Lifelong environmental enrichment in rats: Impact on emotional behavior, spatial memory vividness, and cholinergic neurons over the lifespan

Age

Volumn 35, Issue 4, 2013, Pages 1027-1043

  Harati, Hayat ^a   Barbelivien, Alexandra ^a   Herbeaux, Karine ^a   Muller, Marc Antoine ^a   Engeln, Michel ^a   Kelche, Christian ^a   Cassel, Jean Christophe ^a   Majchrzak, Monique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Acetylcholine; Aging; Anxiety; Basal forebrain; Enriched environment; Recent and remote memory; Striatum

Indexed keywords

ADULT; AGE; AGED; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CONTROLLED STUDY; EMOTION; ENVIRONMENTAL ENRICHMENT; FEMALE; FOREBRAIN; INFORMATION RETRIEVAL; LEARNING DISORDER; LIFELONG ENVIRONMENTAL ENRICHMENT; LIFESPAN; LONG EVANS RAT; LONG TERM MEMORY; MIDDLE AGED; MORRIS WATER MAZE TEST; NONHUMAN; RAT; REARING; SPATIAL LEARNING; SPATIAL MEMORY; STRESS; YOUNG ADULT; AGING; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; MAZE TEST; MEMORY; MENTAL STRESS; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SOCIAL ENVIRONMENT; PSYCHOLOGICAL ASPECT;

AGING; ANIMALS; BEHAVIOR, ANIMAL; CHOLINERGIC NEURONS; DISEASE MODELS, ANIMAL; EMOTIONS; FEMALE; MAZE LEARNING; MEMORY; NEURONAL PLASTICITY; RATS; RATS, LONG-EVANS; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL;

EID: 84891689237     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9424-8     Document Type: Article

References (74)

