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

Journal of Neural Transmission

Volumn 116, Issue 8, 2009, Pages 1007-1016

  Segovia, Gregorio ^a   Arco, Alberto Del ^a   Mora, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Acetylcholine; Aging; Dopamine; Environmental enrichment; Prefrontal cortex; Stress

Indexed keywords

ACETYLCHOLINE; DOPAMINE; NEUROTROPHIC FACTOR;

ACETYLCHOLINE RELEASE; ACUTE STRESS; ADAPTATION; AGING; CHOLINERGIC SYSTEM; CONFERENCE PAPER; COPING BEHAVIOR; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; ENVIRONMENTAL FACTOR; LEARNING; MEMORY; MENTAL STRESS; MORPHOLOGY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL;

ACETYLCHOLINE; AGING; ANIMALS; BRAIN; DOPAMINE; ENVIRONMENT; GLUCOCORTICOIDS; HOUSING, ANIMAL; HUMANS; MODELS, NEUROLOGICAL; PREFRONTAL CORTEX; STRESS, PSYCHOLOGICAL;

EID: 67651249565     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-009-0214-0     Document Type: Conference Paper

References (115)

1. ED Abercrombie KA Keefe SD Daniel MJ Zigmond 1989 Differential effects of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex J Neurochem 52 1655 1658
2. E Acquas C Wilson HC Fibiger 1996 Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear J Neurosci 16 3089 3096
3. JP Aggleton HS Blindt JM Candy 1989 Working memory in aged rats Behav Neurosci 103 975 983
4. J Amat MV Baratta E Paul ST Bland LR Watkins SF Maier 2005 Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus Nat Neurosci 8 365 371
5. J Amat E Paul C Zarza LR Watkins SF Maier 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 13272
6. AFT Arnsten 1998 Neuroscience: enhanced: the biology of being frazzled Science 280 1711 1712
7. AF Arnsten PS Goldman-Rakic 1998 Noise stress impairs prefrontal cortical cognitive function in monkeys Arch Gen Psychiatry 55 362 368
8. MT Bardo SL Bowling JK Rowlett P Manderscheid ST Buxton LP Dwoskin 1995 Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine Pharmacol Biochem Behav 51 397 405
9. KA Baskerville C Kent MM Nicolle M Gallagher M McKinney 2006 Aging causes partial loss of basal forebrain but no loss of pontine reticular cholinergic neurons Neuroreport 17 1819 1823
10. S Berretta H Pantazopoulos M Caldera P Pantazopoulos D Paré 2005 Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala Neuroscience 132 943 953
11. E Bezard S Dovero D Belin S Duconger V Jackson-Lewis S Przedborski PV Piazza CE Gross M Jaber 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 11007
12. A Biegon R Duvdevani V Greenberger M Segal 1988 Aging and brain cholinergic muscarinic receptors: an autoradiographic study in the rat J Neurochem 51 1381 1385
13. ST Bland D Hargrave JL Pepin J Amat LR Watkins SF Maier 2003 Stressor controllability modulates stress-induced dopamine and serotonin efflux and morphine-induced serotonin efflux in the medial prefrontal cortex Neuropsychopharmacology 28 1589 1596
14. SL Bowling JK Rowlett MT Bardo 1993 The effect of enviromental enrichment on amphetamine-sitimulated locomotor activity, dopamine synthesis and dopamine release Neuropharmacology 32 885 893
15. TW Bredy TY Zhang RJ Grant J Diorio MJ Meaney 2004 Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression Eur J Neurosci 20 1355 1362
16. SN Burke CA Barnes 2006 Neural plasticity in the ageing brain Nat Neurosci 7 30 40
17. JX Cai AF Arnsten 1997 Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys J Pharmacol Exp Ther 283 183 189
18. SA Castner PS Goldman-Rakic 2004 Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation J Neurosci 24 1446 1450
19. ST Charles DM Almeida 2007 Genetic and environmental effects on daily life stressors: more evidence for greater variation in later life Psychol Aging 22 331 340
20. JD Churchill R Galvez S Colcombe RA Swain AF Kramer WT Greenough 2002 Exercise, experience and the aging brain Neurobiol Aging 23 941 955
21. M Cobo I Expósito A Porras F Mora 1992 Release of amino acid neurotransmitters in different cortical areas of conscious adult and aged rats Neurobiol Aging 13 705 709
22. M Cobo I Expósito F Mora 1993 Aging, prefrontal cortex, and amino acid neurotransmitters: differential effects produced by electrical stimulation Neurobiol Aging 14 187 190
