Abstract
During the perinatal period, the brain undergoes substantial structural changes, synaptic rearrangements, and development of neuronal circuits which ultimately determine brain function and behavior. Environmental factors—such as exposure to adverse experiences—have major impact on brain function and structure during this sensitive period. These alterations can be long-lasting, and have been implicated in psychopathology such as cognitive decline and emotional dysfunction. Here we briefly review how early postnatal adversity determines structure and function of the hippocampus, amygdala, and prefrontal cortex (PFC) areas, which are crucial for proper cognitive and emotional function.
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References
Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ (2007) Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology. 32:256–266
Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joëls M (2009) Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 92:292–300
Bagot RC, Tse YC, Nguyen HB, Wong AS, Meaney MJ, Wong TP (2012) Maternal care influences hippocampal N-methyl-D-aspartate receptor function and dynamic regulation by corticosterone in adulthood. Biol Psychiatry 72:491–498
Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, Stern H (2012) Fragmentation and unpredictability of early-life experience in mental disorders. Am J Psychiatry 169:907–915
Baudin A, Blot K, Verney C, Estevez L, Santamaria J, Gressens P, Giros B, Otani S, Daugé V, Naudon L (2012) Maternal deprivation induces deficits in temporal memory and cognitive flexibility and exaggerates synaptic plasticity in the rat medial prefrontal cortex. Neurobiol Learn Mem 98:207–214
Belsky J, Fearon RMP (2002) Early attachment security, subsequent maternal sensitivity, and later child development: does continuity in development depend upon continuity of caregiving? Attach Hum Dev 4:361–387
Bock J, Gruss M, Becker S, Braun K (2005) Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 15:802–808
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
Brunson KL, Kramár E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ (2005) Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 25:9328–9338
Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335–5340
Caldji C, Diorio J, Meaney MJ (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48:1164–1174
Carballedo A, Morris D, Zill P, Fahey C, Reinhold E, Meisenzahl E, Bondy B, Gill M, Möller HJ, Frodl T (2013) Brain-derived neurotrophic factor Val66Met polymorphism and early life adversity affect hippocampal volume. Am J Med Genet B Neuropsychiatr Genet 162:183–190
Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, Joëls M, Krugers H (2008) Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 28:6037–6045
Champagne DL, de Kloet ER, Joëls M (2009) Fundamental aspects of the impact of glucocorticoids on the (immature) brain. Semin Fetal Neonatal Med 14:136–142
Cohen MM, Jing D, Yang RR, Tottenham N, Lee FS, Casey BJ (2013) Early-life stress has persistent effects on amygdala function and development in mice and humans. Proc Natl Acad Sci USA 110:18274–18278
De Wolff MS, van Ijzendoorn MH (1997) Sensitivity and attachment: a meta-analysis on parental antecedents of infant attachment. Child Dev 68:571–591
De Kloet ER, Rosenfeld P, Van Eekelen JA, Sutanto W, Levine S (1988) Stress, glucocorticoids and development. Prog Brain Res 73:101–120
Egeland B, Sroufe LA, Erickson M (1983) The developmental consequence of different patterns of maltreatment. Child Abuse Negl 7:459–469
Egeland B, Farber EA (1984) Infant-mother attachment: factors related to its development and changes over time. Child Dev 55:753–771
Ellis BH, Fisher PA, Zaharie S (2004) Predictors of disruptive behavior, developmental delays, anxiety, and affective symptomatology among institutionally reared romanian children. J Am Acad Child Adolesc Psychiatry 43:1283–1292
Farah MJ, Shera DM, Savage JH, Betancourt L, Giannetta JM, Brodsky NL, Malmud EK, Hurt H (2006) Childhood poverty: specific associations with neurocognitive development. Brain Res 1110:166–174
