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Electrophysiological insights into the enduring effects of early life stress on the brain

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Abstract

Increasing evidence links exposure to stress early in life to long-term alterations in brain function, which in turn have been linked to a range of psychiatric and neurological disorders in humans. Electrophysiological approaches to studying these causal pathways have been relatively underexploited. Effects of early life stress on neuronal electrophysiological properties offer a set of potential mechanisms for these susceptibilities, notably in the case of epilepsy. Thus, we review experimental evidence for altered cellular and circuit electrophysiology resulting from exposure to early life stress. Much of this work focuses on limbic long-term potentiation, but other studies address alterations in electrophysiological properties of ion channels, neurotransmitter systems, and the autonomic nervous system. We discuss mechanisms which may mediate these effects, including influences of early life stress on key components of brain synaptic transmission, particularly glutamate, GABA and 5-HT receptors, and influences on neuroplasticity (primarily neurogenesis and synaptic density) and on neuronal network activity. The existing literature, although small, provides strong evidence that early life stress induces enduring, often robust effects on a range of electrophysiological properties, suggesting further study of enduring effects of early life stress employing electrophysiological methods and concepts will be productive in illuminating disease pathophysiology.

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References

  • Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2007) Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32:256–266

    Article  PubMed  CAS  Google Scholar 

  • Aisa B, Gil-Bea FJ, Marcos B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2009) Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: involvement of the HPA axis. Psychoneuroendocrinology 34:1495–1505

    Article  PubMed  CAS  Google Scholar 

  • Andersen SL, Teicher MH (2004) Delayed effects of early stress on hippocampal development. Neuropsychopharmacology 29:1988–1993

    Article  PubMed  Google Scholar 

  • Arborelius L, Hawks BW, Owens MJ, Plotsky PM, Nemeroff CB (2004) Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology (Berl) 176:248–255

    Article  CAS  Google Scholar 

  • Aston-Jones G, Card JP (2000) Use of pseudorabies virus to delineate multisynaptic circuits in brain: opportunities and limitations. J Neurosci Methods 103:51–61

    Article  PubMed  CAS  Google Scholar 

  • Auvergne R, Lere C, El Bahh B, Arthaud S, Lespinet V, Rougier A, Le Gal La Salle G (2002) Delayed kindling epileptogenesis and increased neurogenesis in adult rats housed in an enriched environment. Brain Res 954:277–285

    Article  PubMed  CAS  Google Scholar 

  • Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joels 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

    Article  PubMed  Google Scholar 

  • Banihashemi L, Rinaman L (2009) Repeated brief postnatal maternal separation enhances hypothalamic gastric autonomic circuits in juvenile rats. Neuroscience 165:265–277

    Article  PubMed  CAS  Google Scholar 

  • Baram TZ, Hatalski CG (1998) Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci 21:471–476

    Article  PubMed  CAS  Google Scholar 

  • Barna I, Balint E, Baranyi J, Bakos N, Makara GB, Haller J (2003) Gender-specific effect of maternal deprivation on anxiety and corticotropin-releasing hormone mRNA expression in rats. Brain Res Bull 62:85–91

    Article  PubMed  CAS  Google Scholar 

  • Bartesaghi R (2004) Effect of early isolation on the synaptic function in the dentate gyrus and field CA1 of the guinea pig. Hippocampus 14:482–498

    Article  PubMed  Google Scholar 

  • Bartesaghi R, Serrai A (2001) Effects of early environment on granule cell morphology in the dentate gyrus of the guinea pig. Neuroscience 102:87–100

    Article  PubMed  CAS  Google Scholar 

  • Bartesaghi R, Raffi M, Ciani E (2006) Effect of early isolation on signal transfer in the entorhinal cortex-dentate-hippocampal system. Neuroscience 137:875–890

    Article  PubMed  CAS  Google Scholar 

  • Beck SL, Gavin DL (1976) Susceptibility of mice to audiogenic seizures is increased by handling their dams during gestation. Science 193:427–428

    Google Scholar 

  • Belelli D, Lambert JJ (2005) Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6:565–575

    Article  PubMed  CAS  Google Scholar 

  • Bender RA, Baram TZ (2008) Hyperpolarization activated cyclic-nucleotide gated (HCN) channels in developing neuronal networks. Prog Neurobiol 86:129–140

    Article  PubMed  CAS  Google Scholar 

  • Berkovic SF, Mulley JC, Scheffer IE, Petrou S (2006) Human epilepsies: interaction of genetic and acquired factors. Trends Neurosci 29:391–397

    Article  PubMed  CAS  Google Scholar 

  • Blaise JH, Koranda JL, Chow U, Haines KE, Dorward EC (2008) Neonatal isolation stress alters bidirectional long-term synaptic plasticity in amygdalo-hippocampal synapses in freely behaving adult rats. Brain Res 1193:25–33

