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Published in: Journal of Neural Transmission 8/2009

01-08-2009 | Basic Neurosciences, Genetics and Immunology - Review Article

Environmental enrichment, prefrontal cortex, stress, and aging of the brain

Authors: Gregorio Segovia, Alberto del Arco, Francisco Mora

Published in: Journal of Neural Transmission | Issue 8/2009

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Abstract

As a result of living in an enriched environment, the brain of animals undergoes molecular and morphological changes leading to improvements in learning and memory. These improvements correlate well with increase in neurogenesis, synaptic density, or neurotrophic factors. We review here, in the context of the literature, the experiments performed in our own laboratory on the effects of environmental enrichment on the dynamics of dopamine and acetylcholine in the prefrontal cortex under a situation of acute mild stress. In these last studies we found that the release of dopamine and acetylcholine under stress is reduced in animals housed in an enriched environment. We also reported that the stress-induced release of dopamine but not acetylcholine is lower in aged rats compared with young rats. These results suggest that environmental enrichment reduces the reactivity to stress of the prefrontal dopaminergic and cholinergic systems in the rat. We further hypothesize that the positive effects on stress coping behaviors of housing animals in an enriched environment are associated with reductions, rather than increases, in the release of dopamine and acetylcholine in the prefrontal cortex. Finally we propose that a reduction in the stress-induced release of dopamine observed during aging in control animals might be an index of a better adaptation to stressful stimuli.
Literature
go back to reference Abercrombie ED, Keefe KA, Daniel SD, Zigmond MJ (1989) Differential effects of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52:1655–1658PubMed Abercrombie ED, Keefe KA, Daniel SD, Zigmond MJ (1989) Differential effects of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52:1655–1658PubMed
go back to reference Acquas E, Wilson C, Fibiger HC (1996) Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci 16:3089–3096PubMed Acquas E, Wilson C, Fibiger HC (1996) Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci 16:3089–3096PubMed
go back to reference Aggleton JP, Blindt HS, Candy JM (1989) Working memory in aged rats. Behav Neurosci 103:975–983PubMed Aggleton JP, Blindt HS, Candy JM (1989) Working memory in aged rats. Behav Neurosci 103:975–983PubMed
go back to reference 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 8:365–371PubMed 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 8:365–371PubMed
go back to reference Amat J, Paul E, Zarza C, Watkins LR, Maier SF (2006) Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: role of the ventral medial prefrontal cortex. J Neurosci 26:13264–13272PubMed Amat J, Paul E, Zarza C, Watkins LR, Maier SF (2006) Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: role of the ventral medial prefrontal cortex. J Neurosci 26:13264–13272PubMed
go back to reference Arnsten AFT (1998) Neuroscience: enhanced: the biology of being frazzled. Science 280:1711–1712PubMed Arnsten AFT (1998) Neuroscience: enhanced: the biology of being frazzled. Science 280:1711–1712PubMed
go back to reference Arnsten AF, Goldman-Rakic PS (1998) Noise stress impairs prefrontal cortical cognitive function in monkeys. Arch Gen Psychiatry 55:362–368PubMed Arnsten AF, Goldman-Rakic PS (1998) Noise stress impairs prefrontal cortical cognitive function in monkeys. Arch Gen Psychiatry 55:362–368PubMed
go back to reference Bardo MT, Bowling SL, Rowlett JK, Manderscheid P, Buxton ST, Dwoskin LP (1995) Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51:397–405PubMed Bardo MT, Bowling SL, Rowlett JK, Manderscheid P, Buxton ST, Dwoskin LP (1995) Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51:397–405PubMed
go back to reference Baskerville KA, Kent C, Nicolle MM, Gallagher M, McKinney M (2006) Aging causes partial loss of basal forebrain but no loss of pontine reticular cholinergic neurons. Neuroreport 17:1819–1823PubMed Baskerville KA, Kent C, Nicolle MM, Gallagher M, McKinney M (2006) Aging causes partial loss of basal forebrain but no loss of pontine reticular cholinergic neurons. Neuroreport 17:1819–1823PubMed