Gee DG, Barad-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH, Hare TA, Bookheimer SY, Tottenham N (2013) Earlt developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci USA 110:15638–15643
Hackman DA, Farah MJ, Meaney MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev Neurosci 11:651–659
Herringa RJ, Birn RM, Ruttle PL, Burghy CA, Stodola DE, Davidson RJ, Essex MJ (2013) Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proc Natl Acad Sci USA 110:19119–19124
Kendler KS, Thornton LM, Gardner CO (2000) Stressful life events and previous episodes in the etiology of major depression in women: an evaluation of the “kindling” hypothesis. Am J Psychiatry 157:1243–1251
Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340–350
Kim P, Evans GW, Angstadt M, Ho SS, Sripada CS, Swain JE, Liberzon I, Phan KL (2013) Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proc Natl Acad Sci USA 110:18442–18447
Kishiyama MM, Boyce WT, Jimenez AM, Perry LM, Knight RT (2009) Socioeconomic disparities affect prefrontal function in children. J Cogn Neurosci 21:1106–1115
Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM, Pace TW, Mercer KB, Mayberg HS, Bradley B, Nemeroff CB, Holsboer F, Heim CM, Ressler KJ, Rein T, Binder EB (2013) Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 16:33–41
Korosi A, Naninck EFG, Oomen CA, Schouten M, Krugers H, Fitzsimons C, Lucassen PJ (2012) Early-life stress mediated modulation of adult neurogenesis and behavior. Behav Brain Res 227:400–409
Krugers HJ, Oomen CA, Gumbs M, Li M, Velzing EH, Joels M, Lucassen PJ (2012) Maternal deprivation and dendritic complexity in the basolateral amygdala. Neuropharmacology 62:534–537
Lehmann J, Russig H, Feldon J, Pryce CR (2002) Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav 73:141–145
Lejeune S, Dourmap N, Martres MP, Giros B, Daugé V, Naudon L (2013) The dopamine D1 receptor agonist SKF 38393 improves temporal order memory performance in maternally deprived rats. Neurobiol Learn Mem 106:268–273
Levine S (1994) The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors. Ann N Y Acad Sci 746:275–288
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
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
Lupien SJ, Parent S, Evans AC, Tremblay RE, Zelazo PD, Corbo V, Pruessner JC, Séguin JR (2011) Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci USA 108:14324–14329
Macrí S, Mason GJ, Würbel H (2004) Dissociation in the effects of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur J Neurosci 20:1017–1024
McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonté 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
Meaney MJ, Aitken DH, van Berkel C, Bhatnagar S, Sapolsky RM (1988) Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239:766–768
Monroy E, Hernández-Torres E, Flores G (2010) Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J Chem Neuroanat 40:93–101
Nederhof E, Schmidt MV (2012) Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol Behav 106:691–700
Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9:65–75
Noble KG, McCandliss BD, Farah MJ (2007) Socioeconomic gradients predict individual differences in neurocognitive abilities. Dev Sci 10:464–480
Oomen CA, Girardi CE, Cahyadi R, Verbeek EC, Krugers H, Joëls M, Lucassen PJ (2009) Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS ONE 4:e3675
Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Lucassen PJ, Krugers H (2010) Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci 30:6635–6645
Pascual R, Zamora-León SP (2007) Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiol Exp 67:471–479
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
Pryce CR, Feldon J (2003) Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 27:57–71
Rao U, Chen LA, Bidesi AS, Shad MU, Thomas MA, Hammen CL (2010) Hippocampal changes associated with early-life adversity and vulnerability to depression. Biol Psychiatry 67:357–364
Rice CJ, Sandman CA, Lenjavi MR, Baram TZ (2008) A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149:4892–4900
Rodenas-Ruano A, Chávez AE, Cossio MJ, Castillo PE, Zukin RS (2012) REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat Neurosci 15:1382–1390
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
