Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-25T18:54:07.897Z Has data issue: false hasContentIssue false

Early life environment: does it have implications for predisposition to disease?

Published online by Cambridge University Press:  24 June 2014

Nola Shanks*
Affiliation:
University Research Center for Neuroendocrinology, University of Bristol, Dorothy Hodgkins Laboratories, Bristol,UK

Abstract

Early life environmental factors have been associated with altered predisposition to a variety of pathologies. A considerable literature examines pre- and postnatal factors associated with increased risk of cardiovascular, metabolic (i.e. insulin resistance, hyperlipidemia) and psychiatric disease, and the importance of hormonal programming. The brain is exquisitely sensitive to environmental inputs during development and the stress responsiveness of the hypothalamic–pituitary–adrenal (HPA) axis has been shown to be both up- and down-regulated by early life exposure to limited nutrition, stress, altered maternal behaviors, synthetic steroids and inflammation. It has been suggested that peri-natal programming of HPA axis regulation might therefore contribute to metabolic and psychiatric disease etiology. In addition, glucocorticoids play modulatory roles regulating many aspects of immune function, notably controlling both acute and chronic inflammatory responses. Neuroendocrine–immune communication is bidirectional, and therefore it is expected that environmental factors altering HPA regulation have implications for stress effects on immune function and predisposition to inflammation. The impact of pre- and postnatal factors altering immune function, stress responsivity and predisposition to inflammatory disease are reviewed. It is also examined whether the early ‘immune environment’ might similarly influence predisposition to disease and alter neuroendocrine function. Evidence indicating a role for early life inflammation and infection as an important factor programming the neuroendocrine–immune axis and altering predisposition to disease is considered.

Type
Review Article
Copyright
Copyright © Acta Neuropsychiatrica 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arshad, SH, Hide, DW. Effect of environmental factors on the development of allergic disorders in infancy. J Allergy Clin Immunol 1992;90: 235241.CrossRefGoogle ScholarPubMed
Brown, GR, Anderson, B. Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse. Am J Psychiatry 1991;148: 5561.Google Scholar
Flinn, MV, England, BG. Socioeconomics of childhood glucocorticoid stress response and health. Am J Phys Anthropol 1997;102: 3353.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Holmes, S, Robins, L. The influence of childhood disciplinary experiences on the development of alcoholism and depression. J Child Psycho Psychiatry Allied Professions 1987;28: 399415. CrossRefGoogle Scholar
Levitt, NS, Lambert, EV, Woods, D, Hales, D, Andrew, R, Seckl, JR. Impaired glucose tolerance and elevated blood pressure in low birth weight, non-obese young South African adults: early programming of the cortisol axis. J Clin Endocrinol Metabol 2000;85: 46114618. Google Scholar
Marmot, MG, Shipley, MJ, Rose, G. Inequalities in death – specific explanations of a general pattern? Lancet 1984;1: 10031006.CrossRefGoogle ScholarPubMed
Yarnell, JGW, Limb, ES, Layzell, JM, Baker, IA. Height: a risk marker for ischaemic heart disease. Eur Hear J 1992;13: 16021605. CrossRefGoogle ScholarPubMed
Barker, DJP. Fetal origins of coronary heart disease. Br Heart J 1993;69: 195196.CrossRefGoogle ScholarPubMed
