Rescue of cognitive aging by long-lasting environmental enrichment exposure initiated before median lifespan

Neurobiology of Aging

Volumn 33, Issue 5, 2012, Pages 1005.e1-

  Freret, T ^a   Billard, J M ^b   Schumann Bard, P ^a   Dutar, P ^b   Dauphin, F ^a   Boulouard, M ^a   Bouet, V ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

Author keywords

Cognitive reserve; Hippocampus; Learning; Lifespan; Memory; NMDA receptor; Synaptic plasticity; Theta burst induced long term potentiation

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; COGNITION; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; LIFE EXTENSION; LIFESPAN; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; MOUSE; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC POTENTIAL; ANIMAL; HIPPOCAMPUS; LONGEVITY; MICROCLIMATE; MOUSE STRAIN; NERVE CELL PLASTICITY; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SYNAPSE;

AGING; ANIMALS; ANXIETY; COGNITION; ENVIRONMENT, CONTROLLED; ENVIRONMENTAL EXPOSURE; FEMALE; HIPPOCAMPUS; LONGEVITY; MEMORY DISORDERS; MICE; MICE, INBRED STRAINS; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; SYNAPSES;

EID: 85058205902     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.09.028     Document Type: Article

References (62)

1. Anderson W.W., Collingridge G.L. The LTP Program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. Neurosci. Methods 2001, 108:71-83.
2. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., Kandel E.R. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5280-5285.
3. Barnes C.A., Rao G., Shen J. Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol. Aging 1997, 18:445-452.
4. Beattie E.C., Carroll R.C., Yu X., Morishita W., Yasuda H., von Zastrow M., Malenka R.C. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. J. Nat. Neurosci 2000, 3:1291-1300.
5. Belzung C., Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res 2001, 125:141-149.
6. 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, 20:1341-1347.
7. 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, 85:139-152.
8. Boissier J.R., Simon P. Action of caffeine on the spontaneous motility of the mouse. Arch. Int. Pharmacodyn. Ther 1965, 158:212-221.
9. Bouet V., Freret T., Dutar P., Billard J.M., Boulouard M. 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 2011, 132:240-248.
10. 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, 21:513-521.
11. Chapillon P., Manneché C., Belzung C., Caston J. Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav. Genet 1999, 29:41-46.
12. Chourbaji S., Hellweg R., Brandis D., Zörner B., Zacher C., Lang U.E., Henn F.A., Hörtnagl H., Gass P. Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res. Mol. Brain Res 2004, 121:28-36.
13. Clayton D.A., Grosshans D.R., Browning M.D. Aging and surface expression of hippocampal NMDA receptors. J. Biol. Chem 2002, 277:14367-14369.
14. Connor J.R., Wang E.C., Diamond M.C. Increased length of terminal dendritic segments in old adult rats' somatosensory cortex: an environmentally induced response. Exp. Neurol 1982, 78:466-470.
15. Diamond M.C., Ingham C.A., Johnson R.E., Bennett E.L., Rosenzweig M.R. Effects of environment on morphology of rat cerebral cortex and hippocampus. J. Neurobiol 1976, 7:75-85.
16. 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, 8:26-34.
17. Eichenbaum H. Learning from LTP: a comment on recent attempts to identify cellular and molecular mechanisms of memory. Learn. Mem 1996, 3:61-73.
18. Faherty C.J., Kerley D., Smeyne R.J. A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res. Dev. Brain Res 2003, 141:55-61.
19. Foster T.C. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res. Brain Res. Rev 1999, 30:236-249.
20. Foster T.C., Dumas T.C. Mechanism for increased hippocampal synaptic strength following differential experience. J. Neurophysiol 2001, 85:1377-1383.
21. Foster T.C., Kumar A. Calcium dysregulation in the aging brain. Neuroscientist 2002, 8:297-301.
22. Frick K.M., Fernandez S.M. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol. Aging 2003, 24:615-626.
23. Gagné J., Gélinas S., Martinoli M.G., Foster T.C., Ohayon M., Thompson R.F., Baudry M., Massicotte G. AMPA receptor properties in adult rat hippocampus following environmental enrichment. Brain Res 1998, 799:16-25.
24. Goshen I., Avital A., Kreisel T., Licht T., Segal M., Yirmiya R. Environmental enrichment restores memory functioning in mice with impaired IL-1 signaling via reinstatement of long-term potentiation and spine size enlargement. J. Neurosci 2009, 29:3395-3403.
25. Gower A.J., Lamberty Y. The aged mouse as a model of cognitive decline with special emphasis on studies in NMRI mice. Behav. Brain Res 1993, 57:163-173.
26. Greenough W.T., Volkmar F.R. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol 1973, 40:491-504.
27. Greenough W.T., Volkmar F.R., Juraska J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol 1973, 41:371-378.
