohistochemical expression of tumor necrosis factor alpha in neonatal leukomalacia. Pediatr. Neurol. 14, 13-16.
37. Dobbing, J., and Sands, J. (1979). Comparative aspects of the brain growth spurt. Early Hum. Dev. 3, 79-83.
38. Eklind, S., Mallard, C., Leverin, A. L., Gilland, E., Blomgren, K., Mattsby-Baltzer, I., and Hagberg, H. (2001). Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur. J. Neurosci. 13, 1101-1106.
39. Ellestad, K. K., Tsutsui, S., Noorbakhsh, F., Warren, K. G., Yong, V. W., Pittman, Q. J., and Power, C. (2009). Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J. Immunol. 183, 298-309.
40. Fanselow, M. (1990). Factors governing one trial contextual conditioning. Anim. Learn. Behav. 18, 264-270.
41. Fatemi, S. H., and Folsom, T. D. (2009). The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr. Bull. 35, 528-548.
42. Fidel, P. L., Jr., Romero, R., Wolf, N., Cutright, J., Ramirez, M., Araneda, H., and Cotton, D. B. (1994). Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice. Am. J. Obstet. Gynecol. 170, 1467-1475.
43. Fish, E. W., Shahrokh, D., Bagot, R., Caldji, C., Bredy, T., Szyf, M., and Meaney, M. J. (2004). Epigenetic programming of stress responses through variations in maternal care. Ann. N. Y. Acad. Sci. 1036, 167-180.
44. Fortier, M. E., Joober, R., Luheshi, G. N., and Boksa, P. (2004). Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamineinduced locomotion and startle responses in adult rat offspring. J. Psychiatr. Res. 38, 335-345.
45. Fortier, M. E., Luheshi, G. N., and Boksa, P. (2007). 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, 270-277.
46. Frank, M. G., Barrientos, R. M., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R., and Maier, S. F. (2006). mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 27, 717-722.
47. Fruntes, V., and Limosin, F. (2008). Schizophrenia and viral infection during neurodevelopment: a pathogenesis model? Med. Sci. Monit. 14, RA71-RA77.
48. Fujioka, M., Nishio, K., Miyamoto, S., Hiramatsu, K. I., Sakaki, T., Okuchi, K., Taoka, T., and Fujioka, S. (2000). Hippocampal damage in the human brain after cardiac arrest. Cerebrovasc. Dis. 10, 2-7.
49. Fujita, S., Tsuchihashi, Y., and Kitamura, T. (1981). Origin, morphology and function of the microglia. Prog. Clin. Biol. Res. 59A, 141-169.
50. Galic, M. A., Riazi, K., Heida, J. G., Mouihate, A., Fournier, N. M., Spencer, S. J., Kalynchuk, L. E., Teskey, G. C., and Pittman, Q. J. (2008). Postnatal inflammation increases seizure susceptibility in adult rats. J. Neurosci. 28, 6904-6913.
51. Gallo, P., Frei, K., Rordorf, C., Lazdins, J., Tavolato, B., and Fontana, A. (1989). Human immunodeficiency virus type 1 (HIV-1) infection of the central nervous system: an evaluation of cytokines in cerebrospinal fluid. J. Neuroimmunol. 23, 109-116.
52. Garnier, Y., Coumans, A. B., Jensen, A., Hasaart, T. H., and Berger, R. (2003). Infection-related perinatal brain injury: the pathogenic role of impaired fetal cardiovascular control. J. Soc. Gynecol. Investig. 10, 450-459.
53. Giaume, C., Kirchhoff, F., Matute, C., Reichenbach, A., and Verkhratsky, A. (2007). Glia: the fulcrum of brain diseases. Cell Death Differ. 14, 1324-1335.
54. Giulian, D., Young, D. G., Woodward, J., Brown, D. C., and Lachman, L. B. (1988). Interleukin-1 is an astroglial growth factor in the developing brain. J. Neurosci. 8, 709-714.
55. Godbout, J. P., Chen, J., Abraham, J., Richwine, A. F., Berg, B. M., Kelley, K. W., and Johnson, R. W. (2005). Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19, 1329-1331.
