Complex mental activity and the aging brain: Molecular, cellular and cortical network mechanisms

Brain Research Reviews

Volumn 56, Issue 1, 2007, Pages 198-213

  Valenzuela, Michael J ^a,b   Breakspear, Michael ^a,b   Sachdev, Perminder ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b PRINCE OF WALES HOSPITAL   (Australia)

Author keywords

Brain aging; Brain reserve; Compensation; Dementia; Mental activity; Neuroplasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CREATINE PHOSPHATE; GLUCOSE; NERVE GROWTH FACTOR; PROTEINASE;

ADAPTATION; AGING; ALZHEIMER DISEASE; ANGIOGENESIS; BEHAVIOR; BRAIN CORTEX; BRAIN DAMAGE; BRAIN FUNCTION; BRAIN INJURY; DEGENERATIVE DISEASE; DEMENTIA; DISEASE MODEL; GENE EXPRESSION; HUMAN; HUNTINGTON CHOREA; MENTAL PERFORMANCE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NEUROIMAGING; NEUROPROTECTION; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SYNAPTOGENESIS;

AGING; ANIMALS; CEREBRAL CORTEX; CYTOPROTECTION; DEMENTIA; ENERGY METABOLISM; HUMANS; MENTAL PROCESSES; NERVE DEGENERATION; NERVE GROWTH FACTORS; NERVE NET;

EID: 36148936744     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2007.07.007     Document Type: Review

References (137)

1. Achard S., Salvador R., Whitcher B., Suckling J., and and E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26 (2006) 63-72
2. Adlard P., Perreau V., Engesser-Cesar C., and Cotman C.W. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci. Lett. 363 (2004) 43-48
3. Adlard P., Perreau V., Pop V., and Cotman C.W. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J. Neurosci. 25 (2005) 4217-4221
4. Alexander G.E., Furey M.L., Grady C.L., Pietrini P., Brady D.R., Mentis M.J., and Schapiro M.B. Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: implications for the cognitive reserve hypothesis. Am. J. Psychiatry 154 (1997) 165-172
5. Altman J., Wallace R., Anderson W., and Das G. Behaviourally induced changes in length of cerebrum in rat. Dev. Psychobiol. 1 (1968) 112-117
6. Arendash G., et al. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable b-amyloid deposition. NeuroReport 15 (2004) 1751-1754
7. Artola A., von Frijtag J., Fermont P., Gispen W., Schrama L., Kamal A., and Sruijt B. Long-lasting modulation of the induction of LTD & LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 23 (2006) 261-272
8. Axmacher N., Mormann F., Fernandez G., Elger C., and Fell J. Memory formation by neural synchronization. Brain Res. Rev. 52 (2006) 170-182
9. Ball K., Bersch D., Helmers K., Jobe J., Leveck M., Marsiske M., Morris J., Rebok G., Smith D., Tennstedt S., Unverzagt F., and Willis S. Effect of cognitive training interventions with older adults - a randomised control trial. JAMA 288 (2002) 2271-2281
10. Black J., Isaacs K., Anderson B., Alcantara A., and Greenough W. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerenellar cortex of adult rats. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 5568-5572
11. Borenstein G.A., Mortimer J.A., Bowen J.D., McCormick W.C., McCurry S.M., Schellenberg G.D., and Larson E.B. Head circumference and incident Alzheimer's disease: modification by apolipoprotein E. Neurology 57 (2001) 1453-1460
12. Breakspear M., and Stam C. Dynamics of a neural system with a multiscale architecture. Philos. Trans. R. Soc. Lond., B Biol. Sci. 360 (2005) 1051-1074
13. Breakspear M., Terry J., and Friston K. Modulation of excitatory synaptic coupling facilitates synchronisation and complex dynamics in a biophysical model of neuronal dynamics. Network 14 (2003) 703-732
14. Brustovetsky N., Brustovetsky T., and Dubinsky J. On the mechanisms of neuroprotection by creatine and phosphocreatine. J. Neurochem. 76 (2001) 425-434
15. Burke D., Hickie I., Breakspear M., and Gotz M. Possibilities for the prevention and treatment of cognitive impairment and dementia. Br. J. Psychiatry 190 (2007) 371-372