    Article  PubMed  CAS  Google Scholar 

  • Bliss T, Collingridge G, Morris R (2007) Synaptic plasticity in the hippocampus. In: Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, Oxford, pp 343–474

    Google Scholar 

  • Blumenfeld H, Lampert A, Klein JP, Mission J, Chen MC, Rivera M, Dib-Hajj S, Brennan AR, Hains BC, Waxman SG (2009) Role of hippocampal sodium channel Nav1.6 in kindling epileptogenesis. Epilepsia 50:44–55

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  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 

  • Bronzino JD, Kehoe P, Austin-LaFrance RJ, Rushmore RJ, Kurdian J (1996) Neonatal isolation alters LTP in freely moving juvenile rats: sex differences. Brain Res Bull 41:175–183

    Article  PubMed  CAS  Google Scholar 

  • Brunson KL, Eghbal-Ahmadi M, Bender R, Chen Y, Baram TZ (2001) Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci USA 98:8856–8861

    Article  PubMed  CAS  Google Scholar 

  • Brunson KL, Kramar E, Lin B, Chen YC, Colgin LL, Yanagihara TK, Lynch G, Baram TZ (2005) Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 25:9328–9338

    Article  PubMed  CAS  Google Scholar 

  • Bryan GK, Riesen AH (1989) Deprived somatosensory–motor experience in stumptailed monkey neocortex: dendritic spine density and dendritic branching of layer IIIB pyramidal cells. J Comp Neurol 286:208–217

    Article  PubMed  CAS  Google Scholar 

  • Byrne J (2008) Learning and memory: basic mechanisms. In: Squire L, Berg D, Bloom F, du Lac S, Ghosh A, Spitzer N (eds) Fundamental neuroscience. Academic, Burlington MA, pp 1133–1152

    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 

  • Card JP, Levitt P, Gluhovsky M, Rinaman L (2005) Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J Neurosci 25:9102–9111

    Article  PubMed  CAS  Google Scholar 

  • Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, Joels 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

    Article  PubMed  CAS  Google Scholar 

  • Champagne DL, Ronald de Kloet E, Joels M (2009) Fundamental aspects of the impact of glucocorticoids on the (immature) brain. Semin Fetal Neonatal Med 14:136–142

    Article  PubMed  Google Scholar 

  • Chung EK, Zhang X, Li Z, Zhang H, Xu H, Bian Z (2007) Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat. Brain Res 1153:68–77

    Article  PubMed  CAS  Google Scholar 

  • Cirulli F, Francia N, Berry A, Aloe L, Alleva E, Suomi SJ (2009) Early life stress as a risk factor for mental health: role of neurotrophins from rodents to non-human primates. Neurosci Biobehav Rev 33:573–585

    Article  PubMed  CAS  Google Scholar 

  • Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025–1034

    Article  PubMed  CAS  Google Scholar 

  • Colley BS, Cavallin MA, Biju K, Marks DR, Fadool DA (2009) Brain-derived neurotrophic factor modulation of Kv1.3 channel is disregulated by adaptor proteins Grb10 and nShc. BMC Neurosci 10:8

    Article  PubMed  CAS  Google Scholar 

  • Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473

    Article  PubMed  CAS  Google Scholar 

  • Cui M, Yang Y, Yang J, Zhang J, Han H, Ma W, Li H, Mao R, Xu L, Hao W, Cao J (2006) Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress. Neurosci Lett 404:208–212

    Article  PubMed  CAS  Google Scholar 

  • Curtis AL, Bethea T, Valentino RJ (2006) Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology 31:544–554

    Article  PubMed  CAS  Google Scholar 

  • Cyr M, Ghribi O, Di Paolo T (2000) Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain. J Neuroendocrinol 12:445–452

    Article  PubMed  CAS  Google Scholar 

  • Deadwyler SA (2010) Electrophysiological correlates of abused drugs: relation to natural rewards. Ann NY Acad Sci 1187:140–147

    Article  PubMed  CAS  Google Scholar 

  • Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339–350

    Article  PubMed  CAS  Google Scholar 

  • Douglas RM (1977) Long lasting synaptic potentiation in the rat dentate gyrus following brief high frequency stimulation. Brain Res 126:361–365

    Article  PubMed  CAS  Google Scholar 

  • Dremencov E, Gur E, Lerer B, Newman ME (2003) Effects of chronic antidepressants and electroconvulsive shock on serotonergic neurotransmission in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 27:729–739

    Article  PubMed  CAS  Google Scholar 

  • Edwards HE, Dortok D, Tam J, Won D, Burnham WM (2002) Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats. Horm Behav 42:437–447