28. 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, 185:43-48.
29. Huang F.L., Huang K.P., Boucheron C. Long-term enrichment enhances the cognitive behavior of the aging neurogranin null mice without affecting their hippocampal LTP. Learn. Mem 2007, 14:512-519.
30. Iso H., Simoda S., Matsuyama T. Environmental change during postnatal development alters behaviour, cognitions and neurogenesis of mice. Behav. Brain Res 2007, 179:90-98.
31. Iwata E., Kikusui T., Takeuchi Y., Mori Y. Fostering and environmental enrichment ameliorate anxious behavior induced by early weaning in Balb/c mice. Physiol. Behav 2007, 91:318-324.
32. Janson M. Orthomolecular medicine: the therapeutic use of dietary supplements for anti-aging. Clin. Interv. Aging 2006, 1:261-265.
33. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol 2002, 52:135-143.
34. Kim S.J., Linden D.J. Ubiquitous plasticity and memory storage. Neuron 2007, 56:582-592.
35. Leal-Galicia P., Castañeda-Bueno M., Quiroz-Baez R., Arias C. Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol. Learn. Mem 2008, 90:511-518.
36. Lores-Arnaiz S., Bustamante J., Arismendi M., Vilas S., Paglia N., Basso N., Capani F., Coirini H., Costa J.J., Arnaiz M.R. Extensive enriched environments protect old rats from the aging dependent impairment of spatial cognition, synaptic plasticity and nitric oxide production. Behav. Brain Res 2006, 169:294-302.
37. Lynch M.A. Long-term potentiation and memory. Physiol. Rev 2004, 84:87-136.
38. Magnusson K.R. Declines in mRNA expression of different subunits may account for differential effects of aging on agonist and antagonist binding to the NMDA receptor. J. Neurosci 2000, 20:1666-1674.
39. Magnusson K.R., Bai L., Zhao X. The effects of aging on different C-terminal splice forms of the zeta1(NR1) subunit of the N-methyl-d-aspartate receptor in mice. Brain Res. Mol. Brain Res 2005, 135:141-149.
40. Magnusson K.R., Cotman C.W. Effects of aging on NMDA and MK801 binding sites in mice. Brain Res 1993, 604:334-337.
41. Milgram N.W., Siwak-Tapp C.T., Araujo J., Head E. Neuroprotective effects of cognitive enrichment. Ageing Res. Rev 2006, 5:354-369.
42. Naka F., Narita N., Okado N., Narita M. Modification of AMPA receptor properties following environmental enrichment. Brain Dev 2005, 27:275-278.
43. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci 2006, 7:697-709.
44. Nithianantharajah J., Hannan A.J. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog. Neurobiol 2009, 89:369-382.
45. Nithianantharajah J., Levis H., Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol. Learn. Mem 2004, 81:200-210.
46. Noël A., Quinette P., Guillery-Girard B., Dayan J., Piolino P., Marquis S., de la Sayette V., Viader F., Desgranges B., Eustache F. Psychopathological factors, memory disorders and transient global amnesia. Br. J. Psychiatry 2008, 193:145-151.
47. Nomura Y., Okuma Y. Age-related defects in lifespan and learning ability in SAMP8 mice. Neurobiol. Aging 1999, 20:111-115.
48. Norris C.M., Halpain S., Foster T.C. Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J. Neurophysiol 1998, 80:1567-1570.
49. Pham T.M., Söderström S., Winblad B., Mohammed A.H. Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats. Behav. Brain Res 1999, 103:63-70.
50. Potier B., Poindessous-Jazat F., Dutar P., Billard J.M. NMDA receptor activation in the aged rat hippocampus. Exp. Gerontol 2000, 35:1185-1199.
51. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., Hu Y. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12880-12884.
52. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol 2003, 69:143-179.
53. Roy V., Belzung C., Delarue C., Chapillon P. Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol. Behav 2001, 74:313-320.
54. Schmitt F., Ryan M., Cooper G. A brief review of the pharmacologic and therapeutic aspects of memantine in Alzheimer's disease. Expert Opin. Drug Metab. Toxicol 2007, 3:135-141.
55. Soffié M., Hahn K., Terao E., Eclancher F. Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res 1999, 101:37-49.
56. 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, 41:779-790.
57. Turner C.A., Lewis M.H. Environmental enrichment: effects on stereotyped behavior and neurotrophin levels. Physiol. Behav 2003, 80:259-266.
58. Volkmar F.R., Greenough W.T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 1972, 176:1445-1447.
59. Warren J.M., Zerweck C., Anthony A. Effects of environmental enrichment on old mice. Dev. Psychobiol 1982, 15:13-18.
60. Winocur G. Environmental influences on cognitive decline in aged rats. Neurobiol. Aging 1998, 19:589-597.
61. Zambrana C., Marco E.M., Arranz L., de Castro N.M., Viveros M.P., de la Fuente M. Influence of aging and enriched environment on motor activity and emotional responses in mice. Ann. N. Y. Acad. Sci 2007, 1100:543-552.
62. Zhu S.W., Yee B.K., Nyffeler M., Winblad B., Feldon J., Mohammed A.H. Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav. Brain Res 2006, 169:10-20.