16. Cabeza R. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J. Neurosci. 17 (1997) 391-400
17. Casti J. Complexification: explaining a paradoxical world through the science of surprise (1994), Harper Collins, New York
18. Cirrito J., Yamada K., Finn M., Sloviter R., Bales K., May P., Schoepp D., Paul S., Mennerick S., and Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-b levels in vivo. Neuron 48 (2005) 913-922
19. Colcombe S., Eriksson E., Scalf P., Kim J., Prakash R., McAuley E., Elavasky S., Marquez D., Hu L., and Kramer A. Aerobic exercise training increases brain volume in aging humans. J. Gerontol., Med. Sci. 61A (2006) 1166-1170
20. Costa D., Cracchiolo J., Bachstetter A., Hughes T., Bales K., Paul S., Mervis R., Arendash G., and Potter H. Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol. Aging 28 (2006) 831-844
21. Coyle J. Use it or lose it - do effortful mental activities protect against dementia?. New Engl. J. Med. 348 (2003) 25
22. Cracchiolo, J. T. Mori, S. Nazian, J. Tan, H. Potter, and G. Arendash, in press. Enhanced cognitive activity - over and above social or physical activity - is required to protect Alzheimer's mice against cognitive impairment, reduce Ab deposition, and increase synaptic immunostaining, Neurobiology of Learning & Memory.
23. D'Esposito M., Deouell L., and Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci. 4 (2003) 863-872
24. De Rosa R., Garcia A., Braschi C., Capsoni S., Maffei L., Berardi N., and Cattaneo A. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3811-3816
25. Diamond M. Enriching Heredity: The Impact of the Environment on the Anatomy of the Brain (1988), Collier MacMillan, London
26. Dickerson B., Salat D., Greve D., Chua E., et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65 (2005) 404-411
27. Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., and May A. Neuroplasticity: changes in grey matter induced by training. Nature 427 (2004) 311-312
28. Edland S., Xu Y., Plevak M., O'Brien P., Tangalos E., Peterson R., and Jack C. Total intracranial volume: normative values and lack of association with Alzheimer's disease. Neurology 59 (2002) 272-274
29. Emmerling M., Morganti-Kossman M., Kossman T., Stahel P., Watson M., Evans L., Spiegel K., Kuo Y., Roher A., and Raby C. Traumatic brain injury elevates the Alzheimer's amyloid peptide Aβ42 in human CSF: a possible role for nerve cell injury. Ann. N.Y. Acad. Sci. 903 (2000) 118-122
30. Fabrigoule C., Letenneur L., Dartigues J.F., Zarrouk M., Commenges D., and Barberger-Gateau P. Social and leisure activities and risk of dementia: a prospective longitudinal study. J. Am. Geriatr. Soc. 43 (1995) 485-490
31. Fratiglioni L., Wang H.X., Ericsson K., Maytan M., and Winblad B. Influence of social network on occurrence of dementia: a community-based longitudinal study. Lancet 355 (2000) 1315-1319
32. Ferrer I., Goutan E., Marin C., Rey M., and Ribalta T. Brain-derived neurotrophic factor in Huntington disease. Brain Res. 866 (2000) 257-261
33. Frick K., and Fernandez S. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol. Aging 24 (2003) 615-626
34. Fumagalli F., Racagni G., and Riva M. The expanding role of BDNF: a therapeutic target for Alzheimer's disease. Pharmacogenomics J. 6 (2006) 8-15
35. Gallacher J., Bayer A., and Ben-Shlomo Y. Commentary: activity each day keeps dementia away - does social interaction really preserve cognitive function?. Int. J. Epidemiol. 34 (2005) 872-873
36. Genoud C., Knott G., Sakata K., Lu B., and Welker E. Altered synapse formation in the adult somatosensory cortex of brain-derived neurotrophic factor heterozygote mice. J. Neurosci. 24 (2004) 2394-2400
37. Gould E., McEwen B., Tanapat P., Galea L., and Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17 (1997) 2492-2498
38. Grady C., McIntosh A., Beig S., Keightley M., Burian H., and Black S. Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer's disease. J. Neurosci. 23 (2003) 986-993