    Google Scholar 

  • Engel J, Dichter M, Schwartzkroin P (2007) Basic mechanisms of human epilepsy. In: Engel J, Pedley T (eds) Epilepsy: a comprehensive textbook. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, pp 495–507

    Google Scholar 

  • Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317

    Article  PubMed  CAS  Google Scholar 

  • Fabricius K, Wortwein G, Pakkenberg B (2008) The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct Funct 212:403–416

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frye CA, Bayon LE (1999) Prenatal stress reduces the effectiveness of the neurosteroid 3 alpha, 5 alpha-THP to block kainic-acid-induced seizures. Dev Psychobiol 34:227–234

    Google Scholar 

  • Fukushima F, Nakao K, Shinoe T, Fukaya M, Muramatsu S, Sakimura K, Kataoka H, Mori H, Watanabe M, Manabe T, Mishina M (2009) Ablation of NMDA receptors enhances the excitability of hippocampal CA3 neurons. PLoS ONE 4:e3993

    Article  PubMed  CAS  Google Scholar 

  • Fureman BE, Hess EJ (2005) Noradrenergic blockade prevents attacks in a model of episodic dysfunction caused by a channelopathy. Neurobiol Dis 20:227–232

    Article  PubMed  CAS  Google Scholar 

  • Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438:185–192

    Article  PubMed  CAS  Google Scholar 

  • Galanopoulou AS (2008) Dissociated gender-specific effects of recurrent seizures on GABA signaling in CA1 pyramidal neurons: role of GABA(A) receptors. J Neurosci 28:1557–1567

    Article  PubMed  CAS  Google Scholar 

  • Galea LA (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 57:332–341

    Article  PubMed  CAS  Google Scholar 

  • Gardner KL, Hale MW, Lightman SL, Plotsky PM, Lowry CA (2009) Adverse early life experience and social stress during adulthood interact to increase serotonin transporter mRNA expression. Brain Res 1305:47–63

    Article  PubMed  CAS  Google Scholar 

  • Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4:e5464

    Article  PubMed  CAS  Google Scholar 

  • Gartside SE, Johnson DA, Leitch MM, Troakes C, Ingram CD (2003) Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur J Neurosci 17:2401–2408

    Article  PubMed  Google Scholar 

  • Genest SE, Gulemetova R, Laforest S, Drolet G, Kinkead R (2004) Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554:543–557

    Article  PubMed  CAS  Google Scholar 

  • Genest SE, Balon N, Laforest S, Drolet G, Kinkead R (2007) Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: the role of GABAergic modulation within the paraventricular nucleus of the hypothalamus. J Physiol 583:299–314

    Article  PubMed  CAS  Google Scholar 

  • Gilby KL, Sydserff S, Patey AM, Thorne V, St-Onge V, Jans J, McIntyre DC (2009) Postnatal epigenetic influences on seizure susceptibility in seizure-prone versus seizure-resistant rat strains. Behav Neurosci 123:337–346

    Google Scholar 

  • Gluckman PD, Hanson MA, Beedle AS (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 19:1–19

    Article  PubMed  Google Scholar 

  • Gomes CM, Raineki C, Ramos de Paula P, Severino GS, Helena CV, Anselmo-Franci JA, Franci CR, Sanvitto GL, Lucion AB (2005) Neonatal handling and reproductive function in female rats. J Endocrinol 184:435–445

    Article  PubMed  CAS  Google Scholar 

  • Goodfellow NM, Benekareddy M, Vaidya VA, Lambe EK (2009) Layer II/III of the prefrontal cortex: inhibition by the serotonin 5-HT1A receptor in development and stress. J Neurosci 29:10094–10103

    Article  PubMed  CAS  Google Scholar 

  • Gorter JA, Titulaer M, Bos NP, Huisman E (1991) Chronic neonatal MK-801 administration leads to a long-lasting increase in seizure sensitivity during the early stages of hippocampal kindling. Neurosci Lett 134:29–32

    Article  PubMed  CAS  Google Scholar 

  • Gos T, Bock J, Poeggel G, Braun K (2008) Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 62:229–232

    Article  PubMed  CAS  Google Scholar 

  • Gruss M, Braun K, Frey JU, Korz V (2008) Maternal separation during a specific postnatal time window prevents reinforcement of hippocampal long-term potentiation in adolescent rats. Neuroscience 152:1–7

    Article  PubMed  CAS  Google Scholar 

  • Gue M, Del Rio-Lacheze C, Eutamene H, Theodorou V, Fioramonti J, Bueno L (1997) Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol Motil 9:271–279

    Article  PubMed  CAS  Google Scholar 

  • Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84

    Article  PubMed  CAS  Google Scholar 

  • Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y, Ogiue-Ikeda M, Ishii H, Kimoto T, Kawato S (2008) Estrogen synthesis in the brain—role in synaptic plasticity and memory. Mol Cell Endocrinol 290:31–43

