Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging

Neurochemistry International

Volumn 52, Issue 6, 2008, Pages 1198-1203

  Segovia, Gregorio ^a   Del Arco, Alberto ^a   Garrido, Pedro ^a   de Blas, Marta ^a   Mora, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Acetylcholine; Aging; Environmental enrichment; Prefrontal cortex; Stress

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANNULA; CHOLINERGIC SYSTEM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL STRESS; MALE; MICRODIALYSIS; MOTOR ACTIVITY; NONHUMAN; OPEN FIELD TEST; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STEREOTAXIC SURGERY; STRESS;

ACETYLCHOLINE; AGING; ANIMALS; BASAL NUCLEUS OF MEYNERT; CHOLINERGIC FIBERS; ENVIRONMENT; ENVIRONMENT DESIGN; EXPLORATORY BEHAVIOR; EXTRACELLULAR FLUID; MALE; MICRODIALYSIS; MOTOR ACTIVITY; NEURAL PATHWAYS; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 40949128694     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2007.12.007     Document Type: Article

References (59)

1. Acquas E., Wilson C., and Fibiger H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J. Neurosci. 16 (1996) 3089-3096
2. Bardo M.T., Bowling S.L., Rowlett J.K., Manderscheid P., Buxton S.T., and Dwoskin L.P. Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol. Biochem. Behav. 51 (1995) 397-405
3. Baskerville K.A., Kent C., Nicolle M.M., Gallagher M., and McKinney M. Aging causes partial loss of basal forebrain but no loss of pontine reticular cholinergic neurons. NeuroReport 17 (2006) 1819-1823
4. Belz E.E., Kennell J.S., Czambell R.K., Rubin R.T., and Rhodes M.E. Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacol. Biochem. Behav. 76 (2003) 481-486
5. Biegon A., Duvdevani R., Greenberger V., and Segal M. Aging and brain cholinergic muscarinic receptors: an autoradiographic study in the rat. J. Neurochem. 51 (1988) 1381-1385
6. Bizon J.L., Helm K.A., Han J.S., Chun H.J., Pucilowska J., Lund P.K., and Gallagher M. Hypothalamic-pituitary-adrenal axis function and corticosterone receptor expression in behaviourally characterized young and aged Long-Evans rats. Eur. J. Neurosci. 14 (2001) 1739-1751
7. Bland S.T., Hargrave D., Pepin J.L., Amat J., Watkins L.R., and Maier S.F. Stressor controllability modulates stress-induced dopamine and serotonin efflux and morphine-induced serotonin efflux in the medial prefrontal cortex. Neuropsychopharmacology 28 (2003) 1589-1596
8. Cobo M., Expósito I., and Mora F. Aging, prefrontal cortex, and amino acid neurotransmitters: differential effects produced by electrical stimulation. Neurobiol. Aging 14 (1993) 187-190
9. Cobo M., Expósito I., Porras A., and Mora F. Release of amino acid neurotransmitters in different cortical areas of conscious adult and aged rats. Neurobiol. Aging 13 (1992) 705-709
10. Crawford C.A., and Levine M.S. Dopaminergic function in the neostriatum and nucleus accumbens of young and aged Fisher 344 rats. Neurobiol. Aging 18 (1997) 57-66
11. Day J., Damsma G., and Fibiger H.C. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol. Biochem. Behav. 38 (1991) 723-729
12. Dazzi L., Vacca G., Ladu S., Pisu M.Ga., Serra M., and Biggio G. Long-term treatment with anitdepressant drugs reduces the sensitivity of cortical cholinergic neurons to the activating actions of stress and the anxiogenic drug FG 7142. Neuropharmacology 41 (2001) 229-237
13. Decker M.W. The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res. Rev. 12 (1987) 423-438
14. Del Arco A., and Mora F. Dopamine release in the prefrontal cortex during stress is reduced by the local activation of glutamate receptors. Brain Res. Bull. 56 (2001) 125-130
15. Del Arco A., Segovia G., Canales J.J., Garrido P., De Blas M., García-Verdugo J.M., and Mora F. Environmental enrichment reduces the function of D1dopamine receptors in the prefrontal cortex of the rat. J. Neural Transm. 114 (2007) 43-48
16. Del Arco A., Segovia G., Garrido P., De Blas M., and Mora F. Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav. Brain Res. 176 (2007) 267-273
17. Del Arco A., Segovia G., and Mora F. Dopamine release during stress in the prefrontal cortex of the rat decreases with age. NeuroReport 12 (2001) 4019-4022
18. Emerich D.F., McDermott P., Krueger P., Banks M., Zhao J., Marszalkowski J., Frydel B., Winn S.R., and Sanberg P.R. Locomotion of aged rats: relationship to neurochemical but not morphological changes in nigrostriatal dopaminergic neurons. Brain Res. Bull. 32 (1993) 477-486
19. Fernández C.I., Collazo J., Bauza Y., Castellanos M.R., and López A. Environmental enrichment-behavior-oxidative stress interactions in the aged rat. Ann. N. Y. Acad. Sci. 1019 (2004) 53-57
20. Fischer W., Wictorin K., Bjorklund A., Williams L.R., Varon S., and Gage F.H. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329 (1987) 65-68
21. Fuster J.M. The Prefrontal Cortex. Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (1997), Lippincott-Raven, New York
22. Giovannini M.G., Rakovska A., Benton R.S., Pazzagli M., Bianchi L., and Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106 (2001) 43-53
23. Green A., Cain E., Michael T., and Bardo M.T. Environmental enrichment decreases nicotine-induced hyperactivity in rats. Psychopharmacology 170 (2003) 235-241
24. Hebert M.A., and Gerhardt G.A. Normal and drug-induced locomotor behavior in aging: comparison to evoked DA release and tissue content in Fischer 344 rats. Brain Res. 797 (1998) 42-54