Sapolsky RM, Meaney MJ (1986) Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396:64–76
Schmidt MV, Oitzl MS, Levine S, de Kloet ER (2002) The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Res Dev Brain Res 139:39–49
Sroufe LA (2005) Attachment and development: a prospective, longitudinal study from birth to adulthood. Attach Hum Dev 7:349–367
Stanton ME, Gutierrez YR, Levine S (1988) Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behav Neurosci 102:692–700
Suderman M, McGowan PO, Sasaki A, Huang TC, Hallett MT, Meaney MJ, Turecki G, Szyf M (2012) Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc Natl Acad Sci USA 109:17266–17272
Teicher MH, Samson JA, Polcari A, McGreenery CE (2006) Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. Am J Psychiatry 163:993–1000
Teicher MH, Anderson CM, Polcari A (2012) Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci USA 109:563–572
Touma C, Gassen NC, Herrmann L, Cheung-Flynn J, Büll DR, Ionescu IA, Heinzmann JM, Knapman A, Siebertz A, Depping AM, Hartmann J, Hausch F, Schmidt MV, Holsboer F, Ising M, Cox MB, Schmidt U, Rein T (2011) FK506 binding protein 5 shapes stress responsiveness: modulation of neuroendocrine reactivity and coping behavior. Biol Psychiatry 70:928–936
van Harmelen AL, de Jong PJ, Glashouwer KA, Spinhoven P, Penninx BW, Elzinga BM (2010) Child abuse and negative explicit and automatic self-associations: the cognitive scars of emotional maltreatment. Behav Res Ther 48:486–494
van Harmelen AL, van Tol MJ, Demenescu LR, van der Wee NJ, Veltman DJ, Aleman A, van Buchem MA, Spinhoven P, Penninx BW, Elzinga BM (2013) Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Soc Cogn Affect Neurosci 8:362–369
van Hasselt FN, Cornelisse S, Zhang TY, Meaney MJ, Velzing EH, Krugers HJ, Joëls M (2012a) Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus 22:255–266
van Hasselt FN, Boudewijns ZS, van der Knaap NJ, Krugers HJ, Joëls M (2012b) Maternal care received by individual pups correlates with adult CA1 dendritic morphology and synaptic plasticity in a sex-dependent manner. J Neuroendocrinol 24:331–340
van Hasselt FN, de Visser L, Tieskens JM, Cornelisse S, Baars AM, Lavrijsen M, Krugers HJ, van den Bos R, Joëls M (2012c) Individual variations in maternal care early in life correlate with later life decision-making and c-fos expression in prefrontal subregions of rats. PLoS ONE 7:e37820
Wang XD, Rammes G, Kraev I, Wolf M, Liebl C, Scharf SH, Rice CJ, Wurst W, Holsboer F, Deussing JM, Baram TZ, Stewart MG, Müller MB, Schmidt MV (2011) Forebrain CRF1 modulates early-life stress-programmed cognitive deficits. J Neurosci 31:13625–13634
Wang XD, Su YA, Wagner KV, Avrabos C, Scharf SH, Hartmann J, Wolf M, Liebl C, Kühne C, Wurst W, Holsboer F, Eder M, Deussing JM, Müller MB, Schmidt MV (2013) Nectin-3 links CRHR1 signaling to stress-induced memory deficits and spine loss. Nat Neurosci 16:706–713
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
Weaver IC, Meaney MJ, Szyf M, Weaver IC, Meaney MJ, Szyf M (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 103:3480–3485
Weinberg J, Levine S (1977) Early handling influences on behavioral and physiological responses during active avoidance. Dev Psychobiol 10:161–169
Wiener SG, Levine S (1978) Perinatal malnutrition and early handling: interactive effects on the development of the pituitary-adrenal system. Dev Psychobiol 11:335–352
Wiener SG, Levine S (1983) Influence of perinatal malnutrition and early handling on the pituitary-adrenal response to noxious stimuli in adult rats. Physiol Behav 31:285–291
Workel JO, Oitzl MS, Fluttert M, Lesscher H, Karssen A, de Kloet ER (2001) Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of brown norway rats from youth to senescence. J Neuroendocrinol 13:569–580
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Krugers, H.J., Joëls, M. (2014). Long-lasting Consequences of Early Life Stress on Brain Structure, Emotion and Cognition. In: Pariante, C., Lapiz-Bluhm, M. (eds) Behavioral Neurobiology of Stress-related Disorders. Current Topics in Behavioral Neurosciences, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7854_2014_289
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