Skip to main content
SpringerLink
Log in

Epigenetic Influence of the Social Environment

  • Chapter
  • First Online:
Brain, Behavior and Epigenetics

Part of the book series: Epigenetics and Human Health ((EHH))

Abstract

Social experiences occurring during infancy have been demonstrated to exert persistent effects on neurobiological and behavioral outcomes. This social modulation of the developing brain has been observed in humans and animal models of abuse, neglect, and variation in parental style. Although the mechanisms through which these effects are achieved likely involve diverse cellular and molecular pathways, there is emerging evidence supporting the hypothesis that epigenetic changes, such as DNA methylation and histone modifications, may mediate the effects of early life variations in the social interactions between mothers and infants. Moreover, there may be plasticity within these epigenetic pathways at later developmental time points, such that the social experiences of juveniles and adults may also induce epigenetic change. These findings have implications for behavioral variation observed both within and across generations and highlight the dynamic interactions occurring between genes and environments during the course of development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahern TH, Young LJ (2009) The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster). Front Behav Neurosci 3:17

    Article  PubMed  CAS  Google Scholar 

  • Arborelius L, Eklund MB (2007) Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 145:738–750

    Article  PubMed  CAS  Google Scholar 

  • Barr CS, Newman TK, Lindell S, Becker ML, Shannon C, Champoux M, Suomi SJ, Higley JD (2004) Early experience and sex interact to influence limbic-hypothalamic-pituitary-adrenal-axis function after acute alcohol administration in rhesus macaques (Macaca mulatta). Alcohol Clin Exp Res 28:1114–1119

    Article  PubMed  CAS  Google Scholar 

  • Beckett C, Bredenkamp D, Castle J, Groothues C, O’Connor TG, Rutter M (2002) Behavior patterns associated with institutional deprivation: a study of children adopted from Romania. J Dev Behav Pediatr 23:297–303

    Article  PubMed  Google Scholar 

  • Bellinger FP, Davidson MS, Bedi KS, Wilce PA (2006) Ethanol prevents NMDA receptor reduction by maternal separation in neonatal rat hippocampus. Brain Res 1067:154–157

    Article  PubMed  CAS  Google Scholar 

  • Belz EE, Kennell JS, Czambel RK, Rubin RT, Rhodes ME (2003) Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacol Biochem Behav 76:481–486

    Article  PubMed  CAS  Google Scholar 

  • Berman C (1990) Intergenerational transmission of maternal rejection rates among free-ranging rheus monkeys on Cayo Santiago. Anim Behav 44:247–258

    Article  Google Scholar 

  • Bibancos T, Jardim DL, Aneas I, Chiavegatto S (2007) Social isolation and expression of serotonergic neurotransmission-related genes in several brain areas of male mice. Genes Brain Behav 6:529–539

    Article  PubMed  CAS  Google Scholar 

  • Bodnoff SR, Suranyi-Cadotte B, Quirion R, Meaney MJ (1987) Postnatal handling reduces novelty-induced fear and increases [3H]flunitrazepam binding in rat brain. Eur J Pharmacol 144:105–107

    Article  PubMed  CAS  Google Scholar 

  • Brake WG, Zhang TY, Diorio J, Meaney MJ, Gratton A (2004) Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci 19:1863–1874

    Article  PubMed  Google Scholar 

  • Branchi I (2009) The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci Biobehav Rev 33:551–559

    Article  PubMed  Google Scholar 

  • Branchi I, Alleva E (2006) Communal nesting, an early social enrichment, increases the adult anxiety-like response and shapes the role of social context in modulating the emotional behavior. Behav Brain Res 172:299–306

    Article  PubMed  Google Scholar 

  • Branchi I, D’Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E (2006a) Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psychiatry 60:690–696

    Article  PubMed  CAS  Google Scholar 

  • Branchi I, D’Andrea I, Sietzema J, Fiore M, Di Fausto V, Aloe L, Alleva E (2006b) Early social enrichment augments adult hippocampal BDNF levels and survival of BrdU-positive cells while increasing anxiety- and “depression”-like behavior. J Neurosci Res 83:965–973