    Article  PubMed  CAS  Google Scholar 

  • Hsu D (2007) The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res 163:601–613

    Article  PubMed  Google Scholar 

  • Hsu FC, Zhang GJ, Raol YS, Valentino RJ, Coulter DA, Brooks-Kayal AR (2003) Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc Natl Acad Sci USA 100:12213–12218

    Article  PubMed  CAS  Google Scholar 

  • Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002) Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long–Evans rats. Brain Res 950:52–63

    Article  PubMed  CAS  Google Scholar 

  • Ivy AS, Rex CS, Chen Y, Dube C, Maras PM, Grigoriadis DE, Gall CM, Lynch G, Baram TZ (2010) Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J Neurosci 30:13005–13015

    Article  PubMed  CAS  Google Scholar 

  • Jacobi S, Soriano J, Segal M, Moses E (2009) BDNF and NT-3 increase excitatory input connectivity in rat hippocampal cultures. Eur J Neurosci 30:998–1010

    Article  PubMed  Google Scholar 

  • Jacobson-Pick S, Elkobi A, Vander S, Rosenblum K, Richter-Levin G (2008) Juvenile stress-induced alteration of maturation of the GABAA receptor alpha subunit in the rat. Int J Neuropsychopharmacol 11:891–903

    Article  PubMed  CAS  Google Scholar 

  • Jedema HP, Grace AA (2004) Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J Neurosci 24:9703–9713

    Article  PubMed  CAS  Google Scholar 

  • Jedema HP, Finlay JM, Sved AF, Grace AA (2001) Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol Psychiatry 49:351–359

    Article  PubMed  CAS  Google Scholar 

  • Joels M (2009) Stress, the hippocampus, and epilepsy. Epilepsia 50:586–597

    Article  PubMed  Google Scholar 

  • Joels M, Krugers HJ (2007) LTP after stress: up or down? Neural Plast 2007:93202

    Article  PubMed  Google Scholar 

  • Jones NC, Kumar G, O’Brien TJ, Morris MJ, Rees SM, Salzberg MR (2009) Anxiolytic effects of rapid amygdala kindling, and the influence of early life experience in rats. Behav Brain Res 203:81–87

    Article  PubMed  Google Scholar 

  • Karst H, de Kloet ER, Joels M (1999) Episodic corticosterone treatment accelerates kindling epileptogenesis and triggers long-term changes in hippocampal CA1 cells, in the fully kindled state. Eur J Neurosci 11:889–898

    Article  PubMed  CAS  Google Scholar 

  • Kehoe P, Bronzino JD (1999) Neonatal stress alters LTP in freely moving male and female adult rats. Hippocampus 9:651–658

    Article  PubMed  CAS  Google Scholar 

  • Kehoe P, Hoffman JH, Austin-LaFrance RJ, Bronzino JD (1995) Neonatal isolation enhances hippocampal dentate response to tetanization in freely moving juvenile male rats. Exp Neurol 136:89–97

    Article  PubMed  CAS  Google Scholar 

  • Kinkead R, Gulemetova R (2009) Neonatal maternal separation and neuroendocrine programming of the respiratory control system in rats. Biol Psychol (in press)

  • Kinkead R, Genest SE, Gulemetova R, Lajeunesse Y, Laforest S, Drolet G, Bairam A (2005a) Neonatal maternal separation and early life programming of the hypoxic ventilatory response in rats. Respir Physiol Neurobiol 149:313–324

    Article  PubMed  Google Scholar 

  • Kinkead R, Gulemetova R, Bairam A (2005b) Neonatal maternal separation enhances phrenic responses to hypoxia and carotid sinus nerve stimulation in the adult anesthetized rat. J Appl Physiol 99:189–196

    Article  PubMed  Google Scholar 

  • Kinkead R, Balon N, Genest SE, Gulemetova R, Laforest S, Drolet G (2008) Neonatal maternal separation and enhancement of the inspiratory (phrenic) response to hypoxia in adult rats: disruption of GABAergic neurotransmission in the nucleus tractus solitarius. Eur J Neurosci 27:1174–1188

    Article  PubMed  Google Scholar 

  • Kinnunen AK, Koenig JI, Bilbe G (2003) Repeated variable prenatal stress alters pre- and postsynaptic gene expression in the rat frontal pole. J Neurochem 86:736–748

    Article  PubMed  CAS  Google Scholar 

  • Knox AM, Li XF, Kinsey-Jones JS, Wilkinson ES, Wu XQ, Cheng YS, Milligan SR, Lightman SL, O’Byrne KT (2009) Neonatal lipopolysaccharide exposure delays puberty and alters hypothalamic Kiss1 and Kiss1r mRNA expression in the female rat. J Neuroendocrinol 21:683–689