go back to reference Berretta S, Pantazopoulos H, Caldera M, Pantazopoulos P, Paré D (2005) Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala. Neuroscience 132:943–953PubMed Berretta S, Pantazopoulos H, Caldera M, Pantazopoulos P, Paré D (2005) Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala. Neuroscience 132:943–953PubMed
go back to reference Bezard E, Dovero S, Belin D, Duconger S, Jackson-Lewis V, Przedborski S, Piazza PV, Gross CE, Jaber M (2003) Enriched environment confers resistance to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 23:10999–11007PubMed Bezard E, Dovero S, Belin D, Duconger S, Jackson-Lewis V, Przedborski S, Piazza PV, Gross CE, Jaber M (2003) Enriched environment confers resistance to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 23:10999–11007PubMed
go back to reference Biegon A, Duvdevani R, Greenberger V, Segal M (1988) Aging and brain cholinergic muscarinic receptors: an autoradiographic study in the rat. J Neurochem 51:1381–1385PubMed Biegon A, Duvdevani R, Greenberger V, Segal M (1988) Aging and brain cholinergic muscarinic receptors: an autoradiographic study in the rat. J Neurochem 51:1381–1385PubMed
go back to reference 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 28:1589–1596PubMed 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 28:1589–1596PubMed
go back to reference Bowling SL, Rowlett JK, Bardo MT (1993) The effect of enviromental enrichment on amphetamine-sitimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32:885–893PubMed Bowling SL, Rowlett JK, Bardo MT (1993) The effect of enviromental enrichment on amphetamine-sitimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32:885–893PubMed
go back to reference 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 20:1355–1362PubMed 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 20:1355–1362PubMed
go back to reference Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Neurosci 7:30–40 Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Neurosci 7:30–40
go back to reference Cai JX, Arnsten AF (1997) Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys. J Pharmacol Exp Ther 283:183–189PubMed Cai JX, Arnsten AF (1997) Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys. J Pharmacol Exp Ther 283:183–189PubMed
go back to reference Castner SA, Goldman-Rakic PS (2004) Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation. J Neurosci 24:1446–1450PubMed Castner SA, Goldman-Rakic PS (2004) Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation. J Neurosci 24:1446–1450PubMed
go back to reference Charles ST, Almeida DM (2007) Genetic and environmental effects on daily life stressors: more evidence for greater variation in later life. Psychol Aging 22:331–340PubMed Charles ST, Almeida DM (2007) Genetic and environmental effects on daily life stressors: more evidence for greater variation in later life. Psychol Aging 22:331–340PubMed
go back to reference Churchill JD, Galvez R, Colcombe S, Swain RA, Kramer AF, Greenough WT (2002) Exercise, experience and the aging brain. Neurobiol Aging 23:941–955PubMed Churchill JD, Galvez R, Colcombe S, Swain RA, Kramer AF, Greenough WT (2002) Exercise, experience and the aging brain. Neurobiol Aging 23:941–955PubMed
go back to reference Cobo M, Expósito I, Porras A, Mora F (1992) Release of amino acid neurotransmitters in different cortical areas of conscious adult and aged rats. Neurobiol Aging 13:705–709PubMed Cobo M, Expósito I, Porras A, Mora F (1992) Release of amino acid neurotransmitters in different cortical areas of conscious adult and aged rats. Neurobiol Aging 13:705–709PubMed
go back to reference Cobo M, Expósito I, Mora F (1993) Aging, prefrontal cortex, and amino acid neurotransmitters: differential effects produced by electrical stimulation. Neurobiol Aging 14:187–190PubMed Cobo M, Expósito I, Mora F (1993) Aging, prefrontal cortex, and amino acid neurotransmitters: differential effects produced by electrical stimulation. Neurobiol Aging 14:187–190PubMed
go back to reference Cools R, Robbins TW (2004) Chemistry of the adaptive mind. Philos Trans R Soc Lond A 362:2871–2888 Cools R, Robbins TW (2004) Chemistry of the adaptive mind. Philos Trans R Soc Lond A 362:2871–2888
go back to reference 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 664:207–210PubMed 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 664:207–210PubMed