    Article  PubMed  CAS  Google Scholar 

  • Branchi I, D’Andrea I, Cirulli F, Lipp HP, Alleva E (2009) Shaping brain development: mouse communal nesting blunts adult neuroendocrine and behavioral response to social stress and modifies chronic antidepressant treatment outcome. Psychoneuroendocrinology 35:743–751

    Article  PubMed  CAS  Google Scholar 

  • Bredy TW, Humpartzoomian RA, Cain DP, Meaney MJ (2003) Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience 118:571–576

    Article  PubMed  CAS  Google Scholar 

  • Bredy TW, Zhang TY, Grant RJ, Diorio J, Meaney MJ (2004) Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. Eur J Neurosci 20:1355–1362

    Article  PubMed  Google Scholar 

  • Bredy TW, Brown RE, Meaney MJ (2007) Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus). Eur J Neurosci 25:567–575

    Article  PubMed  Google Scholar 

  • Burton CL, Chatterjee D, Chatterjee-Chakraborty M, Lovic V, Grella SL, Steiner M, Fleming AS (2007) Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Res 1158:28–38

    Article  PubMed  CAS  Google Scholar 

  • Buwalda B, de Boer SF, Schmidt ED, Felszeghy K, Nyakas C, Sgoifo A, Van der Vegt BJ, Tilders FJ, Bohus B, Koolhaas JM (1999) Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats. J Neuroendocrinol 11:513–520

    Article  PubMed  CAS  Google Scholar 

  • Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ (2000) The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22:219–229

    Article  PubMed  CAS  Google Scholar 

  • Caldji C, Diorio J, Meaney MJ (2003) Variations in maternal care alter GABA(A) receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology 28:1950–1959

    PubMed  CAS  Google Scholar 

  • Caldji C, Diorio J, Anisman H, Meaney MJ (2004) Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 29:1344–1352

    Article  PubMed  CAS  Google Scholar 

  • Carlson EA (1998) A prospective longitudinal study of attachment disorganization/disorientation. Child Dev 69:1107–1128

    PubMed  CAS  Google Scholar 

  • Carlson EA, Egeland B, Sroufe LA (2009) A prospective investigation of the development of borderline personality symptoms. Dev Psychopathol 21:1311–1334

    Article  PubMed  Google Scholar 

  • Carroll KA, Maestripieri D (1998) Infant abuse and neglect in monkeys–a discussion of definitions, epidemiology, etiology, and implications for child maltreatment: reply to Cicchetti (1998) and Mason (1998). Psychol Bull 123:234–237

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Meaney MJ (2006) Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 59:1227–1235

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Meaney MJ (2007) Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121:1353–1363

    Article  PubMed  Google Scholar 

  • Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736–12741

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Francis DD, Mar A, Meaney MJ (2003a) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359–371

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ (2003b) Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144:4720–4724

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ (2006) Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147:2909–2915

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA, Curley JP, Keverne EB, Bateson PP (2007) Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav 91:325–334

    Article  PubMed  CAS  Google Scholar 

  • Chugani HT, Behen ME, Muzik O, Juhasz C, Nagy F, Chugani DC (2001) Local brain functional activity following early deprivation: a study of postinstitutionalized Romanian orphans. Neuroimage 14:1290–1301

    Article  PubMed  CAS  Google Scholar 

  • Cooper MA, Huhman KL (2007) Corticotropin-releasing factor receptors in the dorsal raphe nucleus modulate social behavior in Syrian hamsters. Psychopharmacology (Berl) 194:297–307

    Article  CAS  Google Scholar 

  • Coplan JD, Rosenblum LA, Gorman JM (1995) Primate models of anxiety. Longitudinal perspectives. Psychiatr Clin North Am 18:727–743

    PubMed  CAS  Google Scholar 

  • Coplan JD, Trost RC, Owens MJ, Cooper TB, Gorman JM, Nemeroff CB, Rosenblum LA (1998) Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Arch Gen Psychiatry 55:473–477

    Article  PubMed  CAS  Google Scholar 

  • Coplan JD, Smith EL, Altemus M, Scharf BA, Owens MJ, Nemeroff CB, Gorman JM, Rosenblum LA (2001) Variable foraging demand rearing: sustained elevations in cisternal cerebrospinal fluid corticotropin-releasing factor concentrations in adult primates. Biol Psychiatry 50:200–204