23. R Cools TW Robbins 2004 Chemistry of the adaptive mind Philos Trans R Soc Lond A 362 2871 2888
24. M Davis JM Hithcock MB Bowers CW Berridge KR Melia RH Roth 1994 Stress-induced activation of prefrontal cortex dopamine turnover: blockade by lesions of the amygdala Brain Res 664 207 210
25. L Dazzi G Vacca S Ladu MG Pisu M Serra G Biggio 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 41 229 237
26. ER de Kloet M Joëls F Holsboer 2005 Stress and the brain: from adaptation to disease Nat Rev Neurosci 6 463 475
27. MW Decker 1987 The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system Brain Res Rev 12 423 438
28. A Del Arco F Mora 2001 Dopamine release in the prefrontal cortex during stress is reduced by the local activation of glutamate receptors Brain Res Bull 56 125 130
29. A Del Arco F Mora 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 97 109
30. A Del Arco G Segovia F Mora 2001 Dopamine release during stress in the prefrontal cortex of the rat decreases with age Neuroreport 12 4019 4022
31. A Del Arco G Segovia JJ Canales P Garrido M De Blas JM García-Verdugo F Mora 2007 Environmental enrichment reduces the function of D1 dopamine receptors in the prefrontal cortex of the rat J Neural Transm 114 43 48
32. A Del Arco G Segovia P Garrido M De Blas F Mora 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
33. MC Diamond 2001 Response of the brain to enrichment An Acad Bras Cienc 73 211 218
34. P Enrico M Bouma JB De Vries BHC Westerink 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 779 205 213 (Pubitemid 28039953)
35. CJ Faherty KR Shepherd A Herasimtschuk RJ Smeyne 2005 Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism Brain Res Mol Brain Res 134 170 179
36. MGP Feenstra MHA Botterblom S Mastenbroek 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 100 741 748
37. A Fernández-Teruel L Giménez-Llort RM Escorihuela L Gil R Aguilar T Steimer A Tobeña 2002 Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms? Pharmacol Biochem Behav 73 233 245
38. W Fischer K Wictorin A Bjorklund LR Williams S Varon FH Gage 1987 Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor Nature 329 65 68
39. TC Foster J Gagné G Massicotte 1996 Mechanism of altered synaptic strength due to experience: relation to long-term potentiation Brain Res 736 243 250
40. C Fox Z Merali C Harrison 2006 Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress Behav Brain Res 175 1 8
41. KM Frick MG Baxter AL Markowska DS Olton DL Price 1995 Age-related spatial reference and working memory deficits assesed in the water maze Neurobiol Aging 16 149 160
42. Fuster JM (1997) The prefrontal cortex. Anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, New York
43. PLA Gabbott TA Warner PRL Jays P Salway SJ Busby 2005 Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers J Comp Neurol 492 145 177
44. P Garrido M De Blas A Del Arco G Segovia F Mora 2008 Environmental enrichment suppresses dopamine and coricosterone increases produced by acute stress in the prefrontal cortex of the rat FENS Abstr 4 114.8
45. PS Goldman-Rakic RM Brown 1981 Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys Neuroscience 6 177 187
46. PS Goldman-Rakic EC Muly III GV Williams 2000 D1 receptors in prefrontal cells and circuits Brain Res Rev 31 295 301
47. LE Goldstein AM Rasmusson BS Bunney RH Roth 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
48. E Goudsmit MGP Feenstra DF Swaab 1990 Central monoamine metabolism in the male brown-Norway rat in relation to aging and testosterone Brain Res Bull 25 755 763
49. AB Hains AFT Arnsten 2008 Molecular mechanisms of stress-induced prefrontal cortical impairment: Implications for mental illness Learn Mem 15 551 564
50. T Hedden JDE Gabrieli 2004 Insights into the ageing mind: a view from cognitive neuroscience Nat Rev Neurosci 5 87 96
51. P Kitchener F Di Blasi E Borrelli PV Piazza 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
52. BM Kudielka A Buske-Kirschbaum DH Hellhammer C Kirschbaum 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 11 116 121 (Pubitemid 39093269)
53. F Laplante CW Stevenson A Gratton LK Srivastava R Quirion 2004 Effects of neonatal ventral hippocampal lesion in rats on stress-induced acetylcholine release in the prefrontal cortex J Neurochem 91 1473 1482 (Pubitemid 39658573)