Phillips, DIW, Barker, DJP, Fall, CHDet al. Elevated plasma cortisol concentrations. a link between low birthweight and the insulin resistance syndrome? J Clin Endocrinol Metabol 1998;83: 757760. Google ScholarPubMed
Osmond, C, Barker, DJ. Fetal, infant and childhood growth are predictors of coronary heart disease, diabetes and hypertension in adult men and women. Environ Health Perspect 2000;108 (Suppl. 3):545553.CrossRefGoogle ScholarPubMed
Petry, CJ, Ozanne, SE, Hales, CN. Programming of intermediary metabolism. Mol Cell Endocrinol 2001;85: 8191. CrossRefGoogle Scholar
Eriksson, JG, Forsen, T, Tuomilenhto, J, Osmond, C, Barker, DJP. Early growth and coronary heart disease in later life: longitudinal study. BMJ 2001;322: 949953.CrossRefGoogle ScholarPubMed
Phillips, DIW, Walker, BR, Reynolds, RMet al. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension 2000;35: 13011306.CrossRefGoogle ScholarPubMed
Clark, PM, Hindmarsh, PC, Shiell, AW, Law, C, Honour, JW, Barker, DJ. Size at birth and adrenocortical function in childhood. Clin Endocrinol 1996;45: 721726. CrossRefGoogle ScholarPubMed
Rosmond, R, Bjorntorp, P. The hypothalamic-pituitary-adrenal axis activity as a predictor of cardiovasucalr disease, type 2 diabetes and stroke. J Intern Med 2000;247: 188197.CrossRefGoogle ScholarPubMed
Welberg, LAM, Seckl, JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 2001;13: 113128.CrossRefGoogle Scholar
Seckl, JR. Glucocorticoid programming of the fetus;adult phenotypes and molecular mechanisms. Mol Cell Endocrinol 2001;185: 6171.CrossRefGoogle ScholarPubMed
Levitt, N, Lindsay, RS, Holmes, MC, Seckl, JR. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrin 1996;64: 412418. CrossRefGoogle Scholar
Nyirenda, MJ, Lindsay, RS, Kenyon, CJ, Burchell, A, Seckl, JR. Glucocorticoid exposure in late gestation permanently programmes rat hepatic phosphoenopyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 1998;101: 21742181.CrossRefGoogle Scholar
Maccari, S, Piazza, PV, Kabbaj, M, Barbazanges, A, Simon, H, Le Moal, M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 1995;15: 867875. Google ScholarPubMed
Wakshlak, A, Weinstock, M. Neonatal handling reverses behavioural abnormalities induced in rats by prenatal stress. Physiol Behav 1990;48: 289292.CrossRefGoogle Scholar
Weinstock, M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Progr Neurobiol 2001;65: 427451. CrossRefGoogle Scholar
Takahashi, LK, Turner, JG, Kalin, NH. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behaviour in adult rats. Brain Res 1992;574: 131137.CrossRefGoogle Scholar
Vallee, M, Mayo, W, Dellu, F, Lemoal, M, Simon, H, Maccari, S. Prenatal stress induces high anxiety and postnatal handling induced low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 1997;17: 26262636.Google Scholar
Henry, C, Kabbaj, M, Simon, H, Lemoal, M, Maccari, S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 1994;6: 341345.CrossRefGoogle Scholar
McCormick, CM, Smythe, JW, Sharma, S, Meaney, MJ. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Dev Brain Res 1995;84: 5561. CrossRefGoogle Scholar
Ward, HE, Johnson, EA, Salm, AK, Birkle, DI. Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol Behav 2000;70: 359366.CrossRefGoogle Scholar
Cratty, MS, Ward, HE, Johnson, EA, Azzaro, AJ, Birke, DI. Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 1995;675: 297302.CrossRefGoogle Scholar
Kaufman, J, Plotsky, PM, Nemeroff, CB, Charney, DS. Effects of early adverse experiences on brain structure and function: clinical implications. Biol Psychiatry 2000;48: 778790.CrossRefGoogle ScholarPubMed
Plotsky, PM, Meaney, MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 1993;18: 195200.CrossRefGoogle ScholarPubMed