    Article  PubMed  CAS  Google Scholar 

  • Coplan JD, Altemus M, Mathew SJ, Smith EL, Sharf B, Coplan PM, Kral JG, Gorman JM, Owens MJ, Nemeroff CB, Rosenblum LA (2005) Synchronized maternal-infant elevations of primate CSF CRF concentrations in response to variable foraging demand. CNS Spectr 10:530–536

    PubMed  Google Scholar 

  • Coplan JD, Smith EL, Altemus M, Mathew SJ, Perera T, Kral JG, Gorman JM, Owens MJ, Nemeroff CB, Rosenblum LA (2006) Maternal-infant response to variable foraging demand in nonhuman primates: effects of timing of stressor on cerebrospinal fluid corticotropin-releasing factor and circulating glucocorticoid concentrations. Ann NY Acad Sci 1071:525–533

    Article  PubMed  CAS  Google Scholar 

  • Coutellier L, Friedrich AC, Failing K, Marashi V, Wurbel H (2009) Effects of foraging demand on maternal behaviour and adult offspring anxiety and stress response in C57BL/6 mice. Behav Brain Res 196:192–199

    Article  PubMed  Google Scholar 

  • Curley JP, Davidson S, Bateson P, Champagne FA (2009) Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Front Behav Neurosci 3:25

    Article  PubMed  CAS  Google Scholar 

  • Erhardt A, Muller MB, Rodel A, Welt T, Ohl F, Holsboer F, Keck ME (2009) Consequences of chronic social stress on behaviour and vasopressin gene expression in the PVN of DBA/2OlaHsd mice–influence of treatment with the CRHR1-antagonist R121919/NBI 30775. J Psychopharmacol 23:31–39

    Article  PubMed  CAS  Google Scholar 

  • Fairbanks LA, McGuire MT (1988) Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21:711–724

    Article  PubMed  CAS  Google Scholar 

  • Fan G, Hutnick L (2005) Methyl-CpG binding proteins in the nervous system. Cell Res 15:255–261

    Article  PubMed  CAS  Google Scholar 

  • Feng J, Fouse S, Fan G (2007) Epigenetic regulation of neural gene expression and neuronal function. Pediatr Res 61:58R–63R

    Article  PubMed  CAS  Google Scholar 

  • Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178–182

    Article  PubMed  CAS  Google Scholar 

  • Fleming A (1986) Psychobiology of rat maternal behavior: how and where hormones act to promote maternal behavior at parturition. Ann NY Acad Sci 474:234–251

    Article  PubMed  CAS  Google Scholar 

  • Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158

    Article  PubMed  CAS  Google Scholar 

  • Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145–1148

    Article  PubMed  CAS  Google Scholar 

  • Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002a) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843

    PubMed  CAS  Google Scholar 

  • Francis DD, Young LJ, Meaney MJ, Insel TR (2002b) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353

    Article  PubMed  CAS  Google Scholar 

  • Frick KM, Stearns NA, Pan JY, Berger-Sweeney J (2003) Effects of environmental enrichment on spatial memory and neurochemistry in middle-aged mice. Learn Mem 10:187–198

    Article  PubMed  Google Scholar 

  • Fries AB, Ziegler TE, Kurian JR, Jacoris S, Pollak SD (2005) Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proc Natl Acad Sci USA 102:17237–17240

    Article  PubMed  CAS  Google Scholar 

  • Fries AB, Shirtcliff EA, Pollak SD (2008) Neuroendocrine dysregulation following early social deprivation in children. Dev Psychobiol 50:588–599

    Article  PubMed  CAS  Google Scholar 

  • Fukuda S, Taga T (2005) Cell fate determination regulated by a transcriptional signal network in the developing mouse brain. Anat Sci Int 80:12–18

    Article  PubMed  CAS  Google Scholar 

  • Gerra G, Leonardi C, Cortese E, Zaimovic A, Dell’Agnello G, Manfredini M, Somaini L, Petracca F, Caretti V, Baroni C, Donnini C (2008) Adrenocorticotropic hormone and cortisol plasma levels directly correlate with childhood neglect and depression measures in addicted patients. Addict Biol 13:95–104

    Article  PubMed  CAS  Google Scholar 

  • Gorman JM, Mathew S, Coplan J (2002) Neurobiology of early life stress: nonhuman primate models. Semin Clin Neuropsychiatry 7:96–103

