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Differential effects of environmental enrichment and isolation housing on the hormonal and neurochemical responses to stress in the prefrontal cortex of the adult rat: relationship to working and emotional memories

  • Psychiatry and Preclinical Psychiatric Studies - Original Article
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Abstract

The present study was designed to investigate the modulation of the stress responses by the environmental conditions and its putative neurobiological mechanisms. For that an integrative study on the effects of environmental enrichment and isolation housing on (1) the corticosterone, dopamine and acetylcholine responses to acute restraint stress in the prefrontal cortex (PFC) of the awake rat; (2) the mRNA levels of glucocorticoid receptors (GRs) in the PFC, and (3) the behavioral responses to stress, related to the PFC (habituation to a novel environment, spatial-working memory and inhibitory avoidance response) was performed. Male Wistar rats were maintained from 3 to 6 months of age in two different conditions: enriched (EC) or impoverished (IC). Animals were stereotaxically implanted with bilateral guide cannulae in the PFC to perform microdialysis experiments to evaluate the concentrations of corticosterone, dopamine and acetylcholine. EC animals showed lower increases of corticosterone and dopamine but not of acetylcholine than IC animals in the PFC in response to acute restraint stress (20 min). In the PFC, GR mRNA levels showed a trend towards an enhancement in EC animals. EC reduced the days to learn the spatial working memory task (radial-water maze). Spatial working memory, however, was not different between groups in either basal or stress conditions. Inhibitory avoidance response was reduced in EC rats. The changes produced by EC in the neurochemical, neuroendocrine and behavioral parameters evaluated suggest that EC rats could show a better coping during an acute stress challenge.

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Abbreviations

EC:

Environmental enrichment conditions

GRs:

Glucocorticoid receptors

IC:

Impoverished conditions

NS:

Non significant

PFC:

Prefrontal cortex

References

  • Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52:1655–1658

    Article  PubMed  CAS  Google Scholar 

  • Ago Y, Arikawa S, Yata M, Yano K, Abe M, Takuma K, Matsuda T (2009) Role of prefrontal dopaminergic neurotransmission in glucocorticoid receptor-mediated modulation of methamphetamine-induced hyperactivity. Synapse 63:7–14

    Article  PubMed  CAS  Google Scholar 

  • Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365–371

    Article  PubMed  CAS  Google Scholar 

  • Antoni FA (1986) Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor. Endocr Rev 7:351–378

    Article  PubMed  CAS  Google Scholar 

  • Arnsten AFT, Goldman-Rakic PS (1998) Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism. Arch Gen Psychiatry 55:362–368

    Article  PubMed  CAS  Google Scholar 

  • Barsegyan A, Mackenzie SM, Kurose BD, McGaugh JL, Roozendaal B (2010) Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc Natl Acad Sci USA 107:16655–16660

    Article  PubMed  CAS  Google Scholar 

  • Berridge CW, Mitton E, Clark W, Roth RH (1999) Engagement in a non-escape (displacement) behavior elicits a selective and lateralized suppression of frontal cortical dopaminergic utilization in stress. Synapse 32:187–197

    Article  PubMed  CAS  Google Scholar 

  • Bimonte HA, Nelson ME, Granholm A-CE (2003) Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol Aging 24:37–48

    Article  PubMed  CAS  Google Scholar 

  • Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:4320–4324

    PubMed  CAS  Google Scholar 

  • Bland ST, Hargrave D, Pepin JL, Amat J, Watkins LR, Maier SF (2003) Stressor controllability modulates stress-induced dopamine and serotonin efflux and morphine-induced serotonin efflux in the medial prefrontal cortex. Neuropsychopharmacology 28:1589–1596

    Article  PubMed  CAS  Google Scholar 

  • Bruce SM (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172–189

    Article  Google Scholar 

  • Butts KA, Weinberg J, Young AH, Phillips AG (2011) Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad Sci USA 108:18459–18464

    Article  PubMed  CAS  Google Scholar 

  • Carlson JN, Fitzgerald LW, Keller RW Jr, Glick SD (1993) Lateralized changes in prefrontal cortical dopamine activity induced by controllable and uncontrollable stress in the rat. Brain Res 630:178–187

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Coco ML, Weiss JM (2005) Neural substrates of coping behavior in the rat: possible importance of mesocorticolimbic dopamine system. Behav Neurosci 119:429–445