Francis, DD, Caldji, C, Champagne, F, Plotsky, PM, Meaney, MJ. The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioural and endocrine responses to stress. Biol Psychiatry 1999;46: 11531166.CrossRefGoogle Scholar
Francis, DD, Diorio, J, Liu, D, Meaney, MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999;286: 11551158.CrossRefGoogle ScholarPubMed
Liu, D, Caldji, C, Sharma, S, Plotsky, PM, Meaney, MJ. Influence of neonatal rearing condition on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 2000;12: 512.CrossRefGoogle ScholarPubMed
Caldji, C, Francis, D, Sharma, S, Plotsky, PM, Meaney, MJ. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacol 2000;22: 219229. CrossRefGoogle ScholarPubMed
Bremne, JD, Vermetten, E. Stress and development: behavioural and biological consequences. Dev Psychopathol 2001;13: 473489.CrossRefGoogle Scholar
Heim, C, Nemeroff, CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 2001;15: 10231039. CrossRefGoogle Scholar
Liu, D, Diorio, J, Tannenbaum, Bet al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997;277: 16591662.CrossRefGoogle ScholarPubMed
Meaney, MJ, Bhatnagor, S, Larocque, Set al. Individual differences in the hypothalamic-pituitary-adrenal stress response and the hypothalamic CRF system. Ann NY Acad Sci 1993;697: 7085.CrossRefGoogle ScholarPubMed
Weaver, ICG, La Plante, P, Weaver, Set al. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Molcell Endocrinol 2001;185: 205218. Google ScholarPubMed
Avishai-Eliner, S, Eghbal-Ahmadi, M, Tabachnik, E, Brunson, KL, Baram, TZ. Down-regulation of hypothalamic corticotropin-releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinol 2001;142: 8997. CrossRefGoogle ScholarPubMed
Chan, RKW, Brown, ER, Ericsson, A, Kovacs, KJ, Sawchenko, PE. A comparison of two immediate early genes, c-fos and NGFI-B as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci 1993;13: 51265138.Google ScholarPubMed
Ericsson, A, Kovacs, KJ, Sawchenko, PE. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 1994;14: 897913.Google Scholar
Boyce, WT, Jemerin, JM. Psychobiological differences in childhood stress response. I. Patterns of illness and susceptibility. J Dev Behav Pediatr 1990;11: 8694.CrossRefGoogle Scholar
Boyce, WT, Chesney, M, Alkon, Aet al. Psychobiologic reactivity to stress and childhood respiratory illnesses: results of two prospective studies. Psychosom Med 1995;578: 411422. CrossRefGoogle Scholar
Turner Cobb, JM, Steptoe, A. Psychosocial influences on upper respiratory infectious illness in children. J Psychosom Res 1998;45: 319330.CrossRefGoogle ScholarPubMed
Laudenslager, ML, Held, PE, Boccia, ML, Reite, ML, Cohen, JJ. Behavioral and immunological consequences of brief mother-infant separation: a species comparison. Dev Psychobiol 1990;23: 247264.CrossRefGoogle ScholarPubMed
Bailey, MT, Coe, CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999;35: 146155.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Reyes, TM, Coe, CL. Prenatal manipulations reduce the proinflammatory response to a cytokine challenge in juvenile monkeys. Brain Res 1997;769: 2935.CrossRefGoogle ScholarPubMed
Coe, CL, Lubac, GR, Karaszewski, JW. Prenatal stress and immune recognition of self and nonself in the primate neonate. Biol Neonate 1999;76: 301310.CrossRefGoogle ScholarPubMed
Wellberg, LAM, Seckl, JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 2001;13: 113128.CrossRefGoogle Scholar
Gorzynski, RM. Conditioned stress responses by pregnant and/or lactating mice reduce immune responses of their offspring after weaning. Brain Behav Immun 1992;6: 8795.CrossRefGoogle Scholar