39. Haier R., Siegel B., Nuechterlein K., Hazlett E., Wu J., Paek J., Browning H., and Buchsbaum M. Cortical glucose metabolic rate correlates of reasoning and attention studied with positron emission tomography. Intelligence 12 (1988) 199-217
40. Haier R., Siegel B., McLachlan A., Soderling E., Lottenberg S., and Buchsbaum M. Regional glucose metabolic changes after learning a complex visuospatial/motor task: a PET study. Brain Res. 570 (1992) 134-143
41. Hempel A., Giesel F., Garcia Caraballo N., Amann M., Meyer H., Wustenberg T., Essig M., and Schroder J. Plasticity of cortical activation related to working memory during training. Am. J. Psychiatry 161 (2004) 745-747
42. Hilborn R. Sea gulls, butterflies, and grasshoppers: a brief history of the butterfly effect in nonlinear dynamics. Am. J. Phys. 72 (2004) 425-427
43. Honey, C., Kotter, R., Breakspear, M., Sporns, O., in press. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Nat. Acad. Sci. U.S.A.
44. Ickes B., Pham T., Sanders L., Albeck D., Mohammed A., and Granholm A. Long-term environment enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 164 (2000) 45-52
45. Ivanco T., and Greenough W. Physiological consequences of morphologically detectable synaptic plasticity: potential uses for examining recovery following damage. Neuropharmacology 39 (2000) 765-776
46. Jacobs B., Schall M., and Scheibel A. A quantitative dendritic analysis of Wernicke's area in humans: II. Gender, hemispheric, and environmental factors. J. Comp. Neurol. 327 (1993) 97-111
47. Jacobs B., van Praag H., and Gage F. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol. Psychiatry 5 (2000) 262-269
48. Janowsky J., et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J. Neurosci. 25 (2005) 5217-5224
49. Jenkins R., Fox N.C., Rossor A.M., Harvey R.J., and Rossor M.N. Intracranial volume and Alzheimer disease: evidence against the cerebral reserve hypothesis. Arch. Neurol. 57 (2000) 220-224
50. Kalaria R., and Ince P. Vascular factors in Alzheimer's disease. Ann. N.Y. Acad. Sci. 903 (2000)
51. Kamenetz K., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., and Malinow R. APP processing and synaptic function. Neuron 37 (2003) 925-937
52. Katzman R., Terry R., DeTeresa R., Brown T., Davies P., Fuld P., Reinbing X., and Peck A. Clinical, pathological and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann. Neurol. 23 (1988) 138-144
53. Kempermann G. Adult Neurogenesis (2006), Oxford University Press, New York
54. Kempermann G., Gast D., and Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 52 (2002) 135-143
55. Kerick S., Douglass L., and Hatfield B. Cerebral cortical adaptations associated with visuomotor practice. Med. Sci. Sports Exerc. 36 (2004) 118-129
56. Kramer A., Bherer L., Colcombe S., Dong W., and Greenough W. Environmental influences on cognitive and brain plasticity during aging. J. Gerontol., Med. Sci. 59A (2004) 940-957
57. Lavenex P., and Amaral D. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10 (2000) 420-430
58. Lazarov O., Robinson J., Tang Y., Hairston I., Korade-Mirnics Z., Lee V., Hersh L., Sapolsky R., Mirnics K., and Sisodia S. Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120 (2005) 701-713
59. Lee J., Duan W., and Mattson M. 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. 82 (2002) 1367-1375
60. Levi O., Jongen-Relo A., Feldon J., Roses A., and Michaelson D. ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol. Dis. 13 (2003) 273-282
61. Machulda M., Ward H., Borowski B., et al. Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients. Neurology 61 (2003) 500-506
62. Magistretti P., and Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond., B 354 (1999) 1155-1163
63. Malberg J., Eisch A., Nestler E., and Duman R. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
64. Malenka R., and Bear M. LTP & LTD: an embarrassment of riches. Neuron 44 (2004) 5-21