    Article  PubMed  Google Scholar 

  • Grassi-Oliveira R, Stein LM, Lopes RP, Teixeira AL, Bauer ME (2008) Low plasma brain-derived neurotrophic factor and childhood physical neglect are associated with verbal memory impairment in major depression – a preliminary report. Biol Psychiatry 64:281–285

    Article  PubMed  CAS  Google Scholar 

  • Grippo AJ, Cushing BS, Carter CS (2007a) Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom Med 69:149–157

    Article  PubMed  Google Scholar 

  • Grippo AJ, Gerena D, Huang J, Kumar N, Shah M, Ughreja R, Carter CS (2007b) Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32:966–980

    Article  PubMed  CAS  Google Scholar 

  • Hall WG (1975) Weaning and growth of artificially reared rats. Science 190:1313–1315

    Article  PubMed  CAS  Google Scholar 

  • Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. Proc Natl Acad Sci USA 54:90–97

    Article  PubMed  CAS  Google Scholar 

  • Heritch AJ, Henderson K, Westfall TC (1990) Effects of social isolation on brain catecholamines and forced swimming in rats: prevention by antidepressant treatment. J Psychiatr Res 24:251–258

    Article  PubMed  CAS  Google Scholar 

  • Ichise M, Vines DC, Gura T, Anderson GM, Suomi SJ, Higley JD, Innis RB (2006) Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J Neurosci 26:4638–4643

    Article  PubMed  CAS  Google Scholar 

  • Insel TR (1989) Decreased in vivo binding to brain benzodiazepine receptors during social isolation. Psychopharmacology (Berl) 97:142–144

    Article  CAS  Google Scholar 

  • Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Ann NY Acad Sci 981:82–96

    Article  PubMed  Google Scholar 

  • Jankowsky JL, Melnikova T, Fadale DJ, Xu GM, Slunt HH, Gonzales V, Younkin LH, Younkin SG, Borchelt DR, Savonenko AV (2005) Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer’s disease. J Neurosci 25:5217–5224

    Article  PubMed  CAS  Google Scholar 

  • Johnson JG, Cohen P, Brown J, Smailes EM, Bernstein DP (1999) Childhood maltreatment increases risk for personality disorders during early adulthood. Arch Gen Psychiatry 56:600–606

    Article  PubMed  CAS  Google Scholar 

  • Keeney AJ, Hogg S (1999) Behavioural consequences of repeated social defeat in the mouse: preliminary evaluation of a potential animal model of depression. Behav Pharmacol 10:753–764

    Article  PubMed  CAS  Google Scholar 

  • Korosi A, Baram TZ (2009) The pathways from mother’s love to baby’s future. Front Behav Neurosci 3:27

    Article  PubMed  CAS  Google Scholar 

  • Korosi A, Shanabrough M, McClelland S, Liu ZW, Borok E, Gao XB, Horvath TL, Baram TZ (2010) Early-life experience reduces excitation to stress-responsive hypothalamic neurons and reprograms the expression of corticotropin-releasing hormone. J Neurosci 30:703–713

    Article  PubMed  CAS  Google Scholar 

  • Krugers HJ, Koolhaas JM, Bohus B, Korf J (1993) A single social stress-experience alters glutamate receptor-binding in rat hippocampal CA3 area. Neurosci Lett 154:73–77

    Article  PubMed  CAS  Google Scholar 

  • Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Plotsky PM (2004) Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry 55:367–375

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Rea M, Morley-Fletcher S, Di Carlo S, Bacosi A, De Simone R, Bertini M, Pacifici R (2004) Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur J Neurosci 20:1655–1664

    Article  PubMed  Google Scholar 

  • Law AJ, Pei Q, Feldon J, Pryce CR, Harrison PJ (2009a) Gene expression in the anterior cingulate cortex and amygdala of adolescent marmoset monkeys following parental separations in infancy. Int J Neuropsychopharmacol 12:761–772

    Article  PubMed  CAS  Google Scholar 

  • Law AJ, Pei Q, Walker M, Gordon-Andrews H, Weickert CS, Feldon J, Pryce CR, Harrison PJ (2009b) Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder. Neuropsychopharmacology 34:1381–1394