Saravia-Fernandez, F, Durant, S, El Hasnaoui, A, Dardenne, M, Homo-Delarche, F. Environmental and experimental procedures leading to variation in the incidence of diabetes in the nonobese diabetic (NOD) mouse. Autoimmunity 1996;24: 113121.CrossRefGoogle Scholar
Bhatnagar, S, Shanks, N, Meaney, MJ. Plaque-forming cell response and antibody-titers following injection of sheep red-blood cells in nonstressed, acute and/or chronically stressed handled and nonhandled animals. Dev Psychobiol 1996;29: 171181.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
von Hoersten, S, Dimitrijevic, M, Markovic, BM, Jankovic, BD. Effect of early experience on behavior and immune response in the rat. Physiol Behav 1993;54: 931940.CrossRefGoogle Scholar
Hilakivi-Clarke, L, Wright, A, Lippman, ME. DMBA-induced mammary tumor growth in rats exhibiting increased or decreased ability to cope with stress due to early postnatal handling or antidepressant treatment. Physiol Beh 1993;54: 229236. CrossRefGoogle ScholarPubMed
Laban, O, Dimitrijevic, M, Von Hoersten, S, Markovic, BM, Jankovic, BD. Experimental allergic encephalomyelitis in adult DA rats subjected to neonatal handling or gentling. Brain Res 1995;676: 133140.CrossRefGoogle ScholarPubMed
Manni, L, Micera, A, Pistillo, L, Aloe, L. Neonatal handling in EAE-susceptible rats alters NGF levels and mast cell distribution in the brain. Int J Dev Neurosci 1998;16: 18.CrossRefGoogle Scholar
Shanks, N, Windle, RJ, Perks, PA, Harbuz, MS, Jessop, DS, Ingram, CD, Lightman, SL. Early life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation. Proc Natl Acad Sci 2000;97: 56455650.CrossRefGoogle ScholarPubMed
Laban, O, Markovic, BM, Dimitrijevic, M, Jankovic, BD. Maternal deprivation and early weaning modulate EAE in the rat. Brain Beh Imm 1995;9: 919. CrossRefGoogle ScholarPubMed
Dimitrijevic, M, Laban, O, Von Hoersten, S, Markovic, BM, Jankovic, BD. Neonatal sound stress and development of experimetnal allergic encephalomyelitis in Lewis and DA rats. Int J Neurosci 1994;78: 135143.CrossRefGoogle Scholar
Bakker, JM, Kavelaars, A, Kamphuis, P J, Cobelens, PM, Van Vugt, HF, Heijnen, CJ. Neonatal dexamethasone treatment increases susceptibility to experimental autoimmune disease in adult rats. J Immunol 2000;165: 59325937.CrossRefGoogle Scholar
Bakker, JM, Cavelaars, A, Kamphuis, PJ, Zijlstra, J, Van Bel, F, Heijnen, CJ. Neonatal dexamethasone treatment induces long-lasting changes in T-cell receptor vbeta repertoire in rats. J Neuroimmunol 2001;112: 4754.CrossRefGoogle ScholarPubMed
Reul, JM, Stec, I, Wiegers, GJet al. Prenatal immune challenge alters the hypothalamic-pituitary-adrenocortical axis in adult rats. J Clin Invest 1994;93: 002607. CrossRefGoogle ScholarPubMed
Gotz, F, Dorner, G, Malz, Uet al. Short- and long-term effects of perinatal interleukin-1 beta-application in rats. Neuroendocrinology 1993;58: 344351.CrossRefGoogle Scholar
Urakubo, A, Jarskog, LF, Lieberman, JA, Gilmore, JH. Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr Res 2001;47: 2736.CrossRefGoogle ScholarPubMed
Nilsson, C, Larsson, BM, Jennishche, Eet al. Maternal endotoxemia results in obesity and insulin resistance in adult male offspring. Endocrinology 2001;142: 26222630.CrossRefGoogle ScholarPubMed
Fonager, K, Sorensen, HT, Olsen, J, Dahlerup, JF, Rasmussen, SN. Pregnancy outcome for women with Crohn's disease. a follow-up study based on linkage between national registries. Am J Gastroenterol 1998;93: 24262430.CrossRefGoogle ScholarPubMed
Preece, PM, Blount, JM, Glover, J, Fletcher, G, Peckham, CS, Griffiths, PD. The consequences of primary cytomegalovirus infection in pregnancy. Arch Dischild 1983;58: 970975. Google ScholarPubMed
Ling, ZD, Gayle, DA, Ma, SYet al. In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Movement Disord 2002;17: 116124.CrossRefGoogle ScholarPubMed