go back to reference Dazzi L, Vacca G, Ladu S, Pisu MG, Serra M, Biggio G (2001) Long-term treatment with antidepressant drugs reduces the sensitivity of cortical cholinergic neurons to the activating actions of stress and the anxiogenic drug FG 7142. Neuropharmacology 41:229–237PubMed Dazzi L, Vacca G, Ladu S, Pisu MG, Serra M, Biggio G (2001) Long-term treatment with antidepressant drugs reduces the sensitivity of cortical cholinergic neurons to the activating actions of stress and the anxiogenic drug FG 7142. Neuropharmacology 41:229–237PubMed
go back to reference de Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475PubMed de Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475PubMed
go back to reference Decker MW (1987) The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res Rev 12:423–438 Decker MW (1987) The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res Rev 12:423–438
go back to reference Del Arco A, Mora F (2001) Dopamine release in the prefrontal cortex during stress is reduced by the local activation of glutamate receptors. Brain Res Bull 56:125–130PubMed Del Arco A, Mora F (2001) Dopamine release in the prefrontal cortex during stress is reduced by the local activation of glutamate receptors. Brain Res Bull 56:125–130PubMed
go back to reference Del Arco A, Mora F (2005) Glutamate-dopamine in vivo interaction in the prefrontal cortex modulates the release of dopamine and acetylcholine in the nucleus accumbens of the awake rat. J Neural Transm 112:97–109PubMed Del Arco A, Mora F (2005) Glutamate-dopamine in vivo interaction in the prefrontal cortex modulates the release of dopamine and acetylcholine in the nucleus accumbens of the awake rat. J Neural Transm 112:97–109PubMed
go back to reference Del Arco A, Segovia G, Mora F (2001) Dopamine release during stress in the prefrontal cortex of the rat decreases with age. Neuroreport 12:4019–4022PubMed Del Arco A, Segovia G, Mora F (2001) Dopamine release during stress in the prefrontal cortex of the rat decreases with age. Neuroreport 12:4019–4022PubMed
go back to reference Del Arco A, Segovia G, Canales JJ, Garrido P, De Blas M, García-Verdugo JM, Mora F (2007a) Environmental enrichment reduces the function of D1 dopamine receptors in the prefrontal cortex of the rat. J Neural Transm 114:43–48PubMed Del Arco A, Segovia G, Canales JJ, Garrido P, De Blas M, García-Verdugo JM, Mora F (2007a) Environmental enrichment reduces the function of D1 dopamine receptors in the prefrontal cortex of the rat. J Neural Transm 114:43–48PubMed
go back to reference Del Arco A, Segovia G, Garrido P, De Blas M, Mora F (2007b) Stress, prefrontal cortex and environmental enrichment: Studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176:267–273PubMed Del Arco A, Segovia G, Garrido P, De Blas M, Mora F (2007b) Stress, prefrontal cortex and environmental enrichment: Studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176:267–273PubMed
go back to reference Diamond MC (2001) Response of the brain to enrichment. An Acad Bras Cienc 73:211–218PubMed Diamond MC (2001) Response of the brain to enrichment. An Acad Bras Cienc 73:211–218PubMed
go back to reference Enrico P, Bouma M, De Vries JB, Westerink BHC (1998) The role of afferents to the ventral tegmental area in the handling stress-induced increase in the release of dopamine in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain. Brain Res 779:205–213PubMed Enrico P, Bouma M, De Vries JB, Westerink BHC (1998) The role of afferents to the ventral tegmental area in the handling stress-induced increase in the release of dopamine in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain. Brain Res 779:205–213PubMed
go back to reference Faherty CJ, Shepherd KR, Herasimtschuk A, Smeyne RJ (2005) Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 134:170–179PubMed Faherty CJ, Shepherd KR, Herasimtschuk A, Smeyne RJ (2005) Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 134:170–179PubMed
go back to reference Feenstra MGP, Botterblom MHA, Mastenbroek S (2000) Dopamine and noradrenaline efflux in the prefrontal cortex in the light and dark period: effects of novelty and handling and comparison to the nucleus accumbens. Neuroscience 100:741–748PubMed Feenstra MGP, Botterblom MHA, Mastenbroek S (2000) Dopamine and noradrenaline efflux in the prefrontal cortex in the light and dark period: effects of novelty and handling and comparison to the nucleus accumbens. Neuroscience 100:741–748PubMed
go back to reference Fernández-Teruel A, Giménez-Llort L, Escorihuela RM, Gil L, Aguilar R, Steimer T, Tobeña A (2002) Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms? Pharmacol Biochem Behav 73:233–245PubMed Fernández-Teruel A, Giménez-Llort L, Escorihuela RM, Gil L, Aguilar R, Steimer T, Tobeña A (2002) Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms? Pharmacol Biochem Behav 73:233–245PubMed