56. Golan, H. M., Lev, V., Hallak, M., Sorokin, Y., and Huleihel, M. (2005). Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 48, 903-917.
57. Goshen, I., Kreisel, T., Ounallah-Saad, H., Renbaum, P., Zalzstein, Y., Ben-Hur, T., Levy-Lahad, E., and Yirmiya, R. (2007). A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32, 1106-1115.
58. Granger, D. A., Hood, K. E., Ikeda, S. C., Reed, C. L., and Block, M. L. (1996). Neonatal endotoxin exposure alters the development of social behavior and the hypothalamic-pituitaryadrenal axis in selectively bred mice. Brain Behav. Immun. 10, 249-259.
59. Griffin, W. S., Stanley, L. C., Ling, C., White, L., MacLeod, V., Perrot, L. J., White, C. L., 3rd, and Araoz, C. (1989). Brain interleukin 1 and S-100 immunoreactivity are elevated in down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 86, 7611-7615.
60. Hagberg, H., Dammann, O., Mallard, C., and Leviton, A. (2004). Preconditioning and the developing brain. Semin. Perinatol. 28, 389-395.
61. Hagberg, H., and Mallard, C. (2005). Effect of inflammation on central nervous system development and vulnerability. Curr. Opin. Neurol. 18, 117-123.
62. Hales, C. N., and Barker, D. J. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595-601.
63. Harre, E. M., Galic, M. A., Mouihate, A., Noorbakhsh, F., and Pittman, Q. J. (2008). Neonatal inflammation produces selective behavioural deficits and alters N-methyl-D-aspartate receptor subunit mRNA in the adult rat brain. Eur. J. Neurosci. 27, 644-653.
64. Hart, B. L. (1988). Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123-137.
65. Hava, G., Vered, L., Yael, M., Mordechai, H., and Mahoud, H. (2006). Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy. Dev. Psychobiol. 48, 162-168.
66. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A. (2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103.
67. Hayley, S., Poulter, M. O., Merali, Z., and Anisman, H. (2005). The pathogenesis of clinical depression: stressorand cytokine-induced alterations of neuroplasticity. Neuroscience 135, 659-678.
68. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000). A toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
69. Herlenius, E., and Lagercrantz, H. (2004). Development of neurotransmitter systems during critical periods. Exp. Neurol. 190(Suppl. 1), S8-S21.
70. Hillier, S. L., Witkin, S. S., Krohn, M. A., Watts, D. H., Kiviat, N. B., and Eschenbach, D. A. (1993). The relationship of amniotic fluid cytokines and preterm delivery, amniotic fluid infection, histologic chorioamnionitis, and chorioamnion infection. Obstet. Gynecol. 81, 941-948.
71. Hodgson, D. M., Knott, B., and Walker, F. R. (2001). Neonatal endotoxin exposure influences HPA responsivity and impairs tumor immunity in Fischer 344 rats in adulthood. Pediatr. Res. 50, 750-755.
72. Holcberg, G., Amash, A., Sapir, O., Sheiner, E., Levy, S., Myatt, L., and Huleihel, M. (2008). Perfusion with lipopolysaccharide differently affects the secretion of interleukin-1 beta and interleukin-1 receptor antagonist by term and preterm human placentae. Placenta 29, 593-601.
73. Hornig, M., Solbrig, M., Horscroft, N., Weissenbock, H., and Lipkin, W. I. (2001). Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Curr. Top. Microbiol. Immunol. 253, 157-177.
74. Hornig, M., Weissenbock, H., Horscroft, N., and Lipkin, W. I. (1999). An infection-based model of neurodevelopmental damage. Proc. Natl. Acad. Sci. U.S.A. 96, 12102-12107.
75. Huleihel, M., Golan, H., and Hallak, M. (2004). Intrauterine infection/ inflammation during pregnancy and offspring brain damages: possible mechanisms involved. Reprod. Biol. Endocrinol. 2, 17.
76. Husband, A. J. (1995). The immune system and integrated homeostasis. Immunol. Cell Biol. 73, 377-382.
77. Irwin, M. R., and Miller, A. H. (2007). Depressive disorders and immunity: 20 years of progress and discovery. Brain Behav. Immun. 21, 374-383.