54. F Larsson B Winblad AH Mohammed 2002 Psychological stress and environmental adaptation in enriched versus impoverished housed rats Pharmacol Biochem Behav 73 193 207
55. JM Lee ER Ross A Gower JM Paris R Martensson SA Lorens 1994 Spatial learning deficits in the aged rat: neuroanatomical and neurochemical correlates Brain Res Bull 33 489 500
56. ACE Linthorst JM Reul 2008 Stress and the brain: solving the puzzle using microdialysis Pharmacol Biochem Behav 90 163 173
57. V Luine M Hearns 1990 Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT Brain Res 523 321 324
58. V Luine D Bowling M Hearns 1990 Spatial memory deficits in aged rats: contributions of monoaminergic systems Brain Res 537 271 278
59. SF Maier J Amat MV Baratta E Paul LR Watkins 2006 Behavioral control, the medial prefrontal cortex, and resilience Dialogues Clin Neurosci 8 397 406
60. GP Mark PV Rada TJ Shors 1996 Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala Neuroscience 74 767 774
61. J Marx 2005 Preventing Alzheimer's: a lifelong commitment? Science 309 864 866
62. S Maswood JE Barter LR Watkins SF Maier 1998 Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat Brain Res 783 115 120
63. MP Mattson T Magnus 2006 Ageing and neuronal vulnerability Nat Rev Neurosci 7 278 294
64. BS McEwen 2007 Physiology and neurobiology of stress and adaptation: central role of the brain Physiol Rev 87 873 904
65. LW Means KJP Kennard 1991 Working memory and the aged rat: deficient two-choice win-stay water-escape acquisition and retention Physiol Behav 49 301 307
66. RI Melendez ML Gregory MT Bardo PW Kalivas 2004 Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex Neuropsychopharmacology 29 1980 1987
67. 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
68. M Mlynarik BB Johansson D Jezova 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
69. 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
70. F Moncek R Duncko BB Johansson D Jezova 2004 Effect of environmental enrichment on stress related systems in rats J Neuroendocrinol 16 423 431
71. F Mora KF Sweeney ET Rolls AM Sanguinetti 1976 Spontaneous firing rate of neurons in the prefrontal cortex of the rat: evidence for a dopaminergic inhibition Brain Res 116 516 522
72. F Mora G Segovia A Del Arco 2007 Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain Brain Res Rev 55 78 88
73. F Mora G Segovia A Del Arco 2008 Glutamate-dopamine-GABA interactions in the aging basal ganglia Brain Res Rev 58 340 353
74. BL Murphy AFT Arnsten PS Goldman-Rakic RH Roth 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
75. F Naka N Narita N Okado M Narita 2005 Modification of AMPA receptor properties following environmental enrichment Brain Dev 27 275 278
76. J Nithianantharajah AJ Hannan 2006 Enriched environments, experience-dependent plasticity and disorders of the nervous system Nat Rev Neurosci 7 697 709
77. Perls ET, Silver MH (2000) Living to 100: lessons in living your maximum potential at any age. Basic Books, New York
78. AG Phillips S Ahn SB Floresco 2004 Magnitude of dopamine release in medial prefrontal cortex predict accuracy of memory on delayed response task J Neurosci 24 547 553
79. A Porras B Sanz F Mora 1997 Dopamine-glutamate interactions in the prefrontal cortex of the conscious rat: studies on ageing Mech Ageing Dev 99 9 17
80. S Rasmuson T Olsson BG Henriksson PAT Kelly MC Holmes JR Seckl AH Mohammed 1998 Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus Mol Brain Res 53 285 290
81. TW Robbins 1997 Arousal systems and attentional processes Biol Psychiatry 45 57 71
82. TW Robbins 2000 From arousal to cognition: integrative position of the prefrontal cortex Prog Brain Res 126 469 483
83. TW Robbins 2005 Controlling stress: how the brain protects itself from depression Nat Neurosci 8 261 262
84. JA Rosenkranz AA Grace 2002 Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo J Neurosci 22 324 337
85. MR Rosenzweig EL Bennett 1996 Psychobiology of plasticity: effects of training and experience on brain and behavior Behav Brain Res 78 57 65
86. F Rouge-Pont V Deroche M Le Moal PV Piazza 1998 Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone Eur J Neurosci 10 3903 3907