go back to reference Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329:65–68PubMed Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329:65–68PubMed
go back to reference Foster TC, Gagné J, Massicotte G (1996) Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Res 736:243–250PubMed Foster TC, Gagné J, Massicotte G (1996) Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Res 736:243–250PubMed
go back to reference Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175:1–8PubMed Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175:1–8PubMed
go back to reference Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL (1995) Age-related spatial reference and working memory deficits assesed in the water maze. Neurobiol Aging 16:149–160PubMed Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL (1995) Age-related spatial reference and working memory deficits assesed in the water maze. Neurobiol Aging 16:149–160PubMed
go back to reference Fuster JM (1997) The prefrontal cortex. Anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, New York Fuster JM (1997) The prefrontal cortex. Anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, New York
go back to reference Gabbott PLA, Warner TA, Jays PRL, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145–177PubMed Gabbott PLA, Warner TA, Jays PRL, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145–177PubMed
go back to reference Garrido P, De Blas M, Del Arco A, Segovia G, Mora F (2008) Environmental enrichment suppresses dopamine and coricosterone increases produced by acute stress in the prefrontal cortex of the rat. FENS Abstr 4:114.8 Garrido P, De Blas M, Del Arco A, Segovia G, Mora F (2008) Environmental enrichment suppresses dopamine and coricosterone increases produced by acute stress in the prefrontal cortex of the rat. FENS Abstr 4:114.8
go back to reference Goldman-Rakic PS, Brown RM (1981) Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience 6:177–187PubMed Goldman-Rakic PS, Brown RM (1981) Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience 6:177–187PubMed
go back to reference Goldman-Rakic PS, Muly ECIII, Williams GV (2000) D1 receptors in prefrontal cells and circuits. Brain Res Rev 31:295–301PubMed Goldman-Rakic PS, Muly ECIII, Williams GV (2000) D1 receptors in prefrontal cells and circuits. Brain Res Rev 31:295–301PubMed
go back to reference 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 16:4787–4798PubMed 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 16:4787–4798PubMed
go back to reference Goudsmit E, Feenstra MGP, Swaab DF (1990) Central monoamine metabolism in the male brown-Norway rat in relation to aging and testosterone. Brain Res Bull 25:755–763PubMed Goudsmit E, Feenstra MGP, Swaab DF (1990) Central monoamine metabolism in the male brown-Norway rat in relation to aging and testosterone. Brain Res Bull 25:755–763PubMed
go back to reference Hains AB, Arnsten AFT (2008) Molecular mechanisms of stress-induced prefrontal cortical impairment: Implications for mental illness. Learn Mem 15:551–564PubMed Hains AB, Arnsten AFT (2008) Molecular mechanisms of stress-induced prefrontal cortical impairment: Implications for mental illness. Learn Mem 15:551–564PubMed
go back to reference Hedden T, Gabrieli JDE (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 5:87–96PubMed Hedden T, Gabrieli JDE (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 5:87–96PubMed
go back to reference 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 19:1837–1846PubMed 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 19:1837–1846PubMed
go back to reference Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C (2004) Differential heart rate reactivity and recovery after psychosocial stress (TSST) in healthy children, younger adults, and elderly adults: the impact of age and gender. Int J Behav Med 11:116–121PubMed Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C (2004) Differential heart rate reactivity and recovery after psychosocial stress (TSST) in healthy children, younger adults, and elderly adults: the impact of age and gender. Int J Behav Med 11:116–121PubMed
go back to reference Laplante F, Stevenson CW, Gratton A, Srivastava LK, Quirion R (2004) Effects of neonatal ventral hippocampal lesion in rats on stress-induced acetylcholine release in the prefrontal cortex. J Neurochem 91:1473–1482PubMed Laplante F, Stevenson CW, Gratton A, Srivastava LK, Quirion R (2004) Effects of neonatal ventral hippocampal lesion in rats on stress-induced acetylcholine release in the prefrontal cortex. J Neurochem 91:1473–1482PubMed