    Article  PubMed  CAS  Google Scholar 

  • Koe AS, Jones NC, Salzberg MR (2009) Early life stress as an influence on limbic epilepsy: an hypothesis whose time has come? Front Behav Neurosci 3:24

    Article  PubMed  CAS  Google Scholar 

  • Koo JW, Park CH, Choi SH, Kim NJ, Kim HS, Choe JC, Suh YH (2003) The postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation, and synaptic protein expression. FASEB J 17:1556–1558

    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, Hoogenraad CC, Groc L (2010) Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci 11:675–681

    Article  PubMed  CAS  Google Scholar 

  • Kumar G (2010) The effect of stress on the vulnerability to limbic epileptogenesis in rats Department of Medicine. University of Melbourne, Parkville, Victoria, Australia

    Google Scholar 

  • Kumar G, Couper A, O’Brien TJ, Salzberg MR, Jones NC, Rees SM, Morris MJ (2007) The acceleration of amygdala kindling epileptogenesis by chronic low-dose corticosterone involves both mineralocorticoid and glucocorticoid receptors. Psychoneuroendocrinology 32:834–842

    Article  PubMed  CAS  Google Scholar 

  • Lai MC, Holmes GL, Lee KH, Yang SN, Wang CA, Wu CL, Tiao MM, Hsieh CS, Lee CH, Huang LT (2006) Effect of neonatal isolation on outcome following neonatal seizures in rats—the role of corticosterone. Epilepsy Res 68:123–136

    Article  PubMed  CAS  Google Scholar 

  • Lai MC, Lui CC, Yang SN, Wang JY, Huang LT (2009) Epileptogenesis is increased in rats with neonatal isolation and early-life seizure and ameliorated by MK-801: a long-term MRI and histological study. Pediatr Res 66:441–447

    Article  PubMed  Google Scholar 

  • Lambas-Senas L, Mnie-Filali O, Certin V, Faure C, Lemoine L, Zimmer L, Haddjeri N (2009) Functional correlates for 5-HT(1A) receptors in maternally deprived rats displaying anxiety and depression-like behaviors. Prog Neuropsychopharmacol Biol Psychiatry 33:262–268

    Article  PubMed  CAS  Google Scholar 

  • Leach LS, Christensen H, Mackinnon AJ, Windsor TD, Butterworth P (2008) Gender differences in depression and anxiety across the adult lifespan: the role of psychosocial mediators. Soc Psychiatry Psychiatr Epidemiol 43:983–998

    Article  PubMed  Google Scholar 

  • Lee HJ, Kim JW, Yim SV, Kim MJ, Kim SA, Kim YJ, Kim CJ, Chung JH (2001) Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Mol Psychiatry 6(610):725–728

    Article  CAS  Google Scholar 

  • Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032–11037

    Article  PubMed  CAS  Google Scholar 

  • Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN (2006) Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatry 59:786–792

    Article  PubMed  Google Scholar 

  • Lessmann V (1998) Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol 31:667–674

    PubMed  CAS  Google Scholar 

  • Leuner B, Gould E, Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16:216–224

    Article  PubMed  Google Scholar 

  • Lin CW, Sim S, Ainsworth A, Okada M, Kelsch W, Lois C (2010) Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65:32–39

    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 

  • Llinas RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227

    Article  PubMed  CAS  Google Scholar 

  • Lucassen PJ, Bosch OJ, Jousma E, Kromer SA, Andrew R, Seckl JR, Neumann ID (2009) Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci 29:97–103

    Article  PubMed  CAS  Google Scholar 

  • Luine V (2002) Sex differences in chronic stress effects on memory in rats. Stress 5:205–216

    Article  PubMed  CAS  Google Scholar 

  • Lujan R, Shigemoto R, Lopez-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580

    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 

  • Mandyam CD, Crawford EF, Eisch AJ, Rivier CL, Richardson HN (2008) Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev Neurobiol 68:575–589

    Article  PubMed  Google Scholar 

  • Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G (2009) Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63:794–804

    Article  PubMed  CAS  Google Scholar 

  • Mazarati AM, Shin D, Kwon YS, Bragin A, Pineda E, Tio D, Taylor AN, Sankar R (2009) Elevated plasma corticosterone level and depressive behavior in experimental temporal lobe epilepsy. Neurobiol Dis 34:457–461

    Article  PubMed  CAS  Google Scholar 

  • McCormick D (2008) Membrane potential and action potential. In: Squire L, Berg D, Bloom F, du Lac S, Ghosh A, Spitzer N (eds) Fundamental neuroscience. Academic, Burlington MA, pp 112–132

    Google Scholar 

  • McEwen BS (2008) Understanding the potency of stressful early life experiences on brain and body function. Metabolism 57(Suppl 2):S11–S15