78. Katsuki, H., Nakai, S., Hirai, Y., Akaji, K., Kiso, Y., and Satoh, M. (1990). Interleukin-1 beta inhibits longterm potentiation in the CA3 region of mouse hippocampal slices. Eur. J. Pharmacol. 181, 323-326.
79. Kent, S., Bluthe, R. M., Kelley, K. W., and Dantzer, R. (1992). Sickness behavior as a new target for drug development. Trends Pharmacol. Sci. 13, 24-28.
80. Keshavan, M. S. (1999). Development, disease and degeneration in schizophrenia: a unitary pathophysiological model. J. Psychiatr. Res. 33, 513-521.
81. Kohman, R. A., Tarr, A. J., Sparkman, N. L., Bogale, T. M., and Boehm, G. W. (2008). Neonatal endotoxin exposure impairs avoidance learning and attenuates endotoxin-induced sickness behavior and central IL-1beta gene transcription in adulthood. Behav. Brain Res. 194, 25-31.
82. Kraepelin, E. (1919). Dementia praecox and paraphrenia (Foundations of Modern Psychiatry) [FACSIMILE], 1st Edn, July, 2002. Thoemmes Press.
83. Lalancette-Hebert, M., Gowing, G., Simard, A., Weng, Y. C., and Kriz, J. (2007). Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27, 2596-2605.
84. Leviton, A., and Dammann, O. (2002). Brain damage markers in children. Neurobiological and clinical aspects. Acta Paediatr. 91, 9-13.
85. Leviton, A., and Gilles, F. H. (1973). An epidemiologic study of perinatal telencephalic leucoencephalopathy in an autopsy population. J. Neurol. Sci. 18, 53-66.
86. Ling, E. A., and Wong, W. C. (1993). The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7, 9-18.
87. Liu, D., Diorio, J., Day, J. C., Francis, D. D., and Meaney, M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799-806.
88. Lowe, G. C., Luheshi, G. N., and Williams, S. (2008). 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, R1563-R1571.
89. Lynch, A. M., Walsh, C., Delaney, A., Nolan, Y., Campbell, V. A., and Lynch, M. A. (2004). Lipopolysaccharide-induced increase in signalling in hippocampus is abrogated by IL-10-a role for IL-1 beta? J. Neurochem. 88, 635-646.
90. Maier, S. F., and Watkins, L. R. (1998). Cytokines for psychologists: implications of bidirectional immuneto-brain communication for understanding behavior, mood, and cognition. Psychol. Rev. 105, 83-107.
91. Marshall-Clarke, S., Reen, D., Tasker, L., and Hassan, J. (2000). Neonatal immunity: how well has it grown up? Immunol. Today 21, 35-41.
92. Maynard, T. M., Sikich, L., Lieberman, J. A., and LaMantia, A. S. (2001). Neural development, cell-cell signaling, and the "two-hit" hypothesis of schizophrenia. Schizophr. Bull. 27, 457-476.
93. McAfoose, J., and Baune, B. T. (2009). Evidence for a cytokine model of cognitive function. Neurosci. Biobehav. Rev. 33, 355-366.
94. Merrill, J. E. (1992). Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Dev. Neurosci. 14, 1-10.
95. Meyer, U., and Feldon, J. (2008). Neural basis of psychosis-related behaviour in the infection model of schizophrenia. Behav. Brain Res. (in press).
96. Meyer, U., Feldon, J., Schedlowski, M., and Yee, B. K. (2005). Towards an immunoprecipitated neurodevelopmental animal model of schizophrenia. Neurosci. Biobehav. Rev. 29, 913-947.
97. Meyer, U., Feldon, J., Schedlowski, M., and Yee, B. K. (2006). Immunological stress at the maternal-foetal interface: a link between neurodevelopment and adult psychopathology. Brain Behav. Immun. 20, 378-388.
98. Meyer, U., Nyffeler, M., Yee, B. K., Knuesel, I., and Feldon, J. (2008). Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav. Immun. 22, 469-486.