go back to reference Larsson F, Winblad B, Mohammed AH (2002) Psychological stress and environmental adaptation in enriched versus impoverished housed rats. Pharmacol Biochem Behav 73:193–207PubMed Larsson F, Winblad B, Mohammed AH (2002) Psychological stress and environmental adaptation in enriched versus impoverished housed rats. Pharmacol Biochem Behav 73:193–207PubMed
go back to reference Lee JM, Ross ER, Gower A, Paris JM, Martensson R, Lorens SA (1994) Spatial learning deficits in the aged rat: neuroanatomical and neurochemical correlates. Brain Res Bull 33:489–500PubMed Lee JM, Ross ER, Gower A, Paris JM, Martensson R, Lorens SA (1994) Spatial learning deficits in the aged rat: neuroanatomical and neurochemical correlates. Brain Res Bull 33:489–500PubMed
go back to reference Linthorst ACE, Reul JM (2008) Stress and the brain: solving the puzzle using microdialysis. Pharmacol Biochem Behav 90:163–173PubMed Linthorst ACE, Reul JM (2008) Stress and the brain: solving the puzzle using microdialysis. Pharmacol Biochem Behav 90:163–173PubMed
go back to reference Luine V, Hearns M (1990) Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res 523:321–324PubMed Luine V, Hearns M (1990) Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res 523:321–324PubMed
go back to reference Luine V, Bowling D, Hearns M (1990) Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Res 537:271–278PubMed Luine V, Bowling D, Hearns M (1990) Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Res 537:271–278PubMed
go back to reference Maier SF, Amat J, Baratta MV, Paul E, Watkins LR (2006) Behavioral control, the medial prefrontal cortex, and resilience. Dialogues Clin Neurosci 8:397–406PubMed Maier SF, Amat J, Baratta MV, Paul E, Watkins LR (2006) Behavioral control, the medial prefrontal cortex, and resilience. Dialogues Clin Neurosci 8:397–406PubMed
go back to reference 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 74:767–774PubMed 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 74:767–774PubMed
go back to reference Marx J (2005) Preventing Alzheimer’s: a lifelong commitment? Science 309:864–866PubMed Marx J (2005) Preventing Alzheimer’s: a lifelong commitment? Science 309:864–866PubMed
go back to reference Maswood S, Barter JE, Watkins LR, Maier SF (1998) Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 783:115–120PubMed Maswood S, Barter JE, Watkins LR, Maier SF (1998) Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 783:115–120PubMed
go back to reference Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 7:278–294PubMed Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 7:278–294PubMed
go back to reference McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904PubMed McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904PubMed
go back to reference Means LW, Kennard KJP (1991) Working memory and the aged rat: deficient two-choice win-stay water-escape acquisition and retention. Physiol Behav 49:301–307PubMed Means LW, Kennard KJP (1991) Working memory and the aged rat: deficient two-choice win-stay water-escape acquisition and retention. Physiol Behav 49:301–307PubMed
go back to reference Melendez RI, Gregory ML, Bardo MT, Kalivas PW (2004) Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 29:1980–1987PubMed Melendez RI, Gregory ML, Bardo MT, Kalivas PW (2004) Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 29:1980–1987PubMed
go back to reference Mirmiran M, Van Gool WA, Van Haaren F, Polak CE (1986) Environmental influences on brain and behavior in aging and Alzheimer’s disease. In: Swaab DF, Fliers E, Mirmiran M, Van Gool WA, Van Haaren F (eds) Aging of the brain and alzheimer’s disease. Progress in Brain Research, vol 70. Elsevier, Amsterdam Mirmiran M, Van Gool WA, Van Haaren F, Polak CE (1986) Environmental influences on brain and behavior in aging and Alzheimer’s disease. In: Swaab DF, Fliers E, Mirmiran M, Van Gool WA, Van Haaren F (eds) Aging of the brain and alzheimer’s disease. Progress in Brain Research, vol 70. Elsevier, Amsterdam
go back to reference 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 1018:273–280PubMed 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 1018:273–280PubMed