    Article  PubMed  CAS  Google Scholar 

  • McFarlane A, Clark CR, Bryant RA, Williams LM, Niaura R, Paul RH, Hitsman BL, Stroud L, Alexander DM, Gordon E (2005) The impact of early life stress on psychophysiological, personality and behavioral measures in 740 non-clinical subjects. J Integr Neurosci 4:27–40

    Article  PubMed  Google Scholar 

  • McIntosh J, Anisman H, Merali Z (1999) Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res 113:97–106

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ, Szyf M (2005) Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci 28:456–463

    Article  PubMed  CAS  Google Scholar 

  • Michelsen KA, van den Hove DL, Schmitz C, Segers O, Prickaerts J, Steinbusch HW (2007) Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex. BMC Neurosci 8:107

    Article  PubMed  Google Scholar 

  • Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841–846

    Article  PubMed  CAS  Google Scholar 

  • Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540

    Article  PubMed  CAS  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 

  • Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J (2006) Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 24:1477–1487

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oitzl MS, Champagne DL, van der Veen R, de Kloet ER (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 34:853–866

    Article  PubMed  CAS  Google Scholar 

  • Olson TM, Alekseev AE, Liu XK, Park S, Zingman LV, Bienengraeber M, Sattiraju S, Ballew JD, Jahangir A, Terzic A (2006) Kv1.5 channelopathy due to KCNA5 loss-of-function mutation causes human atrial fibrillation. Hum Mol Genet 15:2185–2191

    Article  PubMed  CAS  Google Scholar 

  • Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joels M, Krugers H, Lucassen PJ (2010a) Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats. Psychopharmacology (Berl)

  • Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joels M, Lucassen PJ, Krugers H (2010b) 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

    Article  PubMed  CAS  Google Scholar 

  • Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks. Nat Neurosci 13:812–818

    Article  PubMed  CAS  Google Scholar 

  • Parent JM (2007) Adult neurogenesis in the intact and epileptic dentate gyrus. Prog Brain Res 163:529–540

    Article  PubMed  CAS  Google Scholar 

  • Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727–3738

    PubMed  CAS  Google Scholar 

  • Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141–1144

    Article  PubMed  CAS  Google Scholar 

  • Phillips DI (2007) Programming of the stress response: a fundamental mechanism underlying the long-term effects of the fetal environment? J Intern Med 261:453–460

    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, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ (2005) Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30:2192–2204

    Article  PubMed  CAS  Google Scholar 

  • Radley JJ, Gosselink KL, Sawchenko PE (2009) A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29:7330–7340

    Article  PubMed  CAS  Google Scholar 

  • Ressler KJ, Nemeroff CB (2000) Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12(Suppl 1):2–19

    Article  PubMed  Google Scholar 

  • Richichi C, Brewster AL, Bender RA, Simeone TA, Zha Q, Yin HZ, Weiss JH, Baram TZ (2008) Mechanisms of seizure-induced ‘transcriptional channelopathy’ of hyperpolarization-activated cyclic nucleotide gated (HCN) channels. Neurobiol Dis 29:297–305

    Article  PubMed  CAS  Google Scholar 

  • Roberts AJ, Keith LD (1994) Mineralocorticoid receptors mediate the enhancing effects of corticosterone on convulsion susceptibility in mice. J Pharmacol Exp Ther 270:505–511

    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 

  • Rosen JB, Pishevar SK, Weiss SR, Smith MA, Kling MA, Gold PW, Schulkin J (1994) Glucocorticoid treatment increases the ability of CRH to induce seizures. Neurosci Lett 174:113–116

    Article  PubMed  CAS  Google Scholar 

  • Ryan B, Musazzi L, Mallei A, Tardito D, Gruber SH, El Khoury A, Anwyl R, Racagni G, Mathe AA, Rowan MJ, Popoli M (2009) Remodelling by early-life stress of NMDA receptor-dependent synaptic plasticity in a gene-environment rat model of depression. Int J Neuropsychopharmacol 12:553–559

    Article  PubMed  CAS  Google Scholar 

  • Salzberg M, Kumar G, Supit L, Jones NC, Morris MJ, Rees S, O’Brien TJ (2007) Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia 48:2079–2085

    Article  PubMed  Google Scholar 

  • Sanchez MM, Ladd CO, Plotsky PM (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13:419–449

    Article  PubMed  CAS  Google Scholar 

  • Sanders BJ, Anticevic A (2007) Maternal separation enhances neuronal activation and cardiovascular responses to acute stress in borderline hypertensive rats. Behav Brain Res 183:25–30

    Article  PubMed  Google Scholar 

  • Sapolsky RM (1986) Glucocorticoid toxicity in the hippocampus. Temporal aspects of synergy with kainic acid. Neuroendocrinology 43:440–444