99. Meyers, C. A. (2000). Neurocognitive dysfunction in cancer patients. Oncology 14, 75-79; discussion 79, 81-72, 85.
100. Miller, L. C., Isa, S., LoPreste, G., Schaller, J. G., and Dinarello, C. A. (1990). Neonatal interleukin-1 beta, interleukin-6, and tumor necrosis factor: cord blood levels and cellular production. J. Pediatr. 117, 961-965.
101. Morale, M. C., Serra, P. A., L'Episcopo, F., Tirolo, C., Caniglia, S., Testa, N., Gennuso, F., Giaquinta, G., Rocchitta, G., Desole, M. S., Miele, E., and Marchetti, B. (2006). Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138, 869-878.
102. Morrison, J. H., and Hof, P. R. (1997). Life and death of neurons in the aging brain. Science 278, 412-419.
103. Mustafa, M. M., Lebel, M. H., Ramilo, O., Olsen, K. D., Reisch, J. S., Beutler, B., and McCracken, G. H., Jr. (1989). Correlation of interleukin-1 beta and cachectin concentrations in cerebrospinal fluid and outcome from bacterial meningitis. J. Pediatr. 115, 208-213.
104. Nawa, H., and Takei, N. (2006). Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci. Res. 56, 2-13.
105. Nelson, K. B., and Willoughby, R. E. (2000). Infection, inflammation and the risk of cerebral palsy. Curr. Opin. Neurol. 13, 133-139.
106. Nesse, R., and Williams, G. (1994). Why we get sick. New York, Vintage Books.
107. Nyffeler, M., Meyer, U., Yee, B. K., Feldon, J., and Knuesel, I. (2006). Maternal immune activation during pregnancy increases limbic GABAA receptor immunoreactivity in the adult offspring: implications for schizophrenia. Neuroscience 143, 51-62.
108. Osrin, D., Vergnano, S., and Costello, A. (2004). Serious bacterial infections in newborn infants in developing countries. Curr. Opin. Infect. Dis. 17, 217-224.
109. Owen, D., Andrews, M. H., and Matthews, S. G. (2005). Maternal adversity, glucocorticoids and programming of neuroendocrine function and behaviour. Neurosci. Biobehav. Rev. 29, 209-226.
110. Pang, Y., Cai, Z., and Rhodes, P. G. (2003). Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res. Dev. Brain Res. 140, 205-214.
111. Pantelis, C., Yucel, M., Wood, S. J., McGorry, P. D., and Velakoulis, D. (2003). Early and late neurodevelopmental disturbances in schizophrenia and their functional consequences. Aust. N. Z. J. Psychiatry 37, 399-406.
112. Pearce, B. D. (2001). Schizophrenia and viral infection during neurodevelopment: a focus on mechanisms. Mol. Psychiatry 6, 634-646.
113. Perry, V. H. (2004). The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav. Immun. 18, 407-413.
114. Perry, V. H., Cunningham, C., and Boche, D. (2002). Atypical inflammation in the central nervous system in prion disease. Curr. Opin. Neurol. 15, 349-354.
115. Perry, V. H., Newman, T. A., and Cunningham, C. (2003). The impact of systemic infection on the progression of neurodegenerative disease. Nat. Rev. Neurosci. 4, 103-112.
116. Petito, C. K., Feldmann, E., Pulsinelli, W. A., and Plum, F. (1987). Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37, 1281-1286.
117. Pollak, Y., and Yirmiya, R. (2002). Cytokine-induced changes in mood and behaviour: implications for 'depression due to a general medical condition', immunotherapy and antidepressive treatment. Int. J. Neuropsychopharmacol. 5, 389-399.
118. Pousset, F. (1994). Developmental expression of cytokine genes in the cortex and hippocampus of the rat central nervous system. Brain Res. Dev. Brain Res. 81, 143-146.
119. Pugh, C. R., Kumagawa, K., Fleshner, M., Watkins, L. R., Maier, S. F., and Rudy, J. W. (1998). Selective effects of peripheral lipopolysaccharide administration on contextual and auditorycue fear conditioning. Brain Behav. Immun. 12, 212-229.