    Article  PubMed  CAS  Google Scholar 

  • Croft AP, O’Callaghan MJ, Shaw SG, Connolly G, Jacquot C, Little HJ (2008) Effects of minor laboratory procedures, adrenalectomy, social defeat or acute alcohol on regional brain concentrations of corticosterone. Brain Res 1238:12–22

    Article  PubMed  CAS  Google Scholar 

  • Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477–505

    Article  PubMed  CAS  Google Scholar 

  • Davis M, Hithcock JM, Bowers MB, Berridge CW, Melia KR, Roth RH (1994) Stress-induced activation of prefrontal cortex dopamine turnover: blockade by lesions of the amygdala. Brain Res 664:207–210

    Article  PubMed  CAS  Google Scholar 

  • Day JC, Kornecook TJ, Quirion R (2001) Application of in vivo microdialysis to the study of cholinergic systems. Methods 23:21–39

    Article  PubMed  CAS  Google Scholar 

  • Del Arco A, Mora F (2002) NMDA and AMPA/kainate glutamatergic agonists increase the extracellular concentrations of GABA in the prefrontal cortex of the freely moving rat: modulation by endogenous dopamine. Brain Res Bull 57:623–630

    Article  PubMed  Google Scholar 

  • Del Arco A, Segovia G, Garrido P, de Blas M, Mora F (2007) Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176:267–273

    Article  PubMed  CAS  Google Scholar 

  • Diamond DM, Fleshner M, Ingersoll N, Rose GM (1996) Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 110:661–672

    Article  PubMed  CAS  Google Scholar 

  • Diamond DM, Park CR, Heman KL, Rose GM (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542–552

    Article  PubMed  CAS  Google Scholar 

  • Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839–3847

    PubMed  CAS  Google Scholar 

  • Droste SK, Collins A, Lightman SL, Linthorst ACE, Reul JMHM (2009) Distinct, time-dependent effects of voluntary exercise on circadian and ultradian rhythms and stress responses of free corticosterone in the rat hippocampus. Endocrinology 150:4170–4179

    Article  PubMed  CAS  Google Scholar 

  • Elliott BM, Grunberg NE (2005) Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats. Behav Brain Res 165:187–196

    Article  PubMed  Google Scholar 

  • Feenstra MG, Botterblom MH, van Uum JF (1995) Novelty-induced increase in dopamine release in the rat prefrontal cortex in vivo: inhibition by diazepam. Neurosci Lett 189:81–84

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Teruel A, Escorihuela RM, Castellano B, González B, Tobeña A (1997) Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines. Behav Genet 27:513–526

    Article  PubMed  Google Scholar 

  • Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880–1890

    PubMed  CAS  Google Scholar 

  • Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175:1–8

    Article  PubMed  CAS  Google Scholar 

  • Galani R, Berthel M-C, Lazarus C, Majchrzak M, Barbelivien A, Kelche C, Cassel J-C (2007) The behavioral effects of enriched housing are not altered by serotonin depletion but enrichment alters hippocampal neurochemistry. Neurobiol Learn Mem 88:1–10

    Article  PubMed  CAS  Google Scholar 

  • Garrido P, de Blas M, Del Arco A, Segovia G, Mora F (2012a) Aging increases basal but not stress-induced levels of corticosterone in the brain of the awake rat. Neurobiol Aging 33:375–382

    Article  PubMed  CAS  Google Scholar 

  • Garrido P, De Blas M, Giné E, Santos Á, Mora F (2012b) Aging impairs the control of prefrontal cortex on the release of corticosterone in response to stress and on memory consolidation. Neurobiol Aging 33(827):e821–e829

    Google Scholar 

  • Gisquet-Verrier P, Delatour B (2006) The role of the rat prelimbic/infralimbic cortex in working memory: not involved in the short-term maintenance but in monitoring and processing functions. Neuroscience 141:585–596

    Article  PubMed  CAS  Google Scholar 

  • Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14:477–485

    Article  PubMed  CAS  Google Scholar 

  • Goldstein LE, Rasmusson AM, Bunney BS, Roth RH (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787–4798

    PubMed  CAS  Google Scholar 

  • Hains AB, Arnsten AFT (2008) Molecular mechanisms of stress-induced prefrontal cortical impairment: implications for mental illness. Learn Mem 15:551–564