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1:1–19

    Article  PubMed  CAS  Google Scholar 

  • Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 103:17501–17506

    Article  PubMed  CAS  Google Scholar 

  • Schridde U, van Luijtelaar G (2004a) Corticosterone increases spike-wave discharges in a dose- and time-dependent manner in WAG/Rij rats. Pharmacol Biochem Behav 78:369–375

    Article  PubMed  CAS  Google Scholar 

  • Schridde U, van Luijtelaar G (2004b) The influence of strain and housing on two types of spike-wave discharges in rats. Genes Brain Behav 3:1–7

    Article  PubMed  CAS  Google Scholar 

  • Schridde U, Strauss U, Brauer AU, van Luijtelaar G (2006) Environmental manipulations early in development alter seizure activity, Ih and HCN1 protein expression later in life. Eur J Neurosci 23:3346–3358

    Article  PubMed  Google Scholar 

  • Seckl JR (2008) Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res 167:17–34

    Article  PubMed  CAS  Google Scholar 

  • Setiawan E, Jackson MF, MacDonald JF, Matthews SG (2007) Effects of repeated prenatal glucocorticoid exposure on long-term potentiation in the juvenile guinea-pig hippocampus. J Physiol 581:1033–1042

    Article  PubMed  CAS  Google Scholar 

  • Shansky RM, Morrison JH (2009) Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res 1293:108–113

    Article  PubMed  CAS  Google Scholar 

  • Shepherd G (2008a) Complex information processing in dendrites. In: Squire L, Berg D, Bloom F, du Lac S, Ghosh A, Spitzer N (eds) Fundamental neuroscience. Academic, Burlington, pp 247–269

    Google Scholar 

  • Shepherd G (2008b) Electrotonic properties of axons and dendrites. In: Squire L, Berg D, Bloom F, du Lac S, Ghosh A, Spitzer N (eds) Fundamental neuroscience. Academic, Burlington, pp 87–111

    Google Scholar 

  • Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372–376

    Article  PubMed  CAS  Google Scholar 

  • Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578–584

    Article  PubMed  Google Scholar 

  • Skilbeck KJ, Johnston GA, Hinton T (2010) Stress and GABA receptors. J Neurochem 112:1115–1130

    Article  PubMed  CAS  Google Scholar 

  • Slotten HA, Kalinichev M, Hagan JJ, Marsden CA, Fone KC (2006) Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res 1097:123–132

    Article  PubMed  CAS  Google Scholar 

  • Smith-Swintosky VL, Pettigrew LC, Sapolsky RM, Phares C, Craddock SD, Brooke SM, Mattson MP (1996) Metyrapone, an inhibitor of glucocorticoid production, reduces brain injury induced by focal and global ischemia and seizures. J Cereb Blood Flow Metab 16:585–598

    Article  PubMed  CAS  Google Scholar 

  • Son GH, Geum D, Chung S, Kim EJ, Jo JH, Kim CM, Lee KH, Kim H, Choi S, Kim HT, Lee CJ, Kim K (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci 26:3309–3318

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A, Toutountzi E, Fragioudaki K, Kouvelas ED, Stylianopoulou F, Mitsacos A (2009) Selective effects of neonatal handling on rat brain N-methyl-D-aspartate receptors. Neuroscience 164:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Stevenson CW, Halliday DM, Marsden CA, Mason R (2008a) Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience 155:852–863

    Article  PubMed  CAS  Google Scholar 

  • Stevenson CW, Marsden CA, Mason R (2008b) Early life stress causes FG-7142-induced corticolimbic dysfunction in adulthood. Brain Res 1193:43–50

    Article  PubMed  CAS  Google Scholar 

  • Stewart CA, Petrie RX, Balfour DJ, Matthews K, Reid IC (2004) Enhanced evoked responses after early adversity and repeated platform exposure: the neurobiology of vulnerability? Biol Psychiatry 55:868–870

    Article  PubMed  Google Scholar 

  • Stringer JL, Lothman EW (1992) Reverberatory seizure discharges in hippocampal–parahippocampal circuits. Exp Neurol 116:198–203

    Article  PubMed  CAS  Google Scholar 

  • Szuran TF, Pliska V, Pokorny J, Welzl H (2000) Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 71:353–362

    Article  PubMed  CAS  Google Scholar 

  • Taher TR, Salzberg M, Morris MJ, Rees S, O’Brien TJ (2005) Chronic low-dose corticosterone supplementation enhances acquired epileptogenesis in the rat amygdala kindling model of TLE. Neuropsychopharmacology 30:1610–1616

    Article  PubMed  CAS  Google Scholar 

  • Takatsuru Y, Yoshitomo M, Nemoto T, Eto K, Nabekura J (2009) Maternal separation decreases the stability of mushroom spines in adult mice somatosensory cortex. Brain Res 1294:45–51