go back to reference Mohammed AH, Zhu SW, Darmopil S, Hjerling-Leffler J, Ernfors P, Winblad B, Diamond MC, Eriksson PS, Bogdanovic N (2002) Environmental enrichment and the brain. Progress in Brain Research. Elsevier, Amsterdam Mohammed AH, Zhu SW, Darmopil S, Hjerling-Leffler J, Ernfors P, Winblad B, Diamond MC, Eriksson PS, Bogdanovic N (2002) Environmental enrichment and the brain. Progress in Brain Research. Elsevier, Amsterdam
go back to reference Moncek F, Duncko R, Johansson BB, Jezova D (2004) Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423–431PubMed Moncek F, Duncko R, Johansson BB, Jezova D (2004) Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423–431PubMed
go back to reference Mora F, Sweeney KF, Rolls ET, Sanguinetti AM (1976) Spontaneous firing rate of neurons in the prefrontal cortex of the rat: evidence for a dopaminergic inhibition. Brain Res 116:516–522PubMed Mora F, Sweeney KF, Rolls ET, Sanguinetti AM (1976) Spontaneous firing rate of neurons in the prefrontal cortex of the rat: evidence for a dopaminergic inhibition. Brain Res 116:516–522PubMed
go back to reference 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 55:78–88PubMed 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 55:78–88PubMed
go back to reference Mora F, Segovia G, Del Arco A (2008) Glutamate–dopamine–GABA interactions in the aging basal ganglia. Brain Res Rev 58:340–353PubMed Mora F, Segovia G, Del Arco A (2008) Glutamate–dopamine–GABA interactions in the aging basal ganglia. Brain Res Rev 58:340–353PubMed
go back to reference Murphy BL, Arnsten AFT, 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 93:1325–1329PubMed Murphy BL, Arnsten AFT, 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 93:1325–1329PubMed
go back to reference Naka F, Narita N, Okado N, Narita M (2005) Modification of AMPA receptor properties following environmental enrichment. Brain Dev 27:275–278PubMed Naka F, Narita N, Okado N, Narita M (2005) Modification of AMPA receptor properties following environmental enrichment. Brain Dev 27:275–278PubMed
go back to reference Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709PubMed Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709PubMed
go back to reference Perls ET, Silver MH (2000) Living to 100: lessons in living your maximum potential at any age. Basic Books, New York Perls ET, Silver MH (2000) Living to 100: lessons in living your maximum potential at any age. Basic Books, New York
go back to reference Phillips AG, Ahn S, Floresco SB (2004) Magnitude of dopamine release in medial prefrontal cortex predict accuracy of memory on delayed response task. J Neurosci 24:547–553PubMed Phillips AG, Ahn S, Floresco SB (2004) Magnitude of dopamine release in medial prefrontal cortex predict accuracy of memory on delayed response task. J Neurosci 24:547–553PubMed
go back to reference Porras A, Sanz B, Mora F (1997) Dopamine–glutamate interactions in the prefrontal cortex of the conscious rat: studies on ageing. Mech Ageing Dev 99:9–17PubMed Porras A, Sanz B, Mora F (1997) Dopamine–glutamate interactions in the prefrontal cortex of the conscious rat: studies on ageing. Mech Ageing Dev 99:9–17PubMed
go back to reference Rasmuson S, Olsson T, Henriksson BG, Kelly PAT, Holmes MC, Seckl JR, Mohammed AH (1998) Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Mol Brain Res 53:285–290PubMed Rasmuson S, Olsson T, Henriksson BG, Kelly PAT, Holmes MC, Seckl JR, Mohammed AH (1998) Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Mol Brain Res 53:285–290PubMed
go back to reference Robbins TW (1997) Arousal systems and attentional processes. Biol Psychiatry 45:57–71CrossRef Robbins TW (1997) Arousal systems and attentional processes. Biol Psychiatry 45:57–71CrossRef
go back to reference Robbins TW (2000) From arousal to cognition: integrative position of the prefrontal cortex. Prog Brain Res 126:469–483PubMed Robbins TW (2000) From arousal to cognition: integrative position of the prefrontal cortex. Prog Brain Res 126:469–483PubMed
go back to reference Robbins TW (2005) Controlling stress: how the brain protects itself from depression. Nat Neurosci 8:261–262PubMed Robbins TW (2005) Controlling stress: how the brain protects itself from depression. Nat Neurosci 8:261–262PubMed
go back to reference Rosenkranz JA, Grace AA (2002) Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 22:324–337PubMed Rosenkranz JA, Grace AA (2002) Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 22:324–337PubMed
go back to reference Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65PubMed Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65PubMed