120. Pugh, C. R., Nguyen, K. T., Gonyea, J. L., Fleshner, M., Wakins, L. R., Maier, S. F., and Rudy, J. W. (1999). Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav. Brain Res. 106, 109-118.
121. Rakic, S., and Zecevic, N. (2000). Programmed cell death in the developing human telencephalon. Eur. J. Neurosci. 12, 2721-2734.
122. Rantakallio, P., Jones, P., Moring, J., and Von Wendt, L. (1997). Association between central nervous system infections during childhood and adult onset schizophrenia and other psychoses: a 28-year follow-up. Int. J. Epidemiol. 26, 837-843.
123. Rezaie, P., Cairns, N. J., and Male, D. K. (1997). Expression of adhesion molecules on human fetal cerebral vessels: relationship to microglial colonisation during development. Brain Res. Dev. Brain Res. 104, 175-189.
124. Rezaie, P., and Male, D. (2002). Mesoglia & microglia-a historical review of the concept of mononuclear phagocytes within the central nervous system. J. Hist. Neurosci. 11, 325-374.
125. Rice, D., and Barone, S., Jr. (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108(Suppl 3), 511-533.
126. Richardson-Burns, S. M., and Tyler, K. L. (2004). Regional differences in viral growth and central nervous system injury correlate with apoptosis. J. Virol. 78, 5466-5475.
127. Rodier, P. M. (1980). Chronology of neuron development: animal studies and their clinical implications. Dev. Med. Child. Neurol. 22, 525-545.
128. Romero, E., Ali, C., Molina-Holgado, E., Castellano, B., Guaza, C., and Borrell, J. (2007). Neurobehavioral and immunological consequences of prenatal immune activation in rats. Influence of antipsychotics. Neuropsychopharmacology 32, 1791-1804.
129. Ross, F. M., Allan, S. M., Rothwell, N. J., and Verkhratsky, A. (2003). A dual role for interleukin-1 in LTP in mouse hippocampal slices. J. Neuroimmunol. 144, 61-67.
130. Rudy, J. W., Barrientos, R. M., and O'Reilly, R. C. (2002). Hippocampal formation supports conditioning to memory of a context. Behav. Neurosci. 116, 530-538.
131. Rudy, J. W., Huff, N. C., and Matus-Amat, P. (2004). Understanding contextual fear conditioning: insights from a two-process model. Neurosci. Biobehav. Rev. 28, 675-685.
132. Rudy, J. W., and O'Reilly, R. C. (2001). Conjunctive representations, the hippocampus, and contextual fear conditioning. Cogn. Affect. Behav. Neurosci. 1, 66-82.
133. Salmenpera, T., Kalviainen, R., Partanen, K., and Pitkanen, A. (1998). Hippocampal damage caused by seizures in temporal lobe epilepsy. Lancet 351, 35.
134. Sapolsky, R. M., Uno, H., Rebert, C. S., and Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J. Neurosci. 10, 2897-2902.
135. Schmitz, T., and Chew, L. J. (2008). Cytokines and myelination in the central nervous system. ScientificWorldJournal 8, 1119-1147.
136. Schneider, H., Pitossi, F., Balschun, D., Wagner, A., del Rey, A., and Besedovsky, H. O. (1998). A neuromodulatory role of interleukin-1beta in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 95, 7778-7783.
137. Shanks, N., and Meaney, M. J. (1994). Hypothalamic-pituitary-adrenal activation following endotoxin administration in the developing rat: a CRH-mediated effect. J. Neuroendocrinol. 6, 375-383.
138. Shanks, N., Windle, R. J., Perks, P. A., Harbuz, M. S., Jessop, D. S., Ingram, C. D., and Lightman, S. L. (2000). Early-life exposure to endotoxin alters hypothalamicpituitary-adrenal function and predisposition to inflammation. Proc. Natl. Acad. Sci. U.S.A. 97, 5645-5650.
139. Shi, L., Fatemi, S. H., Sidwell, R. W., and Patterson, P. H. (2003). Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23, 297-302.
140. Shi, L., Smith, S. E., Malkova, N., Tse, D., Su, Y., and Patterson, P. H. (2009). Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 23, 116-123.