25. Huang R.-L., Wang C.-T., Tai M.-Y., Tsai Y.-F., and Peng M.-T. Effects of age on dopamine release in the nucleus accumbens and amphetamine-induced locomotor activity in rats. Neurosci. Lett. 200 (1995) 61-64
26. Laplante F., Stevenson C.W., Gratton A., Srivastava L.K., and Quirion R. Effects of neonatal ventral hippocampal lesion in rats on stress-induced acetylcholine release in the prefrontal cortex. J. Neurochem. 91 (2004) 1473-1482
27. Larsson F., Winblad B., and Mohammed A.H. Psychological stress and environmental adaptation in enriched vs. impoverished housed rats. Pharmacol. Biochem. Behav. 73 (2002) 193-207
28. Luine V., and Hearns M. Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res. 523 (1990) 321-324
29. Mark G.P., Rada P.V., and Shors T.J. Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 74 (1996) 767-774
30. Mirmiran M., Van Gool W.A., Van Haaren F., and Polak C.E. Environmental influences on brain and behavior in aging and Alzheimer's disease. In: Swaab D.F., Fliers E., Mirmiran M., Van Gool W.A., and Van Haaren F. (Eds). Aging of the Brain and Alzheimer's Disease. Progress in Brain Research vol. 70 (1986), Elsevier, Amsterdam 443-459
31. Mitsushima D., Mizuno T., and Kimura F. Age-related changes in diurnal acetylcholine release in the prefrontal cortex of male rats as measured by microdialysis. Neuroscience 72 (1996) 429-434
32. Mohammed A.H., Zhu S.W., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M.C., Eriksson P.S., and Bogdanovic N. Environmental Enrichment and the Brain. Progress in Brain Research (2002), Elsevier pp. 109-133
33. Moncek F., Duncko R., Johansson B.B., and Jezova D. Effect of environmental enrichment on stress related systems in rats. J. Neuroendocrinol. 16 (2004) 423-431
34. Morano M.I., Vazquez D.M., and Akil H. The role of the hippocampal mineralocorticoid and glucocorticoid receptors in the hypothalamo-pituitary-adrenal axis of the aged Fisher rat. Mol. Cell. Neurosci. 5 (1994) 400-412
35. Nyakas C., Buwalda B., Luiten P.G.M., and Bohus B. Effect of low amphetamine doses on cardiac responses to emotional stress in aged rats. Neurobiol. Aging 13 (1992) 123-129
36. Park G.A.S., Pappas B.A., Murtha S.M., and Ally A. Enriched environment primes forebrain choline acetyltransferase activity to respond to learning experience. Neurosci. Lett. 143 (1992) 259-262
37. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, New York
38. Pedersen W.A., Wan R., and Mattson M.P. Impact of aging on stress-responsive neuroendocrine systems. Mech. Ageing Dev. 122 (2001) 963-983
39. Porras A., Sanz B., and Mora F. Dopamine-glutamate interactions in the prefrontal cortex of the conscious rat: studies on ageing. Mech. Ageing Dev. 99 (1997) 9-17
40. Robbins T.W. Arousal systems and attentional processes. Biol. Psychiatry 45 (1997) 57-71
41. Robbins T.W. Controlling stress: how the brain protects itself from depression. Nat. Neurosci. 8 (2005) 261-262
42. Rosenzweig M.R., and Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 78 (1996) 57-65
43. Sapolsky R.M., Krey L.C., and McEwen B.S. The adreno cortical stress-response in the aged male rat: impairment of recovery from stress. Exp. Gerontol. 18 (1983) 55-64
44. Sapolsky R.M., Krey L.C., and McEwen B.S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 7 (1986) 284-301
45. Sarter M., and Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95 (2000) 933-952
46. Sarter M., and Bruno J.P. Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol. Aging 25 (2004) 1127-1139
47. Schrijver N.C.A., Bahr N.I., Weiss I.C., and Würbel H. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol. Biochem. Behav. 73 (2002) 209-224
48. Seeman T.E., and Robbins R.J. Aging and hypothalamic-pituitary-adrenal response to challenge in humans. Endocr. Rev. 15 (2007) 233-260
49. Segovia G., Del Arco A., De Blas M., Garrido P., and Mora F. 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. (2007) 10.1016/j.bbr.2007.09.024
50. Segovia G., and Mora F. 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 (2005) 11-16
51. Segovia G., and Mora F. Dopamine and GABA increases produced by activation of glutamate receptors in the nucleus accumbens are decreased during aging. Neurobiol. Aging 26 (2005) 91-101
52. Segovia G., Porras A., Del Arco A., and Mora F. Glutamatergic neurotransmission in aging: a critical perspective. Mech. Ageing Dev. 122 (2001) 1-29
53. Segovia G., Porras A., and Mora F. Effects of 4-aminopyridine on extracellular concentrations of glutamate in striatum of the freely moving rat. Neurochem. Res. 22 (1997) 1491-1497
54. Segovia G., Yagüe A.G., García-Verdugo J.M., and Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res. Bull. 70 (2006) 8-14
55. Snedecor W.G., and Cochran G.W. Statistical Methods (1989), Iowa State Press, Ames, IA
56. Stemmelin J., Lazarus C., Cassel S., Kelche C., and Cassel J.-C. Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 96 (2004) 275-289
57. van Eekelen J.A.M., Rots N.Y., Sutanto W., and de Kloet E.R. The effect of aging on stress responsiveness and central corticosteroid receptors in the Brown Norway rat. Neurobiol. Aging 13 (1992) 159-170
58. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1 (2000) 191-198
59. Zimmermann A., Stauffacher M., Langhans W., and Wurbel H. Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav. Brain Res. 121 (2001) 11-20