    Article  PubMed  Google Scholar 

  • Hennessy MB, Foy T (1987) Nonedible material elicits chewing and reduces the plasma corticosterone response during novelty exposure in mice. Behav Neurosci 101:237–245

    Article  PubMed  CAS  Google Scholar 

  • Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201–1213

    Article  PubMed  CAS  Google Scholar 

  • Hernandez LF, Segovia G, Mora F (2003) Effects of activation of NMDA and AMPA glutamate receptors on the extracellular concentrations of dopamine, acetylcholine, and GABA in striatum of the awake rat: a microdialysis study. Neurochem Res 28:1819–1827

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann LC, Schütte SRM, Koch M, Schwabe K (2009) Effect of “enriched environment” during development on adult rat behavior and response to the dopamine receptor agonist apomorphine. Neuroscience 158:1589–1598

    Article  PubMed  CAS  Google Scholar 

  • Horger BA, Roth RH (1996) The role of mesoprefrontal dopamine neurons in stress. Crit Rev Neurobiol 10:395–418

    Article  PubMed  CAS  Google Scholar 

  • Imperato A, Puglisi-Allegra S, Casolini P, Zocchi A, Angelucci L (1989) Stress-induced enhancement of dopamine and acetylcholine release in limbic structures: role of corticosterone. Eur J Pharmacol 165:337–338

    Article  PubMed  CAS  Google Scholar 

  • Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134

    Article  PubMed  CAS  Google Scholar 

  • Jankord R, Herman JP (2008) Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann N Y Acad Sci 1148:64–73

    Article  PubMed  Google Scholar 

  • Jones KR, Myers B, Herman JP (2011) Stimulation of the prelimbic cortex differentially modulates neuroendocrine responses to psychogenic and systemic stressors. Physiol Behav 104:266–271

    Article  PubMed  CAS  Google Scholar 

  • Kitchener P, Di Blasi F, Borrelli E, Piazza PV (2004) Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur J Neurosci 19:1837–1846

    Article  PubMed  Google Scholar 

  • Larsson F, Winblad B, Mohammed AH (2002) Psychological stress and environmental adaptation in enriched vs. impoverished housed rats. Pharmacol Biochem Behav 73:193–207

    Article  PubMed  CAS  Google Scholar 

  • Lee EHY, Hsu WL, Ma YL, Lee PJ, Chao CC (2003) Enrichment enhances the expression of sgk, a glucocorticoid-induced gene, and facilitates spatial learning through glutamate AMPA receptor mediation. Eur J Neurosci 18:2842–2852

    Article  PubMed  Google Scholar 

  • Leger M, Bouet V, Freret T, Darmaillacq A-S, Dacher M, Dauphin F, Boulouard M, Schumann-Bard P (2012) Environmental enrichment improves recent but not remote memory in association with a modified brain metabolic activation profile in adult mice. Behav Brain Res 228:22–29

    Article  PubMed  Google Scholar 

  • Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163:78–90

    Article  PubMed  Google Scholar 

  • Lehmann ML, Herkenham M (2011) Environmental enrichment confers stress resiliency to social defeat through an infralimbic cortex-dependent neuroanatomical pathway. J Neurosci 31:6159–6173

    Article  PubMed  CAS  Google Scholar 

  • Lengvári I, Liposits ZS (1977) Diurnal changes in endogenous corticosterone content of some brain regions of rats. Brain Res 124:571–575

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE (2007) The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn 65:209–237

    Article  PubMed  CAS  Google Scholar 

  • Maier SF, Amat J, Baratta MV, Paul E, Watkins LR (2006) Behavioral control, the medial prefrontal cortex, and resilience. Dialogues Clin Neurosci 8:397–406

    PubMed  Google Scholar 

  • Mark GP, Rada PV, Shors TJ (1996) Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 74:767–774

    Article  PubMed  CAS  Google Scholar 

  • McEwen BS, De Kloet ER, Rostene W (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121–1188

    PubMed  CAS  Google Scholar 

  • Meaney MJ, Aitken DH (1985) [3H]Dexamethasone binding in rat frontal cortex. Brain Res 328:176–180

    Article  PubMed  CAS  Google Scholar 

  • Mizoguchi K, Ishige A, Takeda S, Aburada M, Tabira T (2004) Endogenous glucocorticoids are essential for maintaining prefrontal cortical cognitive function. J Neurosci 24:5492–5499