    Article  PubMed  CAS  Google Scholar 

  • Lee RJ, Gollan J, Kasckow J, Geracioti T, Coccaro EF (2006) CSF corticotropin-releasing factor in personality disorder: relationship with self-reported parental care. Neuropsychopharmacology 31:2289–2295

    PubMed  CAS  Google Scholar 

  • Lehmann J, Pryce CR, Bettschen D, Feldon J (1999) The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 64:705–715

    Article  PubMed  CAS  Google Scholar 

  • Levine S (1957) Infantile experience and resistance to physiological stress. Science 126:405

    Article  PubMed  CAS  Google Scholar 

  • Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97:1064–1073

    Article  PubMed  CAS  Google Scholar 

  • Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 100:278–282

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3:799–806

    Article  PubMed  CAS  Google Scholar 

  • Lovic V, Fleming AS (2004) Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task–reversal of effects with maternal-like licking stimulation. Behav Brain Res 148:209–219

    Article  PubMed  Google Scholar 

  • Lovic V, Gonzalez A, Fleming AS (2001) Maternally separated rats show deficits in maternal care in adulthood. Dev Psychobiol 39:19–33

    Article  PubMed  CAS  Google Scholar 

  • Lu L, Bao G, Chen H, Xia P, Fan X, Zhang J, Pei G, Ma L (2003) Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp Neurol 183:600–609

    Article  PubMed  Google Scholar 

  • Lukas M, Bredewold R, Neumann ID, Veenema AH (2010) Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 58:78–87

    Article  PubMed  CAS  Google Scholar 

  • Lukkes JL, Watt MJ, Lowry CA, Forster GL (2009) Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 3:18

    Article  PubMed  CAS  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445

    Article  PubMed  CAS  Google Scholar 

  • MacLean K (2003) The impact of institutionalization on child development. Dev Psychopathol 15:853–884

    Article  PubMed  Google Scholar 

  • Maestripieri D (1998) Parenting styles of abusive mothers in group-living rhesus macaques. Anim Behav 55:1–11

    Article  PubMed  Google Scholar 

  • Maestripieri D, Lindell SG, Ayala A, Gold PW, Higley JD (2005) Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neurosci Biobehav Rev 29:51–57

    Article  PubMed  Google Scholar 

  • Maestripieri D, Higley JD, Lindell SG, Newman TK, McCormack KM, Sanchez MM (2006) Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behav Neurosci 120:1017–1024

    Article  PubMed  Google Scholar 

  • Mathew SJ, Shungu DC, Mao X, Smith EL, Perera GM, Kegeles LS, Perera T, Lisanby SH, Rosenblum LA, Gorman JM, Coplan JD (2003) A magnetic resonance spectroscopic imaging study of adult nonhuman primates exposed to early-life stressors. Biol Psychiatry 54:727–735

    Article  PubMed  CAS  Google Scholar 

  • McCormack K, Sanchez MM, Bardi M, Maestripieri D (2006) Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev Psychobiol 48:537–550

    Article  PubMed  CAS  Google Scholar 

  • McGowan PO, Sasaki A, Huang TC, Unterberger A, Suderman M, Ernst C, Meaney MJ, Turecki G, Szyf M (2008) Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS ONE 3:e2085

    Article  PubMed  CAS  Google Scholar 

  • McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonte B, Szyf M, Turecki G, Meaney MJ (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342–348

    Article  PubMed  CAS  Google Scholar 

  • McLeod J, Sinal CJ, Perrot-Sinal TS (2007) Evidence for non-genomic transmission of ecological information via maternal behavior in female rats. Genes Brain Behav 6:19–29

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ, Aitken DH (1985) The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res 354:301–304

    PubMed  CAS  Google Scholar 

  • Meaney MJ, Aitken DH, Bodnoff SR, Iny LJ, Tatarewicz JE, Sapolsky RM (1985) Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav Neurosci 99:765–770

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ, Aitken DH, Viau V, Sharma S, Sarrieau A (1989) Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50:597–604

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ, Mitchell JB, Aitken DH, Bhatnagar S, Bodnoff SR, Iny LJ, Sarrieau A (1991) The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology 16:85–103

    Article  PubMed  CAS  Google Scholar 

  • Mehta MA, Golembo NI, Nosarti C, Colvert E, Mota A, Williams SC, Rutter M, Sonuga-Barke EJ (2009) Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. J Child Psychol Psychiatry 50:943–951