    Article  PubMed  CAS  Google Scholar 

  • Talmi M, Carlier E, Bengelloun W, Soumireu-Mourat B (1995) Synergistic action of corticosterone on kainic acid-induced electrophysiological alterations in the hippocampus. Brain Res 704:97–102

    Article  PubMed  CAS  Google Scholar 

  • Tang AC, Zou B (2002) Neonatal exposure to novelty enhances long-term potentiation in CA1 of the rat hippocampus. Hippocampus 12:398–404

    Article  PubMed  Google Scholar 

  • Tang AC, Zou B, Reeb BC, Connor JA (2008) An epigenetic induction of a right-shift in hippocampal asymmetry: selectivity for short- and long-term potentiation but not post-tetanic potentiation. Hippocampus 18:5–10

    Article  PubMed  Google Scholar 

  • Uhlhaas PJ, Pipa G, Lima B, Melloni L, Neuenschwander S, Nikolic D, Singer W (2009) Neural synchrony in cortical networks: history, concept and current status. Front Integr Neurosci 3:17

    Article  PubMed  Google Scholar 

  • Vallee M, MacCari S, Dellu F, Simon H, Le Moal M, Mayo W (1999) Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci 11:2906–2916

    Article  PubMed  CAS  Google Scholar 

  • Van den Hove DL, Steinbusch HW, Scheepens A, Van de Berg WD, Kooiman LA, Boosten BJ, Prickaerts J, Blanco CE (2006) Prenatal stress and neonatal rat brain development. Neuroscience 137:145–155

    Article  PubMed  CAS  Google Scholar 

  • van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034

    Article  PubMed  CAS  Google Scholar 

  • van Riel E, van Gemert NG, Meijer OC, Joels M (2004) Effect of early life stress on serotonin responses in the hippocampus of young adult rats. Synapse 53:11–19

    Article  PubMed  CAS  Google Scholar 

  • Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818

    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 

  • Weber K, Miller GA, Schupp HT, Borgelt J, Awiszus B, Popov T, Elbert T, Rockstroh B (2009) Early life stress and psychiatric disorder modulate cortical responses to affective stimuli. Psychophysiology 46:1234–1243

    Article  PubMed  Google Scholar 

  • Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073–1086

    Article  PubMed  CAS  Google Scholar 

  • Welting O, Van Den Wijngaard RM, De Jonge WJ, Holman R, Boeckxstaens GE (2005) Assessment of visceral sensitivity using radio telemetry in a rat model of maternal separation. Neurogastroenterol Motil 17:838–845

    Article  PubMed  CAS  Google Scholar 

  • Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093–1097

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Han H, Cao J, Li L, Xu L (2006) Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16:431–436

    Article  PubMed  Google Scholar 

  • Yang J, Hou C, Ma N, Liu J, Zhang Y, Zhou J, Xu L, Li L (2007) Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol Learn Mem 87:257–263

    Article  PubMed  Google Scholar 

  • Yuen TJ, Browne KD, Iwata A, Smith DH (2009) Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury. J Neurosci Res 87:3620–3625

    Article  PubMed  CAS  Google Scholar 

  • Zhang LX, Levine S, Dent G, Zhan Y, Xing G, Okimoto D, Kathleen Gordon M, Post RM, Smith MA (2002) Maternal deprivation increases cell death in the infant rat brain. Brain Res Dev Brain Res 133:1–11

    Article  PubMed  CAS  Google Scholar 

  • Zobel A, Wellmer J, Schulze-Rauschenbach S, Pfeiffer U, Schnell S, Elger C, Maier W (2004) Impairment of inhibitory control of the hypothalamic pituitary adrenocortical system in epilepsy. Eur Arch Psychiatry Clin Neurosci 254:303–311

    PubMed  Google Scholar 

  • Zolles G, Wenzel D, Bildl W, Schulte U, Hofmann A, Muller CS, Thumfart JO, Vlachos A, Deller T, Pfeifer A, Fleischmann BK, Roeper J, Fakler B, Klocker N (2009) Association with the auxiliary subunit PEX5R/Trip8b controls responsiveness of HCN channels to cAMP and adrenergic stimulation. Neuron 62:814–825

    Article  PubMed  CAS  Google Scholar 

  • Zou B, Golarai G, Connor JA, Tang AC (2001) Neonatal exposure to a novel environment enhances the effects of corticosterone on neuronal excitability and plasticity in adult hippocampus. Brain Res Dev Brain Res 130:1–7

    Article  PubMed  CAS  Google Scholar 

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Ali, I., Salzberg, M.R., French, C. et al. Electrophysiological insights into the enduring effects of early life stress on the brain. Psychopharmacology 214, 155–173 (2011). https://doi.org/10.1007/s00213-010-2125-z

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