141. Skogstrand, K., Hougaard, D. M., Schendel, D. E., Bent, N. P., Svaerke, C., and Thorsen, P. (2008). Association of preterm birth with sustained postnatal inflammatory response. Obstet. Gynecol. 111, 1118-1128.
142. Smith, S. E., Li, J., Garbett, K., Mirnics, K., and Patterson, P. H. (2007). Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 27, 10695-10702.
143. Spencer, S. J., Martin, S., Mouihate, A., and Pittman, Q. J. (2006). Earlylife immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology 31, 1910-1918.
144. Spulber, S., Mateos, L., Oprica, M., Cedazo-Minguez, A., Bartfai, T., Winblad, B., and Schultzberg, M. (2009). Impaired long term memory consolidation in transgenic mice overexpressing the human soluble form of IL-1ra in the brain. J. Neuroimmunol. 208, 46-53.
145. Stanley, L. C., Mrak, R. E., Woody, R. C., Perrot, L. J., Zhang, S., Marshak, D. R., Nelson, S. J., and Griffin, W. S. (1994). Glial cytokines as neuropathogenic factors in HIV infection: pathogenic similarities to Alzheimer's disease. J. Neuropathol. Exp. Neurol. 53, 231-238.
146. Stead, J. D., Neal, C., Meng, F., Wang, Y., Evans, S., Vazquez, D. M., Watson, S. J., and Akil, H. (2006). Transcriptional profiling of the developing rat brain reveals that the most dramatic regional differentiation in gene expression occurs postpartum. J. Neurosci. 26, 345-353.
147. Steiner, A. A., Chakravarty, S., Robbins, J. R., Dragic, A. S., Pan, J., Herkenham, M., and Romanovsky, A. A. (2005). Thermoregulatory responses of rats to conventional preparations of lipopolysaccharide are caused by lipopolysaccharide per se-not by lipoprotein contaminants. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R348-R352.
148. Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., Sher, A., Litke, A. M., Lambris, J. D., Smith, S. J., John, S. W., and Barres, B. A. (2007). The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178.
149. Stoll, B. J., Hansen, N. I., Adams-Chapman, I., Fanaroff, A. A., Hintz, S. R., Vohr, B., and Higgins, R. D. (2004). Neurodevelopmental and growth impairment among extremely lowbirth-weight infants with neonatal infection. JAMA 292, 2357-2365.
150. Stoll, B. J., Hansen, N. I., Higgins, R. D., Fanaroff, A. A., Duara, S., Goldberg, R., Laptook, A., Walsh, M., Oh, W., and Hale, E. (2005). Very low birth weight preterm infants with early onset neo natal sepsis: the predominance of gram-negative infections continues in the National Institute of Child Health and Human Development Neonatal Research Network, 2002-2003. Pediatr. Infect. Dis. J. 24, 635-639.
151. Strachan, D. P. (1989). Hay fever, hygiene, and household size. BMJ 299, 1259-1260.
152. Streit, W. J. (2001). Microglia and macrophages in the developing CNS. Neurotoxicology 22, 619-624.
153. Tenk, C. M., Foley, K. A., Kavaliers, M., and Ossenkopp, K. P. (2007). Neonatal immune system activation with lipopolysaccharide enhances behavioural sensitization to the dopamine agonist, quinpirole, in adult female but not male rats. Brain Behav. Immun. 21, 935-945.
154. Tong, L., Balazs, R., Soiampornkul, R., Thangnipon, W., and Cotman, C. W. (2008). Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol. Aging 29, 1380-1393.
155. Town, T., Nikolic, V., and Tan, J. (2005). The microglial "activation" continuum: from innate to adaptive responses. J. Neuroinflammation 2, 24.
156. Ullian, E. M., Christopherson, K. S., and Barres, B. A. (2004). Role for glia in synaptogenesis. Glia 47, 209-216.
157. Urakubo, A., Jarskog, L. F., Lieberman, J. A., and Gilmore, J. H. (2001). Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr. Res. 47, 27-36.
