Environmental enrichment restores neurogenesis and rapid acquisition in aged rats

Neurobiology of Aging

Volumn 34, Issue 1, 2013, Pages 263-274

  Speisman, Rachel B ^a   Kumar, Ashok ^b,c   Rani, Asha ^b,c   Pastoriza, Jessica M ^a   Severance, Jamie E ^a   Foster, Thomas C ^b,c   Ormerod, Brandi K ^a,b,c  

^a J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Adult neurogenesis; Age related; Enrichment; Fisher 344; Hippocampus; Learning; Memory; Neural progenitor cell; Water maze

Indexed keywords

AGE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FISCHER 344 RAT; HIPPOCAMPUS; MALE; MAZE TEST; MENTAL DETERIORATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; TASK PERFORMANCE;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS; BROMODEOXYURIDINE; CELL COUNT; CUES; ENVIRONMENT; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MALE; MAZE LEARNING; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; PHOSPHOPYRUVATE HYDRATASE; PROTEOGLYCANS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, INBRED F344; SPATIAL BEHAVIOR; TIME FACTORS;

EID: 84868132543     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.05.023     Document Type: Article

References (77)

1. Aizawa K., Ageyama N., Yokoyama C., Hisatsune T. Age-dependent alteration in hippocampal neurogenesis correlates with learning performance of macaque monkeys. Exp. Anim 2009, 58:403-407.
2. Altman J., Das G.D. Post-natal origin of microneurones in the rat brain. Nature 1965, 207:953-956.
3. Bizon J.L., Gallagher M. Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur. J. Neurosci 2003, 18:215-219.
4. Bizon J.L., Lee H.J., Gallagher M. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 2004, 3:227-234.
5. Camel J.E., Withers G.S., Greenough W.T. Persistence of visual cortex dendritic alterations induced by postweaning exposure to a "superenriched" environment in rats. Behav. Neurosci 1986, 100:810-813.
6. Cameron H.A., McKay R.D. Restoring production of hippocampal neurons in old age. Nat. Neurosci 1999, 2:894-897.
7. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol 2001, 435:406-417.
8. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56:337-344.
9. Carter C.S., Leeuwenburgh C., Daniels M., Foster T.C. Influence of calorie restriction on measures of age-related cognitive decline: role of increased physical activity. J. Gerontol. A Biol. Sci. Med. Sci 2009, 64:850-859.
10. Coras R., Siebzehnrubl F.A., Pauli E., Huttner H.B., Njunting M., Kobow K., Villmann C., Hahnen E., Neuhuber W., Weigel D., Buchfelder M., Stefan H., Beck H., Steindler D.A., Blümcke I. Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 2010, 133:3359-3372.
11. Correa D.D., DeAngelis L.M., Shi W., Thaler H., Glass A., Abrey L.E. Cognitive functions in survivors of primary central nervous system lymphoma. Neurology 2004, 62:548-555.
12. Crossen J.R., Garwood D., Glatstein E., Neuwelt E.A. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. J. Clin. Oncol 1994, 12:627-642.
13. Dalla C., Papachristos E.B., Whetstone A.S., Shors T.J. Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2927-2932.
14. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci 2010, 11:339-350.
15. Drapeau E., Mayo W., Aurousseau C., Le Moal M., Piazza P.V., Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14385-14390.
16. Drapeau E., Montaron M.F., Aguerre S., Abrous D.N. Learning-induced survival of new neurons depends on the cognitive status of aged rats. J. Neurosci 2007, 27:6037-6044.
17. Driscoll I., Howard S.R., Stone J.C., Monfils M.H., Tomanek B., Brooks W.M., Sutherland R.J. The aging hippocampus: a multi-level analysis in the rat. Neuroscience 2006, 139:1173-1185.
18. Epp J.R., Galea L.A. Hippocampus-dependent strategy choice predicts low levels of cell proliferation in the dentate gyrus. Neurobiol. Learn. Mem 2009, 91:437-446.
19. Epp J.R., Haack A.K., Galea L.A. Task difficulty in the Morris water task influences the survival of new neurons in the dentate gyrus. Hippocampus 2010, 20:866-876.
20. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med 1998, 4:1313-1317.
21. Fernández C.I., Collazo J., Bauza Y., Castellanos M.R., López 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. Foster T.C. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res. Brain Res. Rev 1999, 30:236-249.
23. 2 channels in senescent synaptic plasticity. Prog. Neurobiol 2012, 96:283-303.
24. Foster T.C., Dumas T.C. Mechanism for increased hippocampal synaptic strength following differential experience. J. Neurophysiol 2001, 85:1377-1383.
25. Foster T.C., Kumar A. Susceptibility to induction of long-term depression is associated with impaired memory in aged Fischer 344 rats. Neurobiol. Learn. Mem 2007, 87:522-535.
26. Foster T.C., Sharrow K.M., Kumar A., Masse J. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol. Aging 2003, 24:839-852.
27. Frick K.M., Fernandez S.M. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol. Aging 2003, 24:615-626.
28. Frick K.M., Stearns N.A., Pan J.Y., Berger-Sweeney J. Effects of environmental enrichment on spatial memory and neurochemistry in middle-aged mice. Learn. Mem 2003, 10:187-198.
29. Gage F.H., Dunnett S.B., Björklund A. Spatial learning and motor deficits in aged rats. Neurobiol. Aging 1984, 5:43-48.
30. Galea L.A., Ormerod B.K., Sampath S., Kostaras X., Wilkie D.M., Phelps M.T. Spatial working memory and hippocampal size across pregnancy in rats. Horm. Behav 2000, 37:86-95.
31. Gerlai R. Behavioral tests of hippocampal function: simple paradigms complex problems. Behav. Brain Res 2001, 125:269-277.
32. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci 1999, 2:260-265.
33. 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.
34. 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.
35. Hattiangady B., Shetty A.K. Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol. Aging 2008, 29:129-147.
36. 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.
37. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
38. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci 1998, 18:3206-3212.
39. Kennard J.A., Woodruff-Pak D.S. Age sensitivity of behavioral tests and brain substrates of normal aging in mice. Front. Aging Neurosci 2011, 3:9.
40. Kolb B., Pedersen B., Ballermann M., Gibb R., Whishaw I.Q. Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J. Neurosci 1999, 19:2337-2346.
41. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci 1996, 16:2027-2033.
42. Kumar A., Rani A., Tchigranova O., Lee W., Foster T.C. Influence of late-life exposure to environmental enrichment or exercise on hippocampal function and CA1 senescent physiology. Neurobiol. Aging 2012, 33:828.e1-828.e17.
43. Kumar A., Thinschmidt J.S., Foster T.C., King M.A. Aging effects on the limits and stability of long-term synaptic potentiation and depression in rat hippocampal area CA1. J. Neurophysiol 2007, 98:594-601.
44. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci 2010, 33:569-579.
45. 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.
46. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J. Neurochem 2002, 82:1367-1375.
47. 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, 163:78-90.
48. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11032-11037.
49. Leventhal C., Rafii S., Rafii D., Shahar A., Goldman S.A. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell. Neurosci 1999, 13:450-464.
50. Lichtenwalner R.J., Forbes M.E., Bennett S.A., Lynch C.D., Sonntag W.E., Riddle D.R. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 2001, 107:603-613.
51. 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.
52. Lugert S., Basak O., Knuckles P., Haussler U., Fabel K., Götz M., Haas C.A., Kempermann G., Taylor V., Giachino C. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 2010, 6:445-456.
53. Madsen T.M., Kristjansen P.E., Bolwig T.G., Wörtwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 2003, 119:635-642.
54. Merrill D.A., Karim R., Darraq M., Chiba A.A., Tuszynski M.H. Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol 2003, 459:201-207.
55. Monje M.L., Vogel H., Masek M., Ligon K.L., Fisher P.G., Palmer T.D. Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann. Neurol 2007, 62:515-520.
56. Nacher J., Alonso-Llosa G., Rosell D.R., McEwen B.S. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol. Aging 2003, 24:273-284.
57. Obiang P., Maubert E., Bardou I., Nicole O., Launay S., Bezin L., Vivien D., Agin V. Enriched housing reverses age-associated impairment of cognitive functions and tPA-dependent maturation of BDNF. Neurobiol. Learn. Mem 2011, 96:121-129.
58. Ormerod B.K., Beninger R.J. Water maze versus radial maze: differential performance of rats in a spatial delayed match-to-position task and response to scopolamine. Behav. Brain Res 2002, 128:139-152.
59. Ormerod B.K., Lee T.T., Galea L.A. Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons. Neuroscience 2004, 128:645-654.
60. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol 2000, 425:479-494.
61. Raber J., Rola R., LeFevour A., Morhardt D., Curley J., Mizumatsu S., VandenBerg S.R., Fike J.R. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res 2004, 162:39-47.
62. Rapp P.R., Rosenberg R.A., Gallagher M. An evaluation of spatial information processing in aged rats. Behav. Neurosci 1987, 101:3-12.
63. Roman D.D., Sperduto P.W. Neuropsychological effects of cranial radiation: current knowledge and future directions. Int. J. Radiat. Oncol. Biol. Phys 1995, 31:983-998.
64. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17501-17506.
65. Schrijver N.C., Bahr N.I., Weiss I.C., Würbel H. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol. Biochem. Behav 2002, 73:209-224.
66. Segovia G., Yagüe A.G., García-Verdugo J.M., Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res. Bull 2006, 70:8-14.
67. Seifert A.W., Zheng Z., Ormerod B.K., Cohn M.J. Sonic hedgehog controls growth of external genitalia by regulating cell cycle kinetics. Nat. Commun 2010, 1:23.
68. Shetty A.K., Hattiangady B., Shetty G.A. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 2005, 51:173-186.
69. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
70. Siffert J., Allen J.C. Late effects of therapy of thalamic and hypothalamic tumors in childhood: vascular, neurobehavioral and neoplastic. Pediatr. Neurosurg 2000, 33:105-111.
71. Siwak-Tapp C.T., Head E., Muggenburg B.A., Milgram N.W., Cotman C.W. Neurogenesis decreases with age in the canine hippocampus and correlates with cognitive function. Neurobiol. Learn. Mem 2007, 88:249-259.
72. Snyder J.S., Hong N.S., McDonald R.J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
73. Uylings H.B., van Eden C.G., Hofman M.A. Morphometry of size/volume variables and comparison of their bivariate relations in the nervous system under different conditions. J. Neurosci. Methods 1986, 18:19-37.
74. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 2002, 415:1030-1034.
75. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci 2005, 25:8680-8685.
76. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec 1991, 231:482-497.
77. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.