del Rey, A, Furukawa, H, Monge-Arditi, G, Kabiersch, A, Voigt, KH, Besedovsky, HO. Alterations in the pituitary-adrenal axis of adult mice following neonatal exposure to interleukin-1. Brain Behav Imm 1996;10: 235248. Google Scholar
Plagemann, A, Staudt, A, Gotz, Fet al. Long-term effects of early postnatally administered interleukin-1-beta on the hypothalamic-pituitary-adrenal (HPA) axis in rats. Endocr Regul 1998;32: 7785.Google ScholarPubMed
Shanks, N, Larocque, S, Meaney, MJ. Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: Early illness and later responsivity to stress. J Neurosci 1995;15: 376384.Google Scholar
Hodgson, DM, Knott, B, Walker, FR. Neonatal endotoxin exposure influences HPA responsivity and impairs tumor immunity in Fischer 344 rats in adulthood. Pediatr Res 2001;50: 750755.CrossRefGoogle ScholarPubMed
Breivik, T, Stephan, M, Brabant, GE, Straub, RH, Pabst, R, Von Horsten, S. Postnatal lipopolysaccharide-induced illness predisposes to periodontal disease in adulthood. Brain Beh Imm 2002; 16: 421438.Google Scholar
Granger, DA, Hood, KE, Ikeda, SC, Reed, CL, Block, ML. Neonatal endotoxin exposure alters the development of social behavior and the hypothalamic-pituitary-adrenal axis in selectively bred mice. Brain Beh Imm 1996;10: 249259. CrossRefGoogle ScholarPubMed
Sternberg, EM. Neuroendocrine regulation of autoimmune disease. J Endocrinol 2001;169: 429435.CrossRefGoogle Scholar
Mason, D. Genetic variation in the stress response. Susceptibility to experimental allergic encephalomyelitis and implications for human inflammatory disease. Immunol Today 1991;12: 5760.CrossRefGoogle ScholarPubMed
van De Lagerijt., AG, Va Lent, PL, Hermus, AR, Sweep, CG, Cools, AR, Van Den Berg, WB. Susceptibility to adjuvant arthritis. relative importance of adrenal activity and bacterial flora. Clin Exp Immunol 1994;97: 3338.CrossRefGoogle Scholar
Kimpen, JLL. Viral infections and childhood asthma. Am J Respir Crit Care Med 2000;162: S108S112.CrossRefGoogle ScholarPubMed
Martinez, FD. Viruses and atopic sensitisation in the first years of life. Am J Respir Crit Care Med 2000;162: S95S99.CrossRefGoogle Scholar
Holt, PG, Sly, PD, Bjorksten, B. Atopic versus infectious diseases in childhood. a question of balance? Pediatr Allegy Immunol 1997;8: 5358. CrossRefGoogle Scholar
Strachan, DP. Hay fever, hygiene and household size. Br Med J 1989;299: 12591260. CrossRefGoogle ScholarPubMed
Strachan, DP, Harkins, LS, Johnston, IDA, Anderson, HR. Childhood antecedents of allergic sensitisation in young British adults. J Allergy Clin Immunol 1997;99: 612.Google Scholar
Rook, GA, Stanford, JL. Give us this day our daily germs. Immunol Today 1998;19: 113116.CrossRefGoogle ScholarPubMed
Folkert, G, Walzl, G, Openshaw, PJM. Do common childhood infections ‘teach’ the immune system not to be allergic? Immunol Today 2000;21: 118120.CrossRefGoogle Scholar
Von Hertzen, LC. Puzzling associations between childhood infections and the later occurrence of asthma and atopy. Ann Med 2000;32: 397400.CrossRefGoogle ScholarPubMed
Ramchandra, RN, Sehon, A, Berczi, I. Neuro-hormonal defence in endotoxin shock. Brain Behav Immun 1992;6: 157169.CrossRefGoogle Scholar
Mendall, MA, Goggin, PMet al. Relation of helicobacter pylori infection and coronary heart disease. Br Heart J 1994;71: 437439.CrossRefGoogle ScholarPubMed
Ridker, PM, Danesh, J, Youngman, Let al. A prospective study of Helicobacter pylori seropositivity and the risk for future myocardial infarction among socioeconomically similar. US Men Ann Intern Med 2001;135: 184188. CrossRefGoogle ScholarPubMed