go back to reference Rouge-Pont F, Deroche V, Le Moal M, Piazza PV (1998) Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone. Eur J Neurosci 10:3903–3907PubMed Rouge-Pont F, Deroche V, Le Moal M, Piazza PV (1998) Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone. Eur J Neurosci 10:3903–3907PubMed
go back to reference Sarter M, Bruno JP (2000) Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95:933–952PubMed Sarter M, Bruno JP (2000) Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95:933–952PubMed
go back to reference Sarter M, Bruno JP (2004) Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol Aging 25:1127–1139PubMed Sarter M, Bruno JP (2004) Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol Aging 25:1127–1139PubMed
go back to reference Schrijver NCA, Bahr NI, Weiss IC, Würbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73:209–224PubMed Schrijver NCA, Bahr NI, Weiss IC, Würbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73:209–224PubMed
go back to reference Segovia G, Mora F (2005) Effects of the metabotropic glutamate receptor agonist, ACPD, on the extracellular concentrations of GABA and acetylcholine in the prefrontal cortex of the rat during the normal process of aging. Brain Res Bull 65:11–16PubMed Segovia G, Mora F (2005) Effects of the metabotropic glutamate receptor agonist, ACPD, on the extracellular concentrations of GABA and acetylcholine in the prefrontal cortex of the rat during the normal process of aging. Brain Res Bull 65:11–16PubMed
go back to reference Segovia G, Porras A, Del Arco A, Mora F (2001) Glutamatergic neurotransmission in aging: a critical perspective. Mech Ageing Dev 122:1–29PubMed Segovia G, Porras A, Del Arco A, Mora F (2001) Glutamatergic neurotransmission in aging: a critical perspective. Mech Ageing Dev 122:1–29PubMed
go back to reference Segovia G, Yagüe AG, García-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 70:8–14PubMed Segovia G, Yagüe AG, García-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 70:8–14PubMed
go back to reference 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 187:304–311PubMed 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 187:304–311PubMed
go back to reference 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 52:1198–1203PubMed 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 52:1198–1203PubMed
go back to reference Seif GI, Clements KM, Wainwright PE (2004) Effects of distraction and stress on delayed matching-to-place performance in aged rats. Physiol Behav 82:477–487PubMed Seif GI, Clements KM, Wainwright PE (2004) Effects of distraction and stress on delayed matching-to-place performance in aged rats. Physiol Behav 82:477–487PubMed
go back to reference Stawski RS, Sliwinski MJ, Smyth JM (2006) Stress-related cognitive interference predicts cognitive function in old age. Psychol Aging 21:535–544PubMed Stawski RS, Sliwinski MJ, Smyth JM (2006) Stress-related cognitive interference predicts cognitive function in old age. Psychol Aging 21:535–544PubMed
go back to reference Stemmelin J, Lazarus C, Cassel S, Kelche C, Cassel J-C (2004) Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 96:275–289 Stemmelin J, Lazarus C, Cassel S, Kelche C, Cassel J-C (2004) Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 96:275–289
go back to reference Stevenson CW, Gratton A (2003) Basolateral amygdala modulation of the nucleus accumbens dopamine response to stress: role of the medial prefrontal cortex. Eur J Neurosci 17:1287–1295PubMed Stevenson CW, Gratton A (2003) Basolateral amygdala modulation of the nucleus accumbens dopamine response to stress: role of the medial prefrontal cortex. Eur J Neurosci 17:1287–1295PubMed
go back to reference Takahata R, Moghaddam B (1998) Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex. J Neurochem 71:1443–1449PubMedCrossRef Takahata R, Moghaddam B (1998) Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex. J Neurochem 71:1443–1449PubMedCrossRef
go back to reference Tanila H, Taira T, Piepponen TP, Honkanen A (1994) Effect of sex and age on brain monoamines and spatial learning in rats. Neurobiol Aging 15:733–741PubMed Tanila H, Taira T, Piepponen TP, Honkanen A (1994) Effect of sex and age on brain monoamines and spatial learning in rats. Neurobiol Aging 15:733–741PubMed
go back to reference Terry RD, Katzman R (2001) Life span and synapses: will there be a primary senile dementia? Neurobiol Aging 22:347–348PubMed Terry RD, Katzman R (2001) Life span and synapses: will there be a primary senile dementia? Neurobiol Aging 22:347–348PubMed
