Exercise Training and Functional Connectivity Changes in Mild Cognitive Impairment and Healthy Elders

Journal of Alzheimer's Disease

Volumn 57, Issue 3, 2017, Pages 845-856

  Chirles, Theresa J ^a   Reiter, Katherine ^b   Weiss, Lauren R ^a   Alfini, Alfonso J ^a   Nielson, Kristy A ^b,c   Smith, J Carson ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b MARQUETTE UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Aging; Alzheimer's disease; cognitive disorders; connectivity; default mode network; exercise intervention; neural plasticity; posterior cingulate; precuneus; resting state functional MRI

Indexed keywords

ADULT; AEROBIC EXERCISE; AGED; ARTICLE; BRAIN MAPPING; CEREBELLUM; CLINICAL ARTICLE; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EXERCISE TEST; FEMALE; FRONTAL CORTEX; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INSULA; MALE; MILD COGNITIVE IMPAIRMENT; PARIETAL CORTEX; PARIETAL LOBE; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PRECUNEUS; PRIORITY JOURNAL; REST; TEMPORAL CORTEX; WALKING; BLOOD; CINGULATE GYRUS; COGNITIVE DYSFUNCTION; DIAGNOSTIC IMAGING; EXERCISE; IMAGE PROCESSING; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; STATISTICAL MODEL; VERY ELDERLY;

OXYGEN;

AGED; AGED, 80 AND OVER; COGNITIVE DYSFUNCTION; EXERCISE; EXERCISE TEST; FEMALE; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PSYCHIATRIC STATUS RATING SCALES;

EID: 85017535174     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-161151     Document Type: Article

References (80)