65. May R. Uses and abuses of mathematics in biology. Science 303 (2004) 790-793
66. May A., Hajak G., Steffens T., Langguth B., Kleinjung T., and Eichammer P. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb. Cortex 17 (2007) 205-210
67. How brainpower can help you cheat old age. New Sci. 17 (2005) 2530 (December)
68. Meshi S., Drew M., Saxe M., Ansorge M., David D., Santarelli L., Malapani C., Moore H., and Hen R. Hippocampal neurogenesis is not required for behavioural effects of environmental enrichment. Nat. Neurosci. 9 (2006) 729-731
69. Mohammed A.H., Zhu S., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M., Eriksson P., and Bogdanovic N. Environmental enrichment and the brain. In: Hofman M., Boer G., Hotmaat A., Van Someren E., and Swaab D. (Eds). Progress in Brain Res. vol. 138 (2002), Elsevier Science 109-133
70. Moore C., Cohen M., and Ranganath C. Neural mechanisms of expert skills in visual working memory. J. Neurosci. 26 (2006) 11187-11196
71. Naka F., Narita N., Okado N., and Narita M. Modification of AMPA receptor properties following environmental enrichment. Brain & Development 27 (2005) 275-278
72. Neuropathology Group of the Medical Research Council Cognitive Function and Aging Study (CFAS). Pathological correlates of late-onset dementia in a multicentre, community-based population in England and Wales. Lancet 375 (2001) 169-175
73. Nithianantharajah J., and Hannan A. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7 (2006) 697-709
74. Nitsch R., Farber S., Growdon J., and Wurtman R. Release of amyloid b-protein precursor derivatives by electrical depolarization of rat hippocampal slices. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 5191-5193
75. Obrien J., et al. Vascular cognitive impairment. Lancet Neurology 2 (2003) 89-98
76. Olesen P., Westerberg H., and Klingberg T. Increased prefrontal and parietal activity after training of working memory. Nat. Neurosci. 7 (2004) 75-79
77. Olson A., Eadie B., Ernst C., and Christie B. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16 (2006) 250-260
78. Owens W. Age and mental abilities: a second adult follow-up. J. Educ. Psychol. 57 (1966) 311-325
79. Patterson S., Abel T., Deuel T., Martin K., Rose J., and Kandel E. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16 (1996) 1137-1145
80. Patton P., and McNaughton B. Connection matrix of the hippocampal formation: I. The Dentate Gyrus. Hippocampus 5 (1995) 245-286
81. Pearson H., and Peers C. Physiological roles for amyloid b peptides. J. Physiol. 575 (2006) 5-10
82. Peigneux P., Laureys S., Fuchs S., Collette F., Perrin F., et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron. 44 (2004) 535-545
83. Peigneux P., Orban P., Balteau E., Degueldre C., Luxen A., Laureys S., and Maquet P. Offline persistence of memory-related cerebral activity during active wakefulness. PLOS Biology 4 (2006) e100
84. Pham T., et al. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94 (1999) 279-286
85. Rae C., Digney A., McEwan S., and Bates T. Oral creatine monohydrate supplementation improves brain performance: a double-blind, placebo-controlled, cross-over trial. Proceedings of the Royal Society of London - Series B: Biological Sciences 270 (2003) 2147-2150
86. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., and Hu Y.H. Effects of environmental enrichment on gene expression in the brain. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 12880-12884
87. Rampon C., Tang Y., Goodhouse J., Shimizu E., Kyin M., and Tsien J. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3 (2000) 238-244
88. Rolls E.T. Hippocampal-cortical and cortico-cortical backprojections. Hippocampus 10 (2000) 380-388
89. Rosen A., Prull M., O'Hara R., Race E., Desmond J., Glover G., Yesavage J., and Gabrieli J. Variable effects of aging on frontal lobe contributions to memory. Neuroreport 13 (2002) 2425-2428