1. Aubert I, Rowe W, Meaney MJ, Gauthier S, Quirion R (1995) Cholinergic markers in aged cognitively impaired Long-Evans rats. Neurosci 67:277-292
2. Bakos J, Hlavacova N, Rajman M, Ondicova K, Koros C, Kitraki E, Steinbusch HWM, Jezova D (2009) Enriched environment influences hormonal status and hippocampal brain derives neurotrophic factor in a sex dependent manner. Neurosci 164:788-797
3. Barbelivien A, Herbeaux K, Oberling P, Kelche C, Galani R, Majchrzak M (2006) Environmental enrichment increases responding to contextual cues but decreases overall conditioned fear in the rat. Behav Brain Res 169:231-238
4. 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. Neuro-Report 17:1819-1823
5. Baxter MG, Gallagher M (1996) Neurobiological substrates of behavioural decline: models and data analytic strategies for individual differences in aging. Neurobiol Aging 17:491-495
6. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995) Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109:714-722
7. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH (2007) Persistence of long-Term memory storage requires a late protein synthesis-And BDNF-dependent phase in the hippocampus. Neuron 53:261-277
8. Benaroya-Milshtein N, Hollander N, Apter A, Kukulansky T, Raz N, Wilf A, Yaniv I, Pick CG (2004) Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 20:1341-1347
9. Bennett JC, McRae PA, Levy LJ, Frick KM (2006) Long-Term continuous, but not daily, environmental enrichment reduces spatial memory decline in aged male mice. Neurobiol Learn Mem 85:139-152
10. Berardi N, Braschi C, Capsoni S, Cattaneo A, Maffei L (2007) Environmental enrichment delays the onset of memory deficits and reduces neuropathological hallmarks in a mouse model of Alzheimer-like neurodegeneration. J Alzheimers Dis 11:359-370
11. Berry B, McMahan R, Gallagher M (1997) Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav Neurosci 111:267-274
12. Bessa JM, Oliveira M, Cerqueira JJ, Almeida OF, Sousa N (2005) Age-related qualitative shift in emotional behavior: paradoxical findings after re-exposure of rats in the elevated-plus maze. Behav Brain Res 162:135-142
13. Bizon JL, Gallagher M (2003) Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur J Neurosci 18:215-219
14. Bizon JL, Helm KA, Han JS, Chun HJ, Pucilowska J, Lund PK, Gallagher M (2001) Hypothalamic-pituitary-Adrenal axis function and corticosterone receptor expression in behaviorally characterized young and aged Long-Evans rats. Eur J Neurosci 14:1739-1751
15. Bizon JL, LaSarge CL, Montgomery KS, McDermott AN, Setlow B, Griffith WH (2009) Spatial reference and working memory across the lifespan of male Fisher 344 rats. Neurobiol Aging 30:645-655
16. Boguszewski P, Zagrodzka J (2002) Emotional changes related to age in rats-A behavioral analysis. Behav Brain Res 133:323-332
17. Bouet V, Freret T, Dutar P, Billard JM, Boulouard M (2011) Continuous enriched environment improves learning and memory in adult NMRI mice through theta burst-related-LTP independent mechanisms but is not efficient in advanced aged animals. Mech Ageing Dev 132:240-248
18. Briand LA, Robinson TE, Maren S (2005) Enhancement of auditory fear conditioning after housing in a complex environment is attenuated by prior treatment with amphetamine. Learn Mem 12:553-556
19. Bruel-Jungerman E, Laroche S, Rampon C (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-Term memory following environmental enrichment. Eur J Neurosci 21:513-521
20. Cano P, Cardinali DP, Spinedi E, Esquifino AI (2008) Effect of aging on 24-hour pattern of stress hormones and leptin in rats. Life Sci 83:142-148
21. Cassel J-C, Lazaris A, Birthelmer A, Jackisch R (2007) 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 28:1270-1285
22. Cizza G, Calogero AE, Brady LS, Bagdy G, Bergamini E, Blackman MR, Chrousos GP, Gold PW (1994) Male Fischer 344/N rats show a progressive central impairment of the hypothalamic-pituitary-Adrenal axis with advancing age. Endocrinol 134:1611-1620
23. Colombo PJ, Gallagher M (1998) Individual differences in spatial memory and striatal ChAT activity among young and aged rats. Neurobiol Learn Mem 70:314-327
24. De Lacalle S, Cooper JD, Svendsen CN, Dunnett SB, Sofroniew MV (1996) Reduced retrograde labelling with fluorescent tracer accompanies neuronal atrophy of basal forebrain cholinergic neurons in aged rats. Neurosci 75:19-27
25. Depp C, Vahia IV, Jeste D (2010) Successful aging: focus on cognitive and emotional health. Annu Rev Clin Psycho 6:527-550
26. Devan BD, Goad EH, Petri HL (1996) Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze. Neurobio Learn Mem 66:305-323
27. Duffy SN, Craddock KJ, Abel T, Nguyen PV (2001) Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus- dependent memory. Learn Mem 8:26-34
28. Fernandez CI, Collazo J, Bauza Y, Castellanos MR, Lopez O (2004) Environmental enrichment-behavior-oxidative stress interactions in the aged rat: issues for a therapeutic approach in human aging. Ann NY Acad Sc 1019:53-57
29. Fluttert M, Dalm S, Oitzl MS (2000) A refined method for sequential blood sampling by tail incision in rats. Lab Anim 34:372-378
30. Freret T, Billard JM, Schumann-Bard P, Dutar P, Dauphin F, Boulouard M, Bouet V (2011) Rescue of cognitive aging by long-lasting environmental enrichment exposure initiated before median lifespan. Neurobio Aging doi.org/ 10.1016/j.neurobiolaging.2011.09.028
31. Frick KM, Fernandez SM (2003) Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol Aging 24:615-626
32. Galani R, Berthel MC, Lazarus C, Majchrzak M, Barbelivien A, Kelche C, Cassel J-C (2007) The behavioral effects of enriched housing are not altered by serotonin depletion but enrichment alters hippocampal neurochemistry. Neurobiol Learn Mem 88:1-10
33. Harati H, Barbelivien A, Cosquer B, Majchrzak M, Cassel J-C (2008) 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. Neurosci 153:72-83
34. Harati H, Majchrzak M, Cosquer B, Galani R, Kelche C, Cassel J-C, Barbelivien A (2011) Attention and memory in aged rats: impact of lifelong environmental enrichment. Neurobiol Aging 32:718-736
35. Harburger LL, Lambert TJ, Frick KM (2007) Age-dependent effects of environmental enrichment on spatial reference memory in male mice. Behav Brain Res 185:43-48