1. Jack CR, Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, Petersen RC, Trojanowski JQ (2010) Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol 9, 119-128.
2. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol 56, 303-308.
3. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256, 183-194.
4. Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, Broich K, Belleville S, Brodaty H, Bennett D, Chertkow H, Cummings JL, de Leon M, Feldman H, Ganguli M, Hampel H, Scheltens P, Tierney MC, Whitehouse P, Winblad B, impairment IPAEComc (2006) Mild cognitive impairment. Lancet 367, 1262-1270.
5. Pievani M, de Haan W, Wu T, Seeley WW, Frisoni GB (2011) Functional network disruption in the degenerative dementias. Lancet Neurology 10, 829-843.
6. Greicius M (2008) Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 21, 424-430.
7. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 270-279.
8. Pievani M, Filippini N, van den Heuvel MP, Cappa SF, Frisoni GB (2014) Brain connectivity in neurodegenerative diseases-from phenotype to proteinopathy. Nat Rev Neurol 10, 620-633.
9. Yamasaki T, Muranaka H, Kaseda Y, Mimori Y, Tobimatsu S (2012) Understanding the pathophysiology of Alzheimer's disease and mild cognitive impairment: A mini review on fMRI and ERP studies. Neurol Res Int 2012, 719056.
10. Goveas JS, Xie C, Ward BD, Wu Z, Li W, Franczak M, Jones JL, Antuono PG, Li SJ (2011) Recovery of hippocampal network connectivity correlates with cognitive improvement in mild Alzheimer's disease patients treated with donepezil assessed by resting-state fMRI. J Magn Reson Imaging 34, 764-773.
11. Li W, Antuono PG, Xie C, Chen G, Jones JL, Ward BD, Franczak MB, Goveas JS, Li SJ (2012) Changes in regional cerebral blood flow and functional connectivity in the cholinergic pathway associated with cognitive performance in subjects with mild Alzheimer's disease after 12-week donepezil treatment. Neuroimage 60, 1083-1091.
12. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29, 1860-1873.
13. Allen G, McColl R, Barnard H, Ringe WK, Fleckenstein J, Cullum CM (2005) Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage 28, 39-48.
14. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME (2007) Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447, 83-86.
15. Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL (2008) Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol 100, 3328-3342.
16. Wang L, Laviolette P, O'Keefe K, Putcha D, Bakkour A, Van Dijk KR, Pihlajamäki M, Dickerson BC, Sperling RA (2010) Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals. Neuroimage 51, 910-917.
17. Wang L, Negreira A, LaViolette P, Bakkour A, Sperling RA, Dickerson BC (2010) Intrinsic interhemispheric hippocampal functional connectivity predicts individual differences in memory performance ability. Hippocampus 20, 345-351.
18. Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56, 924-935.
19. Sporns O, Honey CJ, Kötter R (2007) Identification and classification of hubs in brain networks. PLoS One 2, e1049.
20. Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12, 512-523.
21. Power JD, Fair DA, Schlaggar BL, Petersen SE (2010) The development of human functional brain networks. Neuron 67, 735-748.
22. Alvarez P, Squire LR (1994) Memory consolidation and the medial temporal lobe: A simple network model. Proc Natl Acad Sci USA 91, 7041-7045.
23. Albert MS (2011) Changes in cognition. Neurobiol Aging 32 (Suppl 1), S58-S63.
24. Zhou Y, Dougherty JH, Hubner KF, Bai B, Cannon RL, Hutson RK (2008) Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer's disease and mild cognitive impairment. Alzheimers Dement 4, 265-270.
25. Greicius MD, Menon V (2004) Default-mode activity during a passive sensory task: Uncoupled from deactivation but impacting activation. J Cogn Neurosci 16, 1484-1492.
26. Hedden T, Van Dijk KR, Becker JA, Mehta A, Sperling RA, Johnson KA, Buckner RL (2009) Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J Neurosci 29, 12686-12694.
27. Drzezga A, Becker JA, Van Dijk KRA, Sreenivasan A, Talukdar T, Sullivan C, Schultz AP, Sepulcre J, Putcha D, Greve D, Johnson KA, Sperling RA (2011) Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain 134, 1635-1646.
28. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, Mintun MA (2005) Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25, 7709-7717.
29. Huang C, Wahlund LO, Svensson L, Winblad B, Julin P (2002) Cingulate cortex hypoperfusion predicts Alzheimer's disease in mild cognitive impairment. BMC Neuro 2, 9.
30. Zhang HY, Wang SJ, Xing J, Liu B, Ma ZL, Yang M, Zhang ZJ, Teng GJ (2009) Detection of PCC functional connectivity characteristics in resting-state fMRI in mild Alzheimer's disease. Behav Brain Res 197, 103-108.
31. Buckner RL (2004) Memory and executive function in aging and AD: Multiple factors that cause decline and reserve factors that compensate. Neuron 44, 195-208.
32. Hillary FG, Roman CA, Venkatesan U, Rajtmajer SM, Bajo R, Castellanos ND (2015) Hyperconnectivity is a fundamental response to neurological disruption. Neuropsychology 29, 59-75.
33. Reuter-Lorenz PA, Park DC (2010) Human neuroscience and the aging mind: A new look at old problems. J Gerontol B Psychol Sci Soc Sci 65, 405-415.
34. Reuter-Lorenz PA, Park DC (2014) How does it STAC up? Revisiting the scaffolding theory of aging and cognition. Neuropsychol Rev 24, 355-370.
35. Kramer AF, Erickson KI, Colcombe SJ (2006) Exercise, cognition, and the aging brain. J Appl Physiol (1985) 101, 1237-1242.
36. Cotman CW, Berchtold NC (2002) Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25, 295-301.
37. Smith JC, Nielson KA, Woodard JL, Seidenberg M, Rao SM (2013) Physical activity and brain function in older adults at increased risk for Alzheimer's disease. Brain Sci 3, 54-83.
38. Heyn P, Abreu BC, Ottenbacher KJ (2004) The effects of exercise training on elderly persons with cognitive impairment and dementia: A meta-analysis. Arch Phys Med Rehabil 85, 1694-1704.
39. Gates N, Fiatarone Singh MA, Sachdev PS, Valenzuela M (2013) The effect of exercise training on cognitive function in older adults with mild cognitive impairment: A meta-analysis of randomized controlled trials. Am J Geriatr Psychiatry 21, 1086-1097.
40. Woodard JL, Sugarman MA, Nielson KA, Smith JC, Seidenberg M, Durgerian S, Butts A, Hantke N, Lancaster M, Matthews MA, Rao SM (2012) Lifestyle and genetic contributions to cognitive decline and hippocampal structure and function in healthy aging. Curr Alzheimer Res 9, 436-446.
41. Voss MW, Prakash RS, Erickson KI, Basak C, Chaddock L, Kim JS, Alves H, Heo S, Szabo AN, White SM, Wójcicki TR, Mailey EL, Gothe N, Olson EA, McAuley E, Kramer AF (2010) Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci 2: 32.
42. Burdette JH, Laurienti PJ, Espeland MA, Morgan A, Telesford Q, Vechlekar CD, Hayasaka S, Jennings JM, Katula JA, Kraft RA, Rejeski WJ (2010) Using network science to evaluate exercise-associated brain changes in older adults. Front Aging Neurosci 2, 23.
43. Heisz JJ, Gould M, McIntosh AR (2015) Age-related shift in neural complexity related to task performance and physical activity. J Cogn Neurosci 27, 605-613.
44. Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, Plymate SR, Fishel MA, Watson GS, Cholerton BA, Duncan GE, Mehta PD, Craft S (2010) Effects of aerobic exercise on mild cognitive impairment: A controlled trial. Arch Neurol 67, 71-79.
45. Lautenschlager NT, Cox KL, Flicker L, Foster JK, van Bockxmeer FM, Xiao J, Greenop KR, Almeida OP (2008) Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: A randomized trial. JAMA 300, 1027-1037.
46. Smith JC, Nielson KA, Antuono P, Lyons JA, Hanson RJ, Butts AM, Hantke NC, Verber MD (2013) Semantic memory functional MRI and cognitive function after exercise intervention in mild cognitive impairment. J Alzheimers Dis 37, 197-215.
47. Stern Y (2009) Cognitive reserve. Neuropsychologia 47, 2015-2028.
48. Arenaza-Urquijo EM, Landeau B, La Joie R, Mevel K, Mézenge F, Perrotin A, Desgranges B, Bartrés-Faz D, Eustache F, Chételat G (2013) Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage 83, 450-457.
49. Fratiglioni L, Paillard-Borg S, Winblad B (2004) An active and socially integrated lifestyle in late life might protect against dementia. Lancet Neurol 3, 343-353.
50. Oldfield RC (1971) The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97-113.
51. Yesavage JA (1988) Geriatric depression scale. Psychopharmacol Bull 24, 709-711.
52. Folstein MF, Folstein SE, McHugh PR (1975), "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
53. Jurica P, Leitten C, Mattis S (2001) Dementia Rating Scale-2 Professional Manual, Psychological Assessment Resources, Lutz, Florida.
54. Rey A (1964) L'examen clinique en psychologic, Presses Universitaires de France, Paris.
55. Wechsler D (1997) WAIS-III/WMS-III technical manual, Psychological Corporation, San Antonio.
56. Smith A (1991) Symbol Digit Modalities Test, Western Psychological Services, Los Angeles.
57. Benton A, Hamsher K (1978) Multilingual Aphasia Examination: Manual of Instructions, Associates A, Iowa City.
58. Cosentino S, Jefferson A, Chute DL, