Enriched Environment and White Matter in Aging Brain

Anatomical Record

Volumn 295, Issue 9, 2012, Pages 1406-1414

  Yang, Shu ^a,b   Lu, Wei ^b   Zhou, De Shan ^a   Tang, Yong ^b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Aging; Enriched environment; Myelinated fiber; Stereology; White matter

Indexed keywords

AGE DISTRIBUTION; AGING; BRAIN FUNCTION; BRAIN SIZE; CELL LOSS; COGNITIVE DEFECT; DEMYELINATION; ENRICHED ENVIRONMENT; EPISODIC MEMORY; HUMAN; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROANATOMY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REMYELINIZATION; REVIEW; SOCIAL ENVIRONMENT; SPATIAL MEMORY; STIMULATION; WHITE MATTER;

AGING; ANIMALS; BRAIN; ENVIRONMENT; HUMANS; NERVE FIBERS, MYELINATED;

EID: 84865299284     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22526     Document Type: Review

References (109)

1. Albert M. 1993. Neuropsychological and neurophysiological changes in healthy adult humans across the age range. Neurobiol Aging 14: 623-625.
2. Bartzokis G, Cummings JL, Sultzer D, Henderson VW, Nuechterlein KH, Mintz J. 2003. White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Arch Neurol 60: 393-398.
3. Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullén F. 2005. Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8: 1148-1150.
4. Bennett EL, Diamond MC, Krech D, Rosenzweig MR. 1964. Chemical and anatomical plasticity of the brain. Science 164: 610-619.
5. Bennett EL, Rosenzweig MR, Diamond MC. 1969. Rat brain: effects of environmental enrichment on wet and dry weights. Science 163: 825-826.
6. Berlucchi G. 2002. The origin of the term plasticity in the neurosciences: Ernesto Lugaro and chemical synaptic transmission. J Hist Neurosci 11: 305-309.
7. Briones T, Shah P, Juraska J, Greenough WT. 1999. Effects of prolonged exposure to and subsequent removal from a complex environment on corpus callosum myelination in the adult rat, Soc Neurosci Abstr 25: 638.
8. Brody H. 1955. Organization of the cerebral cortex III: a study of aging in the human cerebral cortex. J Comp Neurol 102: 511-516.
9. Buckner RL. 2004. Buckner memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 44: 195-208.
10. Budson AE, Price BH. 2005. Memory dysfunction. N Engl J Med 352: 692-699.
11. Chen L, Lu W, Yang Z, Yang S, Li C, Shi X, Tang Y. 2011. Age-related changes of the oligodendrocytes in rat subcortical white matter. Anat Rec 294: 487-493.
12. Christiansen P, Larsson HB, Thomsen C, Wieslander SB, Henriksen O. 1994. Age dependent white matter lesions and brain volume changes in healthy volunteers. Acta Radiol 35: 117-122.
13. Colon EJ. 1972. The elderly brain: a quantitative analysis in the cerebral cortex of two cases. Psychiatr Neurol Neurochir 75: 261-270.
14. de Groot JC, de Leeuw FE, Oudkerk M, van Gijn J, Hofman A, Jolles J, Breteler MM. 2000. Cerebral white matter lesions and cognitive function: the Rotterdam scan study. Ann Neurol 47: 145-151.
15. Devaney KO, Johnson HA. 1980. Neuron loss in the aging visual cortex of man. J Gerontol 35: 836-841.
16. Diamond DM, Fleshner M, Ingersoll N, Rose GM. 1996. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 110: 661-672.
17. Diamond MC. 1967. Extensive cortical depth measurements and neuron size increases in the cortex of environmentally enriched rats. J Comp Neurol 131: 357-364.
18. Duce JA, Hollander W, Jaffe R, Abraham CR. 2006. Activation of early components of complement targets myelin and oligodendrocytes in the aged rhesus monkey brain. Neurobiol Aging 27: 633-644.
19. Erickson CA, Barnes CA. 2003. The neurobiology of memory changes in normal aging. Exp Gerontol 38: 61-69.
20. Fernandez CI, Collazo J, Bauza Y, Castellanos MR, Lopez O. 2004. Environmental enrichment-behavior-oxidative stress interactions in the aged rat. Ann N Y Acad Sci 1019: 53-57.
21. Foster TC, Dumas TC. 2001. Mechanism for increased hippocampal synaptic strength following differential experience. J Neurophysiol 85: 1377-1383.
22. Frick KM, Fernandez SM. 2003. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol Aging 24: 615-626.
23. Galani RE, Coutureau E, Kelche C. 1998. Effects of enriched postoperative housing conditions on spatial memory deficits in rats with selective lesions of the hippocampus, subiculum or entorhinal cortex. Restor Neutol Neurosci 13: 173-184.
24. Galani RE, Jarrard LE, Will BE, Kelche C. 1997. Effects of postoperative housing conditions on functional recovery in rats with lesions of the hippocampus, subiculum, or entorhinal cortex. Neurobiol Learn Mem 67: 43-56.
25. Gazzaley AH, Siegel SJ, Kordower JH, Mufson EJ, Morrison JH. 1996. Circuit-specific alterations of N-methyl-D-aspartate receptor subunit 1 in the dentate gyrus of agedmonkeys. Proc Natl Acad Sci USA 93: 3121-3125.
26. Globus A, Rosenzweig MR, Bennett EL, Diamond MC. 1973. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J Comp Physiol Psychol 82: 175-181.
27. Grady CL, Craik FI. 2000. Changes in memory processing with age. Curr Opin Neurobiol 10: 224-231.
28. Gravel M, Peterson J, Yong VW, Kottis V, Trapp B, Braun PE. 1996. Overexpression of 2', 3'-cyclic nucleotide 3'-phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination. Mol Cell Neurosci 7: 453-466.
29. Green EJ, Greenough WT. 1986. Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. J Neurophysiol 55: 739-750.
30. Greenough WT, Volkmar FR. 1973. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp Neurol 40: 491-504.
31. Gundersen HJG. 1986. Stereology of arbitrary particles: a review of unbiased number and size estimators and the presentation of some new ones, in memory of Williams R, Thomsen. J Microsc 143: 3-45.
32. Gundersen HJG, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, West MJ. 1988. The new stereological tools: disector, fractionator, nucleator and point sampling intercepts and their use in pathological research and diagnosis. APMIS 96: 857-881.
33. Guttmann CR, Jolesz FA, Kikinis R, Killiany RJ, Moss MB, Sandor T, Albert MS. 1998. White matter changes with normal aging. Neurology 50: 972-978.
34. Hara Y, Park CS, Janssen WG, Punsoni M, Rapp PR, Morrison JH. 2011. Synaptic characteristics of dentate gyrus axonal boutons and their relationships with aging, menopause, and memory in female rhesus monkeys. J Neurosci 31: 7737-7744.
35. Haug H. 1984. Macroscopic and microscopic morphometry of the human brain and cortex. A survey in the light of new results. Brain Pathol 1: 123-149.
36. Haug H. 1985. Are neurons of the human cerebral cortex really lost during aging? A morphometric evaluation. In: Traber J, Gispen WH, editors. Senile dementia of the Alzheimer type. Berlin: Springer. p 150-163.
37. Haug H, Kunl S, Mecke E, Sass NL, Wasner K. 1984. The significance of morphometric procedures in the investigation of age changes in cytoarchitectonic structures of human brain. J Hirnforch 25: 353-374.
38. Hebb DO. 1949. The organization of behavior: a neuropsychological theory. New York: Wiley.
39. Henderson G, Tomlinson BE, Gibson PH. 1980. Cell counts in human cerebral cortex in normal adults throughout life using an image analyzing computer. J Neurol Sci 46: 113-136.
40. Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, Hesselink JR. 2001. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol Aging 22: 581-594.
41. Juraska JM, Henderson C, Müller J. 1984. Differential rearing experience, gender, and radial maze performance. Dev Psychobiol 17: 209-215.
42. Juraska JM, Kopcik JR. 1988. Sex and environmental influences on the size and ultrastructure of the rat corpus callosum. Brain Res 450: 1-8.
43. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495.
44. 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.
45. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB. 2006. Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex. Exp Neurol 199: 113-121.
46. Kozorovitskiy Y, Gross CG, Kopil C, Battaglia L, McBreen M, Stranahan AM, Gould E. 2005. Experience induces structural and biochemical changes in the adult primate brain. Proc Natl Acad Sci USA 102: 17478-17482.
47. Kramer JH, Mungas D, Reed BR, Wetzel ME, Burnett MM, Miller BL, Weiner MW, Chui HC. 2007. Longitudinal MRI and cognitive change in healthy elderly. Neuropsychology 21: 412-418.
48. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
49. Lee B, Park JY, Jung WH, Kim HS, Oh JS, Choi CH, Jang JH, Kang DH, Kwon JS. 2010. White matter neuroplastic changes in long-term trained players of the game of "Baduk" (GO): a voxel-based diffusion-tensor imaging study. Neuroimage 52: 9-19.
50. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L. 2005. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163: 78-90.
51. Lemaitre H, Crivello F, Grassiot B, Alperovitch A, Tzourio C, Mazoyer B. 2005. Age- and sex-related effects on the neuroanatomy of healthy elderly. Neuroimage 26: 900-911.
52. Leuner B, Kozorovitskiy Y, Gross CG, Gould E. 2007. Diminished adult neurogenesis in the marmoset brain precedes old age. Proc Natl Acad Sci USA 104: 17169-17173.
53. Li C, Yang S, Zhang W, Lu W, Nyengaard JR, Morrison, JH, Tang Y. 2009. Demyelination induces the decline of the myelinated fiber length in aged white matter. Anat Rec 292: 528-535.
54. Lores-Arnaiz S, Bustamante J, Arismendi M, Vilas S, Paglia N, Basso N, Capani F, Coirini H, Costa JJ, Arnaiz MR. 2006. Extensive enriched environments protect old rats from the aging dependent impairment of spatial cognition, synaptic plasticity and nitric oxide production. Behav Brain Res 169: 294-302.
55. Madureira S, Verdelho A, Ferro J, Basile AM, Chabriat H, Erkinjuntti T, Fazekas F, Hennerici M, O'brien J, Pantoni L, Salvadori E, Scheltens P, Visser MC, Wahlund LO, Waldemar G, Wallin A, Inzitari D, LADIS Study Group. 2006. Development of a neuropsychological battery for the leukoaraiosis and disability in the elderly study (LADIS): experience and baseline data. Neuroepidemiology 27: 101-116.
56. Magalon K, Cantarella C, Monti G, Cayre M, Durbec P. 2007. Enriched environment promotes adult neural progenitor cell mobilization in mouse demyelination models. Eur J Neurosci 25: 761-771.
57. Marner L, Nyengaard JR, Tang Y, Pakkenberg B. 2003. Marked loss of myelinated fibers in human brain with age. J Comp Neurol 462: 144-152.
58. Meier-Ruge W, Ulrich J, Bruhlmann M, Meier E. 1992. Age-related white matter atrophy in the human brain. Ann N Y Acad Sci 673: 260-269.
59. Morrison JH, Hof PR. 1997. Life and death of neurons in the aging brain. Science 278: 412-419.
60. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C. 1995. Exercise and brain neurotrophins. Nature 373: 109.
61. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. 1999. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39: 569-578.
62. O'sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, Markus HS. 2001. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 57: 632-638.
63. Okuda H, Tatsumi K, Makinodan M, Yamauchi T, Kishimoto T, Wanaka A. 2009. Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J Neurosci Res 87: 3546-3553.
64. Pakkenberg B, Gundersen HJG. 1997. Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384: 312-320.
65. Paylor R, Morrison SK, Rudy JW, Waltrip LT, Wehner JM. 1992. Brief exposure to an enriched environment improves performance on the Morris water task and increases hippocampal cytosolic protein kinase C activity in young rats. Behav Brain Res 52: 49-59.
66. Peters A, Morrison JH, Rosene DL, Hyman BT. 1998. Feature article: are neurons lost from primate cerebral cortex during normal aging? Cereb Cortex 8: 295-300.
67. Peters A, Moss MB, Sethares C. 2000. Effects of aging on myelinated nerve fibers in monkey primary visual cortex. J Comp Neurol 419: 364-376.
68. Peters A, Sethares C, Killiany RJ. 2001. Effects of age on the thickness of myelin sheaths in monkey primary visual cortex. J Comp Neurol 435: 241-248.
69. Peters A, Sethares C. 2002. Aging and the myelinated fibers in prefrontal cortex and corpus callosum of the monkey. J Comp Neurol 442: 277-291.
70. Peters A, Sethares C. 2003. Is there remyelination during aging of the primate central nervous system? J Comp Neurol 460: 238-254.
71. Pham TM, Ickes B, Albeck D, Söderström S, Granholm A-Ch, Mohammed AH. 1999b. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for 1 year. Neuroscience 94: 279-286.
72. Pham TM, Söderström S, Winblad B, Mohammed AH. 1999a. Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats. Behav Brain Res 103: 63-70.
73. Rapp PR, Gallagher M. 1996. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci USA 93: 9926-9930.
74. Rasband MN, Tayler J, Kaga Y, Yang Y, Lappe-Siefke C, Nave KA, Bansal R. 2005. CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50: 86-90.
75. Rosenzweig MR, Bennett EL. 1996. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78: 57-65.
76. Rosenzweig MR, Bennett EL, Hebert M, Morimoto H. 1978. Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153: 563-576.
77. Saito S, Kaboyashi S, Ohashi Y, Igarashi M, Komiya Y, Ando S. 1994. Decreased synaptic density in aged brains and its prevention by rearing under enriched environment as revealed by synaptophysin contents. J Neurosci Res 39: 57-62.
78. Sanchez MM, Hearn EF, Do D, Rilling JK, Herndon JG. 1998. Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Res 812: 38-49.
79. Sandell JH, Peters A. 2001. Effects of age on nerve fibers in the rhesus monkey optic nerve. J Comp Neurol 429: 541-553.
80. Sandell JH, Peters A. 2002. Effects of age on the glial cells in the rhesus monkey optic nerve. J Comp Neurol 445: 13-28.
81. Sandell JH, Peters A. 2003. Disrupted myelin and axon loss in the anterior commissure of the aged rhesus monkey. J Comp Neurol 466: 14-30.
82. Scholz J, Klein MC, Behrens TE, Johansen-Berg H. 2009. Training induces changes in white-matter architecture. Nat Neurosci 12: 1370-1371.
83. Segovia G, Yagüe AG, García-Verdugo JM, Mora F. 2006. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 70: 8-14.
84. Shefer VF. 1973. Absolute number of neurons and thickness of the cerebral cortex during aging, senile vascular dementia, and Pick's and Alzheimer's diseases. Neurosci Behav Physiol 6: 319-324.
85. Shenkin SD, Bastin ME, Macgillivray TJ, Deary IJ, Starr JM, Rivers CS, Wardlaw JM. 2005. Cognitive correlates of cerebral white matter lesions and water diffusion tensor parameters in community-dwelling older people. Cerebrovasc Dis 20: 310-318.
86. Shields SA, Gilson JM, Blakemore WF, Franklin RJ. 1999. Remyelination occurs as extensively but more slowly in old rats compared to young rats following gliotoxin-induced CNS demyelination. Glia 28: 77-83.
87. Sim FJ, Zhao C, Penderis J, Franklin RJ. 2002. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 22: 2451-2459.