Whincup, PH, Mendal, MA, Perry, IJ, Strachan, DP, Walker, M. Prospective relation between Helicobacter pylori infection, coronary heart disease, and stroke in middle aged men. Heart 1996;75: 568572.CrossRefGoogle ScholarPubMed
Mino, Y, Oshima, I, Tsuda, T, Okagami, K. No relationship between schizophrenic birth and influenza epidemics in Japan. J Psychiatr Res 2000;34: 133138.CrossRefGoogle ScholarPubMed
Watson, JB, Mednick, SA, Huttunen, M, Wang, X. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 1999;11: 457466.CrossRefGoogle ScholarPubMed
Battle, YL, Martin, BC, Dorfman, JH, Miller, LS. Seasonality and infectious disease in schizophrenia: the birth hypothesis revisited. J Psychiatr Res 1999;33: 501509.CrossRefGoogle ScholarPubMed
Selten, JP, Brown, AS, Moons, KG, Slaets, JP, Susser, ES, Kahn, RS. Prenatal exposure to the. influenza pandemic and non-affective psychosis in The Netherlands. Schizophr Res 1957;1999: 8591. Google Scholar
Wahlbeck, K, Forsen, T, Osmond, C, Barker, DJ, Eriksson, JG. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch General Psychiatry 2001;58: 4852. CrossRefGoogle Scholar
Thompson, C, Syddal, H, Rodin, I, Osmond, C, Barker, D J. Birth weight and the risk of depressive disorder in late life. Br J Psychiatry 2001;179: 450455.CrossRefGoogle ScholarPubMed
Commins, S, O'Neill, LA, O'Mara, SM. The effects of the bacterial endotoxin lipopolysaccharide on synaptic transmission and plasticity in the CA1-subiculum pathway in vivo. Neuroscience 2001;102: 273380.CrossRefGoogle ScholarPubMed
Cotterel, M, Balazs, R, Johnson, AL. Effects of corticosteroids on the biochemical maturation of rat brain: postnatal cell formation. J Neurochem 1972;19: 21512167.CrossRefGoogle Scholar
Zhang, Y-H, Lu, J, Elmquist, JK, Saper, CB. Lipopolysaccharide activates specific populations of hypothalamic and brainstem neurons that project to the spinal cord. J Neurosci 2000;20: 65786586.Google ScholarPubMed
Elmquist, JK, Saper, CB. Activation of neurons projecting to the paraventricular hypothalamic nucleus by intravenous lipopolysaccharide. J Comp Neurol 1996;374: 315331.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Kronfol, Z, Remick, DG. Cytokines and the brain: Implications for clinical psychiatry. Am J Psychiatry 2000;157: 683694.CrossRefGoogle ScholarPubMed
Hennessy, MB, Deak, T, Schimi-Webb, PA. Stress-induced sickness behaviors: an alternative hypothesis for responses during maternal separation. Dev Psychobiol 2001;39: 7683.CrossRefGoogle Scholar
Rosmond, R, Dallman, MF, Bjorntorp, P. Stress-related cortisol secretion in men. relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 1998;83: 18531859.Google ScholarPubMed
Plotsky, PM, Owens, MJ, Nemeroff, CB. Psychoneuroendocrinology of depression: Hypothalamic-pituitary-adrenal axis. Psychiatr Clin North Am 1998;21: 293307.CrossRefGoogle ScholarPubMed
Stokes, PE. The potential role of excessive cortisol induced by HPA hyperfunction in the pathogenesis of depression. Eur Neuropsychopharmacol 1995;5: 7782.CrossRefGoogle Scholar
Altamura, AC, Boin, F, Maes, M. HPA axis and cytokines dysregulation in schizophrenia: potential implications for the antipsychotic treatment. Eur Neuropsychopharmacol 1999;10: 14.CrossRefGoogle Scholar
Brown, AS, Cohen, P, Harkavy-Friedman, J, Babulas, V, Malaspina, D, Gorman, JM, Susser, ES. Prenatal rubella, premorbid abnormalities, and adult schizophrenia. Biol Psychiatry 2001;49: 473486.CrossRefGoogle ScholarPubMed
Westergaard, T, Mortensen, PB, Pedersen, CB, Wohlfahrt, J, Melbye, M. Exposure to prenatal and childhood infections and the risk of schizophrenia: suggestions from a study of sibship characteristics and influenza prevalence. Arch General Psychiatry 1999;56: 993998. CrossRefGoogle ScholarPubMed