go back to reference Thierry AM, Tassin JP, Blanc G, Glowinski J (1976) Selective activation of mesocortical DA system by stress. Nature 263:242–244PubMed Thierry AM, Tassin JP, Blanc G, Glowinski J (1976) Selective activation of mesocortical DA system by stress. Nature 263:242–244PubMed
go back to reference Tzschentke TM (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog Neurobiol 63:241–320PubMed Tzschentke TM (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog Neurobiol 63:241–320PubMed
go back to reference van Gelder BM, Tijhuis MAR, Kalmijn S, Giampaoli S, Nissinen A, Kromhout D (2004) Physical activity in relation to cognitive decline in elderly men: the FINE study. Neurology 63:2316–2321PubMed van Gelder BM, Tijhuis MAR, Kalmijn S, Giampaoli S, Nissinen A, Kromhout D (2004) Physical activity in relation to cognitive decline in elderly men: the FINE study. Neurology 63:2316–2321PubMed
go back to reference van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198PubMed van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198PubMed
go back to reference Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58PubMed Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58PubMed
go back to reference Wagner AK, Chen X, Kline AE, Li Y, Zafonte RD, Dixon CE (2005) Gender and environmental enrichment impact dopamine transporter expression after experimental traumatic brain injury. Exp Neurol 195:475–483PubMed Wagner AK, Chen X, Kline AE, Li Y, Zafonte RD, Dixon CE (2005) Gender and environmental enrichment impact dopamine transporter expression after experimental traumatic brain injury. Exp Neurol 195:475–483PubMed
go back to reference Wenk GL, Pierce DJ, Struble RG, Price DL, Corks LC (1989) Aged-related changes in the multiple neurotransmitter systems in the monkey brain. Neurobiol Aging 10:11–19PubMed Wenk GL, Pierce DJ, Struble RG, Price DL, Corks LC (1989) Aged-related changes in the multiple neurotransmitter systems in the monkey brain. Neurobiol Aging 10:11–19PubMed
go back to reference Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263–276PubMed Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263–276PubMed
go back to reference Wilson RS, Mendes de Leon CF, Barnes LL, Schneider JA, Bienias JL, Evans DA, Bennett DA (2002) Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287:742–748PubMed Wilson RS, Mendes de Leon CF, Barnes LL, Schneider JA, Bienias JL, Evans DA, Bennett DA (2002) Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287:742–748PubMed
go back to reference Wood DA, Buse JE, Wellman CL, Rebec GV (2005) Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell. Brain Res 1042:176–183PubMed Wood DA, Buse JE, Wellman CL, Rebec GV (2005) Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell. Brain Res 1042:176–183PubMed
go back to reference Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE (1997) Cortical input to the basal forebrain. Neuroscience 79:1051–1078PubMed Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE (1997) Cortical input to the basal forebrain. Neuroscience 79:1051–1078PubMed
go back to reference Zhu J, Green T, Bardo MT, Dwoskin LP (2004) Environmental enrichment enhances sensitization to GBR 12935-induced activity and decreases dopamine transporter function in the medial prefrontal cortex. Behav Brain Res 148:107–117PubMed Zhu J, Green T, Bardo MT, Dwoskin LP (2004) Environmental enrichment enhances sensitization to GBR 12935-induced activity and decreases dopamine transporter function in the medial prefrontal cortex. Behav Brain Res 148:107–117PubMed
go back to reference Zhu J, Apparsundaram S, Bardo MT, Dwoskin LP (2005) Environmental enrichment decreases cell surface expression of the dopamine transporter in rat medial prefrontal cortex. J Neurochem 93:1434–1443PubMed Zhu J, Apparsundaram S, Bardo MT, Dwoskin LP (2005) Environmental enrichment decreases cell surface expression of the dopamine transporter in rat medial prefrontal cortex. J Neurochem 93:1434–1443PubMed
go back to reference 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 121:11–20PubMed 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 121:11–20PubMed
Metadata
Title
Environmental enrichment, prefrontal cortex, stress, and aging of the brain
Authors
Gregorio Segovia
Alberto del Arco
Francisco Mora
Publication date
01-08-2009
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 8/2009
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-009-0214-0

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