158. Vaccarino, F. M., and Ment, L. R. (2004). Injury and repair in developing brain. Arch. Dis. Child. Fetal Neonatal Ed. 89, F190-F192.
159. Vedhara, K., Miles, J., Crown, A., McCarthy, A., Shanks, N., Davies, D., Lightman, S., Davey-Smith, G., and Ben-Shlomo, Y. (2007). Relationship of early childhood illness with adult cortisol in the Barry Caerphilly Growth (BCG) cohort. Psychoneuroendocrinology 32, 865-873.
160. Vereker, E., Campbell, V., Roche, E., McEntee, E., and Lynch, M. A. (2000). Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J. Biol. Chem. 275, 26252-26258.
161. Vitkovic, L., Bockaert, J., and Jacque, C. (2000). "Inflammatory" cytokines: neuromodulators in normal brain? J. Neurochem. 74, 457-471.
162. Walker, A. K., Nakamura, T., Byrne, R. J., Naicker, S., Tynan, R. J., Hunter, M., and Hodgson, D. M. (2009a). Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxietylike behaviour and blunted corticosterone responses: Implications for the double-hit hypothesis. Psychoneuroendocrinology. (in press).
163. Walker, F. R., Hodyl, N. A., and Hodgson, D. M. (2009b). Neonatal bacterial endotoxin challenge interacts with stress in the adult male rat to modify KLH specific antibody production but not KLH stimulated ex vivo cytokine release. J. Neuroimmunol. 207, 57-65.
164. Walker, F. R., Hodyl, N. A., Krivanek, K. M., and Hodgson, D. M. (2006). Early life host-bacteria relations and development: long-term individual differences in neuroimmune function following neonatal endotoxin challenge. Physiol. Behav. 87, 126-134.
165. Walker, F. R., Knott, B., and Hodgson, D. M. (2008). Neonatal endotoxin exposure modifies the acoustic startle response and circulating levels of corticosterone in the adult rat but only following acute stress. J. Psychiatr. Res. 42, 1094-1103.
166. Walker, F. R., March, J., and Hodgson, D. M. (2004). Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat. Behav. Brain Res. 154, 63-69.
167. Wang, X., Rousset, C. I., Hagberg, H., and Mallard, C. (2006). Lipopolysaccharideinduced inflammation and perinatal brain injury. Semin. Fetal Neonatal Med. 11, 343-353.
168. Westbrook, R. F., Good, A. J., and Kiernan, M. J. (1994). Effects of the interval between exposure to a novel environment and the occurrence of shock on the freezing responses of rats. Q. J. Exp. Psychol. B. 47, 427-446.
169. Wolff, A. R., and Bilkey, D. K. (2008). Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav. Brain Res. 190, 156-159.
170. Wu, C. H., Wen, C. Y., Shieh, J. Y., and Ling, E. A. (1992). A quantitative and morphometric study of the transformation of amoeboid microglia into ramified microglia in the developing corpus callosum in rats. J. Anat. 181(Pt 3), 423-430.
171. Yolken, R. H., and Torrey, E. F. (2008). Are some cases of psychosis caused by microbial agents? A review of the evidence. Mol. Psychiatry 13, 470-479.
172. Yoon, B. H., Romero, R., Kim, C. J., Jun, J. K., Gomez, R., Choi, J. H., and Syn, H. C. (1995). Amniotic fluid interleukin-6: a sensitive test for antenatal diagnosis of acute inflammatory lesions of preterm placenta and prediction of perinatal morbidity. Am. J. Obstet. Gynecol. 172, 960-970.
173. Yu, H. M., Yuan, T. M., Gu, W. Z., and Li, J. P. (2004). Expression of glial fibrillary acidic protein in developing rat brain after intrauterine infection. Neuropathology 24, 136-143.
174. Zuckerman, L., Rehavi, M., Nachman, R., and Weiner, I. (2003). 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, 1778-1789.
175. Zuckerman, L., and Weiner, I. (2003). Postpubertal emergence of disrupted latent inhibition following prenatal immune activation. Psychopharmacology (Berl) 169, 308-313.
176. Zuckerman, L., and Weiner, I. (2005). Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J. Psychiatr. Res. 39, 311-323.