90. Rosenzweig M., and Bennett E. Effects of differential environments on brain weights and enzyme activities in gerbils, rats, and mice. Dev. Psychobiol. 2 (1969) 87-95
91. Rosenzweig M., and Bennett E. Psychobiology of plasticity: effects of training and experience on brain and behavior. Brain Behav. Res. 78 (1996) 57-65
92. Rypma B., Berger J., Prabhakaran V., Martin Bly B., Kimberg D., Biswal B., and D'Esposito M. Neural correlates of cognitive efficiency. Neuroimage 33 (2006) 969-979
93. Salvador R., Suckling J., Schwarzbauer C., and Bullmore E. Unidirectioned graphs of frequency-dependent functional connectivity in whole brain networks. Philos. Trans. R. Soc. Lond., B 360 (2005) 937-946
94. Sapolsky R. Stress, the Aging Brain and the Mechanisms of Neuron Death (1992), MIT Press, Cambridge
95. Satz P. Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology 7 (1993) 273-295
96. Scarmeas N., Levy G., Tang M., Manly J., and Stern Y. Influence of leisure activity on the incidence of Alzheimer's disease. Neurology 57 (2001) 2236-2242
97. Scarmeas N., Zarahn E., ANderson K., Habeck C., Hilton J., Flynn J., Marder K., Bell K., Sackeim H.A., Van Heertum R., Moeller J.R., and Stern Y. Association of life activities with cerebral blood flow in Alzheimer disease. Arch. Neurol. 60 (2003) 359-365
98. Scheff S., and Price D.A. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol. Aging 24 (2003) 1029-1046
99. Scheibel A., Paul A., Fried I., Forsythe A., Tomiyasu U., and Wechsler A. A quantitative study of dendrite complexity in selected areas of the human cortex. Brain Cogn. 12 (1990) 85-101
100. Schofield P. The brain reserve hypothesis. In: Sachdev P. (Ed). Brain Ageing (2002), Swets & Zeitlinger, NY
101. Schofield P., Logroscino G., Andrews H., Albert S., and Stern Y. An association between head circumference and Alzheimer's disease in a population-based study of aging and dementia. Neurology 49 (1997) 30-37
102. Schofield P., Mosesson R., Stern Y., and Mayeux R. The age at onset of Alzheimer's disease and an intracranial area measurement: a relationship. Arch. Neurol. 52 (1995) 95-98
103. Schooler C. Psychological effects of complex environments during the life span: a review and theory. In: Schooler C., and Schaie K. (Eds). Cognitive Functioning and Social Structure Over the Life Course, Ablex, (1987), Norwood, NJ 24-49
104. Sheng J., Boop F., Mrak R., and Griffin S. Increased neuronal b-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1a immunoreactivity. J. Neurochem. 1872 (1994)
105. Shors T., Miesegaes G., Beylin A., et al. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
106. Snowdon D., Kemper S., Mortimer J., Greiner L., Wekstein D., and Markesbery W. Linguistic ability in early life and cognitive function and Alzheimer's disease in late life. JAMA 275 (1996) 528-532
107. Sofroniew M., Howe C., and Mobley W. Nerve growth factor signalling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24 (2001) 1217-1281
108. Spires T., Grote H., Varshney N., Cordery P., van Dellen A., Blakemore C., and Hannan A. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J. Neurosci. 24 (2004) 2270-2276
109. Sporns O., and Zwi J. The small world of the cerebral cortex. Neuroinformatics 2 (2004) 145-162
110. Stam C. Functional connectivity patterns of human magnetoencephalographic recordings: a 'small-world' network?. Neurosci. Lett. 355 (2004) 25-28
111. Stam C., Jones B., Nolte G., Breakspear M., and Scheltens P. Small-world networks and functional connectivity in Alzheimer's disease. Cereb. Cortex 17 (2007) 92-99
112. Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J. Int. Neuropsychol. Soc. 8 (2002) 448-460
113. Stern Y., Alexander G., Prohovnik I., and Mayeux R. Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer's disease. Ann. Neurol. 32 (1992) 371-375