    Article  PubMed  CAS  Google Scholar 

  • Mlynarik M, Johansson BB, Jezova D (2004) Enriched environment influences adrenocortical response to immune challenge and glutamate receptor gene expression in rat hippocampus. Ann N Y Acad Sci 1018:273–280

    Article  PubMed  CAS  Google Scholar 

  • Moncek F, Duncko R, Johansson BB, Jezova D (2004) Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423–431

    Article  PubMed  CAS  Google Scholar 

  • Mora F, Segovia G, del Arco A (2007) Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 55:78–88

    Article  PubMed  CAS  Google Scholar 

  • Mora F, Segovia G, del Arco A, de Blas M, Garrido P (2012) Stress, neurotransmitters, corticosterone and body–brain integration. Brain Res 1476:71–85

    Article  PubMed  CAS  Google Scholar 

  • Murphy BL, Arnsten AF, Goldman-Rakic PS, Roth RH (1996) Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Natl Acad Sci USA 93:1325–1329

    Article  PubMed  CAS  Google Scholar 

  • Oitzl MS, Fluttert M, Ron de Kloet E (1994) The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur J Neurosci 6:1072–1079

    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 

  • Park CR, Campbell AM, Woodson JC, Smith TP, Fleshner M, Diamond DM (2006) Permisive influence of the stress in the expression of a U-shaped relationship between serum corticosterone levels and spatial memory errors in rats. Dose Response 4:55–74

    Article  PubMed  CAS  Google Scholar 

  • Park CR, Zoladz PR, Conrad CD, Fleshner M, Diamond DM (2008) Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learn Mem 15:271–280

    Article  PubMed  Google Scholar 

  • Paul AD (2004) An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev 28:699–709

    Article  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Peña Y, Prunell M, Rotllant D, Armario A, Escorihuela RM (2009) Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 34:1390–1404

    Article  PubMed  CAS  Google Scholar 

  • Radley JJ, Arias CM, Sawchenko PE (2006) Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26:12967–12976

    Article  PubMed  CAS  Google Scholar 

  • Ragozzino ME (2002) The effects of dopamine D(1) receptor blockade in the prelimbic–infralimbic areas on behavioral flexibility. Learn Mem 9:18–28

    Article  PubMed  Google Scholar 

  • Reul JMHM, Kloet ERD (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505–2511

    Article  PubMed  CAS  Google Scholar 

  • Rich EL, Shapiro ML (2007) Prelimbic/infralimbic inactivation impairs memory for multiple task switches, but not flexible selection of familiar tasks. J Neurosci 27:4747–4755

    Article  PubMed  CAS  Google Scholar 

  • Richard CT (1999) The influences of rearing environment and neonatal choline dietary supplementation on spatial learning and memory in adult rats. Behav Brain Res 105:173–188

    Article  Google Scholar 

  • Robbins TW (2005) Controlling stress: how the brain protects itself from depression. Nat Neurosci 8:261–262

    Article  PubMed  CAS  Google Scholar 

  • Robbins TW, Roberts AC (2007) Differential regulation of fronto-executive function by the monoamines and acetylcholine. Cereb Cortex 17:i151–i160

    Article  PubMed  Google Scholar 

  • Roozendaal B, McEwen BS, Chattarji S (2009a) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433

    Article  PubMed  CAS  Google Scholar 

  • Roozendaal B, McReynolds JR, Van der Zee EA, Lee S, McGaugh JL, McIntyre CK (2009b) Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J Neurosci 29:14299–14308

    Article  PubMed  CAS  Google Scholar 

  • Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325:1017–1020

    Article  PubMed  CAS  Google Scholar 

  • Sandi C, Pinelo-Nava T (2007) Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007:78970

    Article  PubMed  Google Scholar 

  • Sandi C, Venero C, Guaza C (1996) Novelty-related rapid locomotor effects of corticosterone in rats. Eur J Neurosci 8:794–800

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Sarter M, Bruno JP (1997) Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Rev 23:28–46

    Article  PubMed  CAS  Google Scholar 

  • Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M (2010) Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry 15:1152–1163

    Article  PubMed  CAS  Google Scholar 

  • Schrijver NC, Bahr NI, Weiss IC, Wurbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73:209–224