87. M Sarter JP Bruno 2000 Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents Neuroscience 95 933 952
88. M Sarter JP Bruno 2004 Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities Neurobiol Aging 25 1127 1139
89. NCA Schrijver NI Bahr IC Weiss H Würbel 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
90. G Segovia F Mora 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 16
91. G Segovia A Porras A Del Arco F Mora 2001 Glutamatergic neurotransmission in aging: a critical perspective Mech Ageing Dev 122 1 29
92. G Segovia AG Yagüe JM García-Verdugo F Mora 2006 Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats Brain Res Bull 70 8 14
93. G Segovia A Del Arco M De Blas P Garrido F Mora 2008 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
94. G Segovia A Del Arco P Garrido M De Blas F Mora 2008 Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging Neurochem Int 52 1198 1203
95. GI Seif KM Clements PE Wainwright 2004 Effects of distraction and stress on delayed matching-to-place performance in aged rats Physiol Behav 82 477 487
96. RS Stawski MJ Sliwinski JM Smyth 2006 Stress-related cognitive interference predicts cognitive function in old age Psychol Aging 21 535 544
97. J Stemmelin C Lazarus S Cassel C Kelche J-C Cassel 2004 Immunohistochemical and neurochemical correlates of learning deficits in aged rats Neuroscience 96 275 289
98. CW Stevenson A Gratton 2003 Basolateral amygdala modulation of the nucleus accumbens dopamine response to stress: role of the medial prefrontal cortex Eur J Neurosci 17 1287 1295 (Pubitemid 36459783)
99. R Takahata B Moghaddam 1998 Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex J Neurochem 71 1443 1449
100. H Tanila T Taira TP Piepponen A Honkanen 1994 Effect of sex and age on brain monoamines and spatial learning in rats Neurobiol Aging 15 733 741
101. RD Terry R Katzman 2001 Life span and synapses: will there be a primary senile dementia? Neurobiol Aging 22 347 348
102. AM Thierry JP Tassin G Blanc J Glowinski 1976 Selective activation of mesocortical DA system by stress Nature 263 242 244
103. TM Tzschentke 2001 Pharmacology and behavioral pharmacology of the mesocortical dopamine system Prog Neurobiol 63 241 320
104. BM van Gelder MAR Tijhuis S Kalmijn S Giampaoli A Nissinen D Kromhout 2004 Physical activity in relation to cognitive decline in elderly men: the FINE study Neurology 63 2316 2321
105. H van Praag G Kempermann FH Gage 2000 Neural consequences of environmental enrichment Nat Rev Neurosci 1 191 198
106. RP Vertes 2004 Differential projections of the infralimbic and prelimbic cortex in the rat Synapse 51 32 58
107. AK Wagner X Chen AE Kline Y Li RD Zafonte CE Dixon 2005 Gender and environmental enrichment impact dopamine transporter expression after experimental traumatic brain injury Exp Neurol 195 475 483 (Pubitemid 41297798)
108. GL Wenk DJ Pierce RG Struble DL Price LC Corks 1989 Aged-related changes in the multiple neurotransmitter systems in the monkey brain Neurobiol Aging 10 11 19
109. GV Williams SA Castner 2006 Under the curve: critical issues for elucidating D1 receptor function in working memory Neuroscience 139 263 276
110. RS Wilson CF Mendes de Leon LL Barnes JA Schneider JL Bienias DA Evans DA Bennett 2002 Participation in cognitively stimulating activities and risk of incident Alzheimer disease JAMA 287 742 748
111. DA Wood JE Buse CL Wellman GV Rebec 2005 Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell Brain Res 1042 176 183
112. L Zaborszky RP Gaykema DJ Swanson WE Cullinan 1997 Cortical input to the basal forebrain Neuroscience 79 1051 1078
113. J Zhu T Green MT Bardo LP Dwoskin 2004 Environmental enrichment enhances sensitization to GBR 12935-induced activity and decreases dopamine transporter function in the medial prefrontal cortex Behav Brain Res 148 107 117 (Pubitemid 37543660)
114. J Zhu S Apparsundaram MT Bardo LP Dwoskin 2005 Environmental enrichment decreases cell surface expression of the dopamine transporter in rat medial prefrontal cortex J Neurochem 93 1434 1443
115. A Zimmermann M Stauffacher W Langhans H Wurbel 2001 Enrichment-dependent differences in novelty exploration in rats can be explained by habituation Behav Brain Res 121 11 20