114. Stern Y., Alexander G., Stricks L., Link B., and Mayeux R. Relationship between lifetime occupation and parietal flow: implications for a reserve against Alzheimer's disease pathology. Neurology 45 (1995) 55-60
115. Stern Y., Moeller J., Anderson K., Luber B., Zubin N., DiMauro A., Park A., Campbell C., Marder K., Bell K., et al. Different brain networks mediate task performance in normal aging and AD - defining compensation. Neurology 55 (2000) 1291-1297
116. Tang Y., Wang H., Feng R., Kyin M., and Tsien J. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 41 (2001) 779-790
117. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations and validation. Brain Res. Rev. 53 (2007) 198-214
118. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L., and Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30 (1991) 572-580
119. Tononi G., Edelman G., and Sporns O. Complexity and coherency: integrating information in the brain. Trends Cogn. Sci. 2 (1998) 474-484
120. Tononi G., Sporns O., and Edelman G. Measures of degeneracy and redundancy in biological networks. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3257-3262
121. Treves A., and Rolls E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus 4 (1994) 374-391
122. Valenzuela M., and Sachdev P. Magnetic resonance spectroscopy in AD. Neurology 506 (2001) 592-598
123. Valenzuela M., and Sachdev P. Brain reserve and cognitive decline: a nonparametric systematic review. Psychol. Med. 36 (2006) 1065-1073
124. Valenzuela M.J., and Sachdev P. Brain reserve and dementia: a systematic review. Psychol. Med. 36 (2006) 441-454
125. Valenzuela, M., Sachdev P. 2006c. Brain Reserve: The impact of complex mental activity on dementia incidence, cognitive decline and hippocampal structure and function. Published abstract, 10th International Conference on Alzheimer's Disease and Related Disorders, Madrid, Spain.
126. Valenzuela M.J., and Sachdev P. Assessment of Complex Mental Activity Across the Lifespan: Development of the Lifetime of Experiences Questionnaire. Psychol. Med. 37 (2007) 1015-1025
127. Valenzuela M.J., Jones M., Wen W., Rae C., Graham S., Shnier R., and Sachdev P. Memory training alters hippocampal neurochemistry in healthy elderly. Neuroreport 14 (2003) 1333-1337
128. Valenzuela M., Sachdev P., Rundeck T., and Bennett D. Cognitive leisure activities, but not watching TV, for future brain benefits. Neurology 67 (2006) 729
129. van Praag H., Christie B., Sejnowski T., and Gage F. Running enhances neurogenesis, learning and long-term potentiation in mice. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13427-13431
130. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1 (2000) 191-198
131. van Praag H., Schinder A., Christie B., Toni N., Palmer T., and Gage F. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
132. Verghese J., Lipton R., Katz M., Hall C., Derby C., Kuslansky G., Ambrose A., Sliwinski M., and Buschke H. Leisure activities and the risk of dementia in the elderly. New Engl. J. Med. 348 (2003) 2508-2516
133. Wakita H., Tomimoto H., Akiguchi I., Ohnishi K., Nakamura S., and Kimura J. Regional accumulation of amyloid beta/A4 protein precursor in the gerbil brain after transient cerebral ischemia. Neurosci. Lett. 146 (1992) 135-138
134. Wang H.X., Karp A., Windblad B., and Fratiglioni L. Late-life engagement in social and leisure activities is associated with a decreased risk of dementia: a longitudinal study from the Kungsholmen project. Am. J. Epidemiol. 155 (2002) 1081-1087
135. Watts D., and Stogratz S. Collective dynamics of 'small world' networks. Nature 393 (1998) 440-442
136. Willis S., Tennstedt S., Ball K., Elias J., Mann Koepke K., Morris J., et al. Long-term effects of cognitive training on everyday functional outcomes in older adults. JAMA 296 (2006) 2805-2814
137. Wilson R.S., Mendes De Leon C.F., Barnes L.L., Schneider J.A., Bienias J.L., Evans D.A., and Bennett D.A. Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 287 (2002) 742-748