    Article  PubMed  CAS  Google Scholar 

  • Seamans JK, Floresco SB, Phillips AG (1998) D1 receptor modulation of hippocampus “prefrontal cortical circuits integrating spatial memory with executive functions in the rat”. J Neurosci 18:1613–1621

    PubMed  CAS  Google Scholar 

  • Seamans JK, Phillips AF (1994) Selective memory impairments produced by transient lidocaine-induced lesions of the nucleus accumbens in rats. Behav Neurosci 108:456–468

    Google Scholar 

  • Segovia G, Del Arco A, de Blas M, Garrido P, Mora F (2008a) Effects of an enriched environment on the release of dopamine in the prefrontal cortex produced by stress and on working memory during aging in the awake rat. Behav Brain Res 187:304–311

    Article  PubMed  CAS  Google Scholar 

  • Segovia G, Del Arco A, Garrido P, de Blas M, Mora F (2008b) Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging. Neurochem Int 52:1198–1203

    Article  PubMed  CAS  Google Scholar 

  • Segovia G, del Arco A, Mora F (2009) Environmental enrichment, prefrontal cortex, stress, and aging of the brain. J Neural Transm 116:1007–1016

    Article  PubMed  CAS  Google Scholar 

  • Shukitt-Hale B, McEwen JJ, Szprengiel A, Joseph JA (2004) Effect of age on the radial arm water maze—a test of spatial learning and memory. Neurobiol Aging 25:223–229

    Article  PubMed  Google Scholar 

  • Stalnaker TA, España RA, Berridge CW (2009) Coping behavior causes asymmetric changes in neuronal activation in the prefrontal cortex and amygdala. Synapse 63:82–85

    Article  PubMed  CAS  Google Scholar 

  • Sullivan RM (2004) Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress 7:131–143

    Article  PubMed  CAS  Google Scholar 

  • Sztainberg Y, Kuperman Y, Tsoory M, Lebow M, Chen A (2010) The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Mol Psychiatry 15:905–917

    Article  PubMed  CAS  Google Scholar 

  • Szyf M, McGowan P, Meaney MJ (2008) The social environment and the epigenome. Environ Mol Mutagen 49:46–60

    Article  PubMed  CAS  Google Scholar 

  • Thierry AM, Tassin JP, Blanc G, Glowinski J (1976) Selective activation of the mesocortical DA system by stress. Nature 263:242–244

    Article  PubMed  CAS  Google Scholar 

  • Thoeringer CK, Sillaber I, Roedel A, Erhardt A, Mueller MB, Ohl F, Holsboer F, Keck ME (2007) The temporal dynamics of intrahippocampal corticosterone in response to stress-related stimuli with different emotional and physical load: an in vivo microdialysis study in C57BL/6 and DBA/2 inbred mice. Psychoneuroendocrinology 32:746–757

    Article  PubMed  CAS  Google Scholar 

  • Weinberg MS, Johnson DC, Bhatt AP, Spencer RL (2010) Medial prefrontal cortex activity can disrupt the expression of stress response habituation. Neuroscience 168:744–756

    Article  PubMed  CAS  Google Scholar 

  • Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263–276

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann A, Stauffacher M, Langhans W, Wurbel H (2001) Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav Brain Res 121:11–20

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by SAF-2006-01554 and SAF-2009-09053. Pedro Garrido and Marta de Blas are recipients for fellowships from the Ministerio de Educación and Universidad Complutense de Madrid, respectively. The authors deeply acknowledge the excellent technical support of Ángela Amores.

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The authors declare no conflict of interest.

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Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, Universidad Complutense, 28040, Madrid, Spain

    P. Garrido, M. De Blas, G. Ronzoni, I. Cordero, M. Antón, A. Del Arco, G. Segovia & F. Mora

  2. Department of Biochemistry, Faculty of Medicine, Universidad Complutense, 28040, Madrid, Spain

    E. Giné & A. Santos

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  1. P. Garrido
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  2. M. De Blas
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  3. G. Ronzoni
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Correspondence to G. Segovia.

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P. Garrido and M. De Blas contributed equally to this work.

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Garrido, P., De Blas, M., Ronzoni, G. et al. Differential effects of environmental enrichment and isolation housing on the hormonal and neurochemical responses to stress in the prefrontal cortex of the adult rat: relationship to working and emotional memories. J Neural Transm 120, 829–843 (2013). https://doi.org/10.1007/s00702-012-0935-3

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