Attention and memory in aged rats: Impact of lifelong environmental enrichment

Neurobiology of Aging

Volumn 32, Issue 4, 2011, Pages 718-736

  Harati, Hayat ^a   Majchrzak, Monique ^a   Cosquer, Brigitte ^a   Galani, Rodrigue ^a   Kelche, Christian ^a   Cassel, Jean Christophe ^a   Barbelivien, Alexandra ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Aging; Enrichment; Five choice serial reaction time task; Medial septum; Memory; Nucleus basalis magnocellularis; Sustained attention; Water maze

Indexed keywords

CHOLINE ACETYLTRANSFERASE; NEUROTROPHIN RECEPTOR P75;

AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION DISTURBANCE; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FEMALE; FOREBRAIN; MAZE TEST; MEMORY DISORDER; MENTAL PERFORMANCE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; RESPONSE TIME; SPATIAL MEMORY; SURVIVAL RATE;

AGING; ANALYSIS OF VARIANCE; ANIMALS; ATTENTION; BODY WEIGHT; BRAIN; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; ENVIRONMENT; FEMALE; HOUSING, ANIMAL; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MEMORY; MOTOR ACTIVITY; NEURONS; PARVALBUMINS; RATS; RATS, LONG-EVANS; REACTION TIME; RECEPTOR, NERVE GROWTH FACTOR; REGRESSION ANALYSIS;

EID: 79953034287     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2009.03.012     Document Type: Article

References (75)

1. Augustsson H., Lindberg L., Hoglund A.U., Dahlborn K. Human-animal interactions and animal welfare in conventionally and pen-housed rats. Lab. Anim. 2002, 36(3):271-281.
2. Backman C., Rose G.M., Hoffer B.J., Henry M.A., Bartus R.T., Friden P., Granholm A.C. Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J. Neurosci. 1996, 16(17):5437-5442.
3. Barbelivien A., Ruotsalainen S., Sirvio J. Metabolic alterations in the prefrontal and cingulate cortices are related to behavioral deficits in a rodent model of attention-deficit hyperactivity disorder. Cereb. Cortex 2001, 11(11):1056-1063.
4. Barbelivien A., Herbeaux K., Oberling P., Kelche C., Galani R., Majchrzak M. Environmental enrichment increases responding to contextual cues but decreases overall conditioned fear in the rat. Behav. Brain Res. 2006, 169(2):231-238.
5. Barense M.D., Fox M.T., Baxter M.G. Aged rats are impaired on an attentional set-shifting task sensitive to medial frontal cortex damage in young rats. Learn. Mem. 2002, 9(4):191-201.
6. Bari A., Dalley J.W., Robbins T.W. The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat. Protoc. 2008, 3(5):759-767.
7. Baskerville K.A., Kent C., Nicolle M.M., Gallagher M., McKinney M. Aging causes partial loss of basal forebrain but no loss of pontine reticular cholinergic neurons. Neuroreport 2006, 17(17):1819-1823.
8. Benaroya-Milshtein N., Hollander N., Apter A., Kukulansky T., Raz N., Wilf A., Yaniv I., Pick C.G. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur. J. Neurosci. 2004, 20(5):1341-1347.
9. Bennett J.C., McRae P.A., Levy L.J., Frick K.M. Long-term continuous, but not daily, environmental enrichment reduces spatial memory decline in aged male mice. Neurobiol. Learn. Mem. 2006, 85(2):139-152.
10. Berry B., McMahan R., Gallagher M. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav. Neurosci. 1997, 111(2):267-274.
11. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci. 2005, 21(2):513-521.
12. Casadesus G., Shukitt-Hale B., Joseph J.A. Automated measurement of age-related changes in the locomotor response to environmental novelty and home-cage activity. Mech. Ageing Dev. 2001, 122(15):1887-1897.
13. Cassel J.C., Schweizer T., Lazaris A., Knorle R., Birthelmer A., Godtel-Armbrust U., Forstermann U., Jackisch R. Cognitive deficits in aged rats correlate with levels of l-arginine, not with nNOS expression or 3,4-DAP-evoked transmitter release in the frontoparietal cortex. Eur. Neuropsychopharmacol. 2005, 15(2):163-175.
14. Cassel J.C., Lazaris A., Birthelmer A., Jackisch R. Spatial reference- (not working- or procedural-) memory performance of aged rats in the water maze predicts the magnitude of sulpiride-induced facilitation of acetylcholine release by striatal slices. Neurobiol. Aging 2007, 28(8):1270-1285.
15. Christie M.A., Dalrymple-Alford J.C. Behavioral consequences of frontal cortex grafts and enriched environments after sensorimotor cortex lesions. J. Neural Transplant. Plast. 1995, 5(4):199-210.
16. Cooper J.D., Lindholm D., Sofroniew M.V. Reduced transport of [125I]nerve growth factor by cholinergic neurons and down-regulated TrkA expression in the medial septum of aged rats. Neuroscience 1994, 62(3):625-629.
17. Daniel J.M., Roberts S.L., Dohanich G.P. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiol. Behav. 1999, 66:11-20.
18. Devan B.D., Goad E.H., Petri H.L. Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze. Neurobiol. Learn. Mem. 1996, 66(3):305-323.
19. Duffy S.N., Craddock K.J., Abel T., Nguyen P.V. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn. Mem. 2001, 8(1):26-34.
20. Elliott B.M., Grunberg N.E. Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats. Behav. Brain Res. 2005, 165(2):187-196.
21. Fernandez C.I., Collazo J., Bauza Y., Castellanos M.R., Lopez O. Environmental enrichment-behavior-oxidative stress interactions in the aged rat: issues for a therapeutic approach in human aging. Ann. N.Y. Acad. Sci. 2004, 1019:53-57.
22. Fordyce D.E., Farrar R.P. Effect of physical activity on hippocampal high affinity choline uptake and muscarinic binding: a comparison between young and old F344 rats. Brain Res. 1991, 541(1):57-62.
23. Frick K.M., Fernandez S.M. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol. Aging 2003, 24(4):615-626.
24. Galani R., Berthel M.-C., Lazarus C., Majchrzak M., Barbelivien A., Kelche C., Cassel J.-C. The behavioral effects of enriched housing are not altered by serotonin depletion but enrichment alters hippocampal neurochemistry. Neurobiol. Learn. Mem. 2007, 88(1):1-10.
25. Galani R., Duconseille E., Bildstein O., Cassel J.C. Effects of room and cage familiarity on locomotor activity measures in rats. Physiol. Behav. 2001, 74(1-2):1-4.
26. Gallagher M., Burwell R.D. Relationship of age-related decline across several behavioral domains. Neurobiol. Aging 1989, 10(6):691-708.
27. Gallagher M., Burwell R., Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci. 1993, 107(4):618-626.
28. Gresack J.E., Frick K.M. Environmental enrichment reduces the mnemonic and neural benefits of estrogen. Neuroscience 2004, 128(3):459-471.
29. Gresack J.E., Kerr K.M., Frick K.M. Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice. Neurobiol. Learn. Mem. 2007, 88(4):393-408.
30. Grottick A.J., Higgins G.A. Assessing a vigilance decrement in aged rats: effects of pre-feeding, task manipulation, and psychostimulants. Psychopharmacology (Berl.) 2002, 164(1):33-41.
31. Grottick A.J., Haman M., Wyler R., Higgins G.A. Reversal of a vigilance decrement in the aged rat by subtype-selective nicotinic ligands. Neuropsychopharmacology 2003, 28(5):880-887.
32. Harati H., Barbelivien A., Cosquer B., Majchrzak M., Cassel J.C. Selective cholinergic lesions in the rat nucleus basalis magnocellularis with limited damage in the medial septum specifically alter attention performance in the five-choice serial reaction time task. Neuroscience 2008, 153(1):72-83.
33. Harburger L.L., Lambert T.J., Frick K.M. Age-dependent effects of environmental enrichment on spatial reference memory in male mice. Behav. Brain Res. 2007, 185(1):43-48.
34. Herrero A.I., Sandi C., Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol. Learn. Mem. 2006, 86(2):150-159.
35. Howell D. Statistical Methods for Psychology 1997, Duxburry Press, Belmont.
36. Ingram D.K., Joseph J.A., Spangler E.L., Roberts D., Hengemihle J., Fanelli R.J. Chronic nimodipine treatment in aged rats: analysis of motor and cognitive effects and muscarinic-induced striatal dopamine release. Neurobiol. Aging 1994, 15(1):55-61.
37. Jones D.N., Barnes J.C., Kirkby D.L., Higgins G.A. Age-associated impairments in a test of attention: evidence for involvement of cholinergic systems. J. Neurosci. 1995, 15(11):7282-7292.
38. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 1998, 18(9):3206-3212.
39. Kobayashi S., Ohashi Y., Ando S. Effects of enriched environments with different durations and starting times on learning capacity during aging in rats assessed by a refined procedure of the Hebb-Williams maze task. J. Neurosci. Res. 2002, 70(3):340-346.
40. LeFevre J., McClintock M.K. Reproductive senescence in female rats: a longitudinal study of individual differences in estrous cycles and behavior. Biol. Reprod. 1988, 38(4):780-789.
41. Leggio M.G., Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 2005, 163(1):78-90.
42. Lehmann O., Grottick A.J., Cassel J.C., Higgins G.A. A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region. Eur. J. Neurosci. 2003, 18(3):651-666.
43. Lindner M.D. Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol. Learn. Mem. 1997, 68(3):203-220.
44. McGaughy J., Sarter M. Behavioral vigilance in rats: task validation and effect of age, amphetamine, and benzodiazepine receptor ligands. Psychopharmacology 1995, 117:340-357.
45. McGaughy J., Kaiser T., Sarter M. Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav. Neurosci. 1996, 110(2):247-265.
46. McGaughy J., Dalley J.W., Morrison C.H., Everitt B.J., Robbins T.W. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J. Neurosci. 2002, 22(5):1905-1913.
47. Means L.W., Holsten R.D. Individual aged rats are impaired on repeated reversal due to loss of different behavioral patterns. Physiol. Behav. 1992, 52(5):959-963.
48. Mohammed A.H., Zhu S.W., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M.C., Eriksson P.S., Bogdanovic N. Environmental enrichment and the brain. Prog. Brain Res. 2002, 138:109-133.
49. Mora F., Segovia G., Del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res. Rev. 2007, 55(1):78-88.
50. Muir J.L., Fischer W., Bjorklund A. Decline in visual attention and spatial memory in aged rats. Neurobiol. Aging 1999, 20(6):605-615.
51. Mura A., Feldon J. Spatial learning in rats is impaired after degeneration of the nigrostriatal dopaminergic system. Mov. Disord. 2003, 18(8):860-871.
52. Nilsson M., Perfilieva E., Johansson U., Orwar O., Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 1999, 39(4):569-578.
53. Park G.A., Pappas B.A., Murtha S.M., Ally A. Enriched environment primes forebrain choline acetyltransferase activity to respond to learning experience. Neurosci. Lett. 1992, 143(1-2):259-262.
54. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 2000, 3(3):238-244.
55. Robbins T.W. The 5-choice serial reaction time task: behavioral pharmacology and functional neurochemistry. Psychopharmacology (Berl.) 2002, 163(3-4):362-380.
56. Sarter M., Turchi J. Age-and dementia-associated impairments in divided attention: psychological constructs, animal models, and underlying neuronal mechanisms. Dement. Geriatr. Cogn. Disord. 2002, 13(1):46-58.
57. Schank J.C. Do Norway rats (Rattus norvegicus) synchronize their estrous cycle?. Physiol. Behav. 2001, 71:129-139.
58. Schoenbaum G., Nugent S., Saddoris M.P., Gallagher M. Teaching old rats new tricks: age-related impairments in olfactory reversal learning. Neurobiol. Aging 2002, 23(4):555-564.
59. Schrijver N.C., Bahr N.I., Weiss I.C., Wurbel H. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol. Biochem. Behav. 2002, 73(1):209-224.
60. Schulz D., Topic B., Souza Silva M.A., Huston J.P. Extinction-induced immobility in the water maze and its neurochemical concomitants in aged and adult rats: a possible model for depression?. Neurobiol. Learn. Mem. 2004, 82(2):128-141.
61. Schulz D., Kouri C., Huston J.P. Behavior on the water maze platform: relationship to learning and open field exploration in aged and adult rats. Brain Res. Bull. 2007, 74(4):206-215.
62. Segovia G., Del Arco A., Garrido P., de Blas M., Mora F. Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging. Neurochem. Int. 2008, 52(6):1198-1203.
63. Skalicky M., Bubna-Littitz H., Viidik A. Influence of physical exercise on aging rats. I. Life-long exercise preserves patterns of spontaneous activity. Mech. Ageing Dev. 1996, 87(2):127-139.
64. Spangenberg E.M., Augustsson H., Dahlborn K., Essen-Gustavsson B., Cvek K. Housing-related activity in rats: effects on body weight, urinary corticosterone levels, muscle properties and performance. Lab. Anim. 2005, 39(1):45-57.
65. Stackman R.W., Blasberg M.E., Langan C.J., Clark A.S. Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiol. Learn. Mem. 1997, 67(2):167-171.
66. Stemmelin J., Cassel J.C., Will B., Kelche C. Sensitivity to cholinergic drug treatments of aged rats with variable degrees of spatial memory impairment. Behav. Brain Res. 1999, 98(1):53-66.
67. Stemmelin J., Lazarus C., Cassel S., Kelche C., Cassel J.C. Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 2000, 96(2):275-289.
68. Tang Y.P., Wang H., Feng R., Kyin M., Tsien J.Z. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 2001, 41(6):779-790.
69. Topic B., Dere E., Schulz D., Souza Silva M.A., Jocham G., Kart E., Huston J.P. Aged and adult rats compared in acquisition and extinction of escape from the water maze: focus on individual differences. Behav. Neurosci. 2005, 119(1):127-144.
70. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 2000, 1(3):191-198.
71. Van Waas M., Soffie M. Differential environmental modulations on locomotor activity, exploration and spatial behavior in young and old rats. Physiol. Behav. 1996, 59(2):265-271.
72. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 1997, 111(2):259-266.
73. Williams B.M., Luo Y., Ward C., Redd K., Gibson R., Kuczaj S.A., McCoy J.G. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol. Behav. 2001, 73(4):649-658.
74. Woodcock E.A., Richardson R. Effects of environmental enrichment on rate of contextual processing and discriminative ability in adult rats. Neurobiol. Learn. Mem. 2000, 73(1):1-10.
75. Zimmermann A., Stauffacher M., Langhans W., Wurbel H. Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav. Brain Res. 2001, 121(1-2):11-20.