88. Sirevaag AM, Greenough WT. 1987. Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries. Brain Res 424: 320-332.
89. Soffié M, Hahn K, Terao E, Eclancher F. 1999. Behavioural and glial changes in old rats following environmental enrichment. Behav Brain Res 101: 37-49.
90. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the dissector. J Microsc 134: 127-136.
91. Sullivan EV, Adalsteinsson E, Pfefferbaum A. 2006. Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber t racking. Cereb Cortex 16: 1030-1039.
92. Szeligo F, Leblond CP. 1977. Response of the three main types of glial cells of cortex and corpus callosum in rats handled during suckling or exposed to enriched, control and impoverished environments following weaning. J Comp Neurol 172: 247-263.
93. Takeuchi H, Sekiguchi A, Taki Y, Yokoyama S, Yomogida Y, Komuro N, Yamanouchi T, Suzuki S, Kawashima R. 2010. Training of working memory impacts structural connectivity. J Neurosci 30: 3297-3303.
94. Tang Y, Nyengaard JR, Pakkenberg B, Gundersen HJG. 1997. Age-induced white matter changes in the human brain: a stereological investigation. Neurobiol Aging 18: 609-615.
95. Tauber H, Waehneldt TV, Neuhoff V. 1980. Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16: 235-238.
96. Terry AV, Jr, Kutiyanawalla A, Pillai A. 2011. Age-dependent alterations in nerve growth factor (NGF)-related proteins, sortilin, and learning and memory in rats. Physiol Behav 102: 149-157.
97. Terry RD, Deteresa R, Hansen LA. 1987. Neocortical cell counts in normal human adult aging. Ann Neurol 21: 530-539.
98. van Waas M, Soffié M. 1996. Differential environmental modulations on locomotor activity, exploration and spatial behaviour in young and old rats. Physiol Behav 59: 265-271.
99. Vance E. 2009. White matter helps brain learn: researchers demonstrate a role for the brain's connective tissue in learning a new task. Available at: http://www.the-scientist.com/news/print/55830/
100. Wenk GL, Pierce DJ, Struble RG, Price DL, Cork LC. 1989. Age-related changes in multiple neurotransmitter systems in the monkey brain. Neurobiol Aging 10: 11-19.
101. 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: 649-658.
102. Xu C, Yang S, Li C, Zhang W, Lu W, Tang Y. 2009a. Age-related changes of corpus callosum volume and myelinated fibers in frontal region of corpus callosum in rats. Chinese J Anat 32: 135-140.
103. Xu C, Yang S, Li C, Zhang W, Lu W, Tang Y. 2009b. Age-related changes of corpus callosum volume and myelinated fibers in frontal region of corpus callosum in rats. Chin J Anat 32: 135-139.
104. Yang S, Li C, Zhang W, Wang WW, Tang Y. 2008. Sex differences in the white matter and myelinated nerve fibers of Long-Evans rats. Brain Res 1216: 16-23.
105. Yang S, Li C, Zhang W, Wang WW, Tang Y. 2009. The myelinated fiber changes in the white matter of aged female Long-Evans rats. J Neurosci Res 87: 1582-1590.
106. Yin X, Peterson J, Gravel M, Braun PE, Trapp BD. 1997. CNP overexpression induces aberrant oligodendrocyte membranes and inhibits MBP accumulation and myelin compaction. J Neurosci Res 50: 238-247.
107. Ylikoski R, Ylikoski A, Erkinjuntti T, Sulkava R, Raininko R, Tilvis R. 1993. White matter changes in healthy elderly persons correlate with attention and speed of mental processing. Arch Neurol 50: 818-824.
108. Zeng Y, Tan M, Kohyama J, Sneddon M, Watson JB, Sun YE, Xie CW. 2011. Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging. J Neurosci 31: 17800-17810.
109. Zhao Y, Shi X, Qiu X, Zhang L, Lu W, Yang S, Li C, Chen G, Yang Z, Tang Y. 2011. Enriched environment increases the total number of CNPase positive cells in the corpus callosum of middle-aged rats. Acta Neurobiol Exp 71: 322-330.