    Article  PubMed  Google Scholar 

  • Miachon S, Manchon M, Fromentin JR, Buda M (1990) Isolation-induced changes in radioligand binding to benzodiazepine binding sites. Neurosci Lett 111:246–251

    Article  PubMed  CAS  Google Scholar 

  • Miller LG, Thompson ML, Greenblatt DJ, Deutsch SI, Shader RI, Paul SM (1987) Rapid increase in brain benzodiazepine receptor binding following defeat stress in mice. Brain Res 414:395–400

    Article  PubMed  CAS  Google Scholar 

  • Moore CL, Power KL (1986) Prenatal stress affects mother-infant interaction in Norway rats. Dev Psychobiol 19:235–245

    Article  PubMed  CAS  Google Scholar 

  • Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23:314–318

    Article  PubMed  CAS  Google Scholar 

  • Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374

    Article  PubMed  Google Scholar 

  • Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28:9055–9065

    Article  PubMed  CAS  Google Scholar 

  • Murgatroyd C, Wigger A, Frank E, Singewald N, Bunck M, Holsboer F, Landgraf R, Spengler D (2004) Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J Neurosci 24:7762–7770

    Article  PubMed  CAS  Google Scholar 

  • Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12:1559–1566

    Article  PubMed  CAS  Google Scholar 

  • Narita K, Takei Y, Suda M, Aoyama Y, Uehara T, Kosaka H, Amanuma M, Fukuda M, Mikuni M (2010) Relationship of parental bonding styles with gray matter volume of dorsolateral prefrontal cortex in young adults. Prog Neuropsychopharmacol Biol Psychiatry 34:624–631

    Article  PubMed  Google Scholar 

  • Neigh GN, Gillespie CF, Nemeroff CB (2009) The neurobiological toll of child abuse and neglect. Trauma Violence Abuse 10:389–410

    Article  PubMed  Google Scholar 

  • O’Connor TG, Rutter M (2000) Attachment disorder behavior following early severe deprivation: extension and longitudinal follow-up. English and Romanian Adoptees Study Team. J Am Acad Child Adolesc Psychiatry 39:703–712

    Article  PubMed  Google Scholar 

  • O’Connor TG, Rutter M, Beckett C, Keaveney L, Kreppner JM (2000) The effects of global severe privation on cognitive competence: extension and longitudinal follow-up. English and Romanian adoptees study team. Child Dev 71:376–390

    Article  PubMed  Google Scholar 

  • Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM (2008) Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3:97–106

    Article  PubMed  Google Scholar 

  • Ognibene E, Adriani W, Caprioli A, Ghirardi O, Ali SF, Aloe L, Laviola G (2008) The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous reeler mice. Prog Neuropsychopharmacol Biol Psychiatry 32:1269–1276

    Article  PubMed  CAS  Google Scholar 

  • Olsson T, Mohammed AH, Donaldson LF, Henriksson BG, Seckl JR (1994) Glucocorticoid receptor and NGFI-A gene expression are induced in the hippocampus after environmental enrichment in adult rats. Brain Res Mol Brain Res 23:349–353

    Article  PubMed  CAS  Google Scholar 

  • Onishchenko N, Karpova N, Sabri F, Castren E, Ceccatelli S (2008) Long-lasting depression-like behavior and epigenetic changes of BDNF gene expression induced by perinatal exposure to methylmercury. J Neurochem 106:1378–1387

    Article  PubMed  CAS  Google Scholar 

  • Parker G (1993) Parental rearing style: examining for links with personality vulnerability factors for depression. Soc Psychiatry Psychiatr Epidemiol 28:97–100

    Article  PubMed  CAS  Google Scholar 

  • Parker G, Tupling H, Brown LB (1979) A parental bonding instrument. Br J Med Psychol 52:1–10

    Google Scholar 

  • Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551

    Article  PubMed  CAS  Google Scholar 

  • Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006) Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099:101–108

    Article  PubMed  CAS  Google Scholar 

  • Plotsky PM, Meaney MJ (1993) 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 18:195–200

    Article  PubMed  CAS  Google Scholar 

  • Pruessner JC, Champagne F, Meaney MJ, Dagher A (2004) Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci 24:2825–2831