36. Herzog CD, Nowak KA, Sater M, Bruno JP (2003) Microdialysis without acetylcholinesterase inhibition reveals an agerelated attenuation in stimulated cortical acetylcholine release. Neurobiol Aging 24:861-863
37. Houston FP, Stevenson GD, McNaughton BL, Barnes CA (1999) Effects of age on the generalization and incubation of memory in the F344 rat. Learn Mem 6:111-119
38. Howell DC (1998) Méthodes statistiques en sciences humaines. De Boeck Université, Paris
39. Kobayashi S, Ohashi Y, Ando S (2002) 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 70:340-346
40. Leal-Galicia P, Saldivar-Gonzalez A, Morimoto S, Arias C (2007) Exposure to environmental enrichment elicits differential hippocampal cell proliferation: role of individual responsiveness to anxiety. Dev Neurobiol 67:395-405
41. Leal-Galicia P, Castaneda-Bueno M, Quiroz-Baez R, Arias C (2008) Long-Term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol Learn Mem 90:511-518
42. LeFevre J, McClintock MK (1988) Reproductive senescence in female rats: a longitudinal study of individual differences in estrous cycles and behaviour. Biol Reprod 38:780-789
43. Leger M, Bouet V, Freret T, Darmaillacq AS, Dacher M, Dauphin F, Boulouard M, Schumann-Bard (2012) Environmental enrichment improves recent but not remote memory in association with a modified brain metabolic activation profile in adult mice. Behav Brain Res 228:22-29
44. Lindner MD (1997) Reliability, distribution, and validity of agerelated cognitive deficits in the Morris water maze. Neurobiol Learn Mem 68:203-220
45. Lopez J, de Vasconcelos AP, Cassel J-C (2008) Environmental cue saliency influences the vividness of a remote spatial memory in rats. Neurobiol Learn Mem 90:285-289
46. Marchand AR, Luck D, DiScala G (2003) Evaluation of an improved automated analysis of freezing behaviour in rats and its use in trace fear conditioning. J Neurosci Methods 126:145-153
47. Markowska AL (1999) Sex dimorphisms in the rate of agerelated decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 19:8122-8133
48. Miyoshi E,Wietzikovski EC, BortolanzaM, Boschen SL, Canteras NS, Izquierdo I, Da Cunha C (2012) Behav Brain Res 226:171-178
49. Moncek F, Duncko R, Johansson BB, Jezova D (2004) Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423-431
50. Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2006) Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging 27:645-654
51. Muir JL, Fischer W, Bjorklund A (1999) Decline in visual attention and spatial memory in aged rats. Neurobiol Aging 20:605-615
52. Nieves-Martinez E, Haynes K, Childers SR, SonntagWE, Nicolle MM (2012) Muscarinic receptor/G-protein coupling is reduced in the dorsomedial striatum of cognitively impaired aged rats. Behav Brain Res 227:258-264
53. O'Callaghan RM, Griffin EW, Kelly AM (2009) Long-Term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 19:1019-1029
54. Oler JA, Markus EJ (1998) Age-related deficits on the radial maze and in fear conditioning: hippocampal processing and consolidation. Hippocampus 8:402-415
55. Parent MB, Baxter MG (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem 11:9-20
56. PenaY, Prunell M, DimitsantosV,Nadal R, EscorihuelaRM(2006) Environmental enrichment effects in social investigation in rats are gender dependent. Behav Brain Res 174:181-187
57. Pham TM, Winblad B, Granholm AC, Mohammed AH (2002) Environmental influences on brain neurotrophins in rats. Pharmacol Biochem Behav 73:167-175
58. Pisarska M, Mulchahey JJ,Welge JA, Geracioti TD Jr, Kasckow JW (2000) Age-related alterations in emotional behaviors and amygdalar corticotropin-releasing factor (CRF) and CRF-binding protein expression in aged Fischer 344 rats. Brain Res 877:184-190
59. Rodgers RJ, Dalvi A (1997) Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 21:801-810
60. Schrijver NC, Bahr NI, Weiss IC, Wurbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Behav 71:129-139
61. Sekeres MJ, Neve RL, Frankland PW, Josselyn SA (2010) Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. Learn Mem 17:280-283
62. Shank JC (2001) Do Norway rats (Rattus norvegicus) synchronize their estrous cycle? Physiol Biochem Behav 73:209-224
63. Shirakawa K, Ichitani Y (2004) Prolonged initiation latency in Morris water maze learning in rats with ibotenic acid lesions to medial striatum: effects of systemic and intranigral muscimol administration. Brain Res 1030:193-200
64. Stackman RW, Blasberg ME, Langan CJ, Clark AS (1997) Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiol Learn Mem 67:167-171
65. Stemmelin J, Lazarus C, Cassel S, Kelche C, Cassel J-C (2000) Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neurosci 96:275-289
66. Sugaya K, Greene R, Personett D, Robbins M, Kent C, Bryan D, Skiba E, Gallagher M, McKinney M (1998) Septo-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline. Neurobiol Aging 19:351-361
67. Suzuki A, Fukushima H, Mukawa T, Toyoda H, Wu L-C, Zhao M-G, Xu H, Shang Y, Endoh K, Iwamoto T, Mamiya N, Okano E, Hasegawa S, Mercaldo V, Zhang Y, Maeda R, Ohta M, Josselyn SA, Zhuo M, Kida S (2011) Upregulation of CREB-mediated transcription enhances both shortand long-Term memory. J Neurosci 31:8786-8802
68. Tang YP, Wang H, Feng R, Kyin M, Tsien JZ (2001) Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacol 41:779-790
69. Torras-Garcia M, Costa-Miserachs D, Coll-Andreu M, Portell-Cortes I (2005) Decreased anxiety levels related to aging. Exp Brain Res 164:177-184
70. Traissard N, Herbeaux K, Cosquer B, Jeltsch H, Ferry B, Galani R, Pernon A, Majchrzak M, Cassel JC (2007) Combined damage to entorhinal cortex and cholinergic basal forebrain neurons, two early neurodegenerative features accompanying Alzheimer's disease: effects on locomotor activity and memory functions in rats. Neuropsychopharmacol 32:851-871
71. Ward MT, Oler JA, Markus EJ (1999) Hippocampal dysfunction during aging I: deficits in memory consolidation. Neurobiol Aging 20:363-372
72. Williams BM, Luo Y, Ward C, Redd K, Gibson R, Kuczaj SA, McCoy JG (2001) Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav 73:649-6
73. Workel JO, Oitzl MS, Fluttert M, Lesscher H, Karssen A, de Kloet ER (2001) Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-Adrenal axis of brown Norway rats from youth to senescence. J Neuroendocrinol 13:569-580
74. Wyss JM, Chambless BD, Kadish I, van Groen T (2000) Agerelated decline in water maze learning and memory in rats: strain differences. Neurobiol Aging 21:671-681