    Article  PubMed  CAS  Google Scholar 

  • Rao H, Betancourt L, Giannetta JM, Brodsky NL, Korczykowski M, Avants BB, Gee JC, Wang J, Hurt H, Detre JA, Farah MJ (2010) Early parental care is important for hippocampal maturation: evidence from brain morphology in humans. Neuroimage 49:1144–1150

    Article  PubMed  Google Scholar 

  • Razin A (1998) CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 17:4905–4908

    Article  PubMed  CAS  Google Scholar 

  • Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517–529

    Article  PubMed  CAS  Google Scholar 

  • Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA (2002) Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 7:609–616

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld P, Wetmore JB, Levine S (1992) Effects of repeated maternal separations on the adrenocortical response to stress of preweanling rats. Physiol Behav 52:787–791

    Article  PubMed  CAS  Google Scholar 

  • Roth TL, Sullivan RM (2005) Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol Psychiatry 57:823–831

    Article  PubMed  Google Scholar 

  • Roth TL, Lubin FD, Funk AJ, Sweatt JD (2009) Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65:760–769

    Article  PubMed  CAS  Google Scholar 

  • Roy A (2002) Self-rated childhood emotional neglect and CSF monoamine indices in abstinent cocaine-abusing adults: possible implications for suicidal behavior. Psychiatry Res 112:69–75

    Article  PubMed  CAS  Google Scholar 

  • Rutter M, O’Connor TG (2004) Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. Dev Psychol 40:81–94

    Article  PubMed  Google Scholar 

  • Seay B, Harlow HF (1965) Maternal separation in the rhesus monkey. J Nerv Ment Dis 140:434–441

    Article  PubMed  CAS  Google Scholar 

  • Segovia G, Yague AG, Garcia-Verdugo JM, Mora F (2006) Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 70:8–14

    Article  PubMed  CAS  Google Scholar 

  • Seth KA, Majzoub JA (2001) Repressor element silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) can act as an enhancer as well as a repressor of corticotropin-releasing hormone gene transcription. J Biol Chem 276:13917–13923

    PubMed  CAS  Google Scholar 

  • Shannon C, Schwandt ML, Champoux M, Shoaf SE, Suomi SJ, Linnoila M, Higley JD (2005) Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants. Am J Psychiatry 162:1658–1664

    Article  PubMed  Google Scholar 

  • Shao F, Jin J, Meng Q, Liu M, Xie X, Lin W, Wang W (2009) Pubertal isolation alters latent inhibition and DA in nucleus accumbens of adult rats. Physiol Behav 98:251–257

    Article  PubMed  CAS  Google Scholar 

  • Silva-Gomez AB, Rojas D, Juarez I, Flores G (2003) Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128–136

    Article  PubMed  CAS  Google Scholar 

  • Spinelli S, Chefer S, Suomi SJ, Higley JD, Barr CS, Stein E (2009) Early-life stress induces long-term morphologic changes in primate brain. Arch Gen Psychiatry 66:658–665

    Article  PubMed  Google Scholar 

  • Spinelli S, Chefer S, Carson RE, Jagoda E, Lang L, Heilig M, Barr CS, Suomi SJ, Higley JD, Stein EA (2010) Effects of early-life stress on serotonin(1A) receptors in juvenile rhesus monkeys measured by positron emission tomography. Biol Psychiatry 67:1146–1153

    Article  PubMed  CAS  Google Scholar 

  • Sroufe LA (2005) Attachment and development: a prospective, longitudinal study from birth to adulthood. Attach Hum Dev 7:349–367

    Article  PubMed  Google Scholar 

  • Sroufe LA, Carlson EA, Levy AK, Egeland B (1999) Implications of attachment theory for developmental psychopathology. Dev Psychopathol 11:1–13

    Article  PubMed  CAS  Google Scholar 

  • Stranahan AM, Khalil D, Gould E (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9:526–533

    Article  PubMed  CAS  Google Scholar 

  • Suomi SJ (1991) Early stress and adult emotional reactivity in rhesus monkeys. Ciba Found Symp 156:171–183

    PubMed  CAS  Google Scholar 

  • Suomi SJ, Harlow HF, Kimball SD (1971) Behavioral effects of prolonged partial social isolation in the rhesus monkey. Psychol Rep 29:1171–1177

    PubMed  CAS  Google Scholar 

  • Trickett P, McBride-Chang C (1995) The developmental impact of different forms of child abuse and neglect. Dev Rev 15:11–37

    Article  Google Scholar 

  • Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519–525

    Article  PubMed  CAS  Google Scholar 

  • Turner B (2001) Chromatin and gene regulation. Blackwell Science Ltd, Oxford

    Book  Google Scholar 

  • van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ (2000) Delaying the onset of Huntington’s in mice. Nature 404:721–722

    Article  PubMed  Google Scholar 

  • Vazquez DM, Bailey C, Dent GW, Okimoto DK, Steffek A, Lopez JF, Levine S (2006) Brain corticotropin-releasing hormone (CRH) circuits in the developing rat: effect of maternal deprivation. Brain Res 1121:83–94

    Article  PubMed  CAS  Google Scholar 

  • Veenema AH, Neumann ID (2007) Neurobiological mechanisms of aggression and stress coping: a comparative study in mouse and rat selection lines. Brain Behav Evol 70:274–285

    Article  PubMed  Google Scholar 

  • Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID (2006) Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur J Neurosci 24:1711–1720

    Article  PubMed  Google Scholar 

  • Viau V, Sharma S, Plotsky PM, Meaney MJ (1993) Increased plasma ACTH responses to stress in nonhandled compared with handled rats require basal levels of corticosterone and are associated with increased levels of ACTH secretagogues in the median eminence. J Neurosci 13:1097–1005

    PubMed  CAS  Google Scholar 

  • Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    Article  PubMed  CAS  Google Scholar 

  • Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, Szyf M (2005) Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25:11045–11054

    Article  PubMed  CAS  Google Scholar 

  • Weaver IC, D’Alessio AC, Brown SE, Hellstrom IC, Dymov S, Sharma S, Szyf M, Meaney MJ (2007) The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 27:1756–1768

    Article  PubMed  CAS  Google Scholar 

  • Weizman R, Lehmann J, Leschiner S, Allmann I, Stoehr T, Heidbreder C, Domeney A, Feldon J, Gavish M (1999) Long-lasting effect of early handling on the peripheral benzodiazepine receptor. Pharmacol Biochem Behav 64:725–729

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson MB, Xiao G, Kumar A, LaPlant Q, Renthal W, Sikder D, Kodadek TJ, Nestler EJ (2009) Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J Neurosci 29:7820–7832

    Article  PubMed  CAS  Google Scholar 

  • Winslow JT (2005) Neuropeptides and non-human primate social deficits associated with pathogenic rearing experience. Int J Dev Neurosci 23:245–251

    Article  PubMed  CAS  Google Scholar 

  • Zakharova E, Miller J, Unterwald E, Wade D, Izenwasser S (2009) Social and physical environment alter cocaine conditioned place preference and dopaminergic markers in adolescent male rats. Neuroscience 163:890–897

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Reinberg D (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15:2343–2360

    Article  PubMed  CAS  Google Scholar 

  • Zhang TY, Chretien P, Meaney MJ, Gratton A (2005) Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. J Neurosci 25:1493–1502

    Article  PubMed  CAS  Google Scholar 

  • Zheng D, Zhao K, Mehler MF (2009) Profiling RE1/REST-mediated histone modifications in the human genome. Genome Biol 10:R9

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by Grant Number DP2OD001674 from the Office of the Director, National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Psychology, Columbia University, Schermerhorn Hall, 1190 Amsterdam Avenue, New York, NY, 10027, USA

    Frances A. Champagne & James P. Curley

Authors
  1. Frances A. Champagne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James P. Curley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frances A. Champagne .

Editor information

Editors and Affiliations

  1. , The Krembil Family Epigenetics Laborator, Centre for Addiction and Mental Health, College Street 250, Toronto, M5T 1R8, Ontario, Canada

    Arturas Petronis

  2. , Institute of Psychiatry, King's College London, De Crispigny Park, London, SE5 8AF, United Kingdom

    Jonathan Mill

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Champagne, F.A., Curley, J.P. (2011). Epigenetic Influence of the Social Environment. In: Petronis, A., Mill, J. (eds) Brain, Behavior and Epigenetics. Epigenetics and Human Health. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-17426-1_10

Download citation

Publish with us

Policies and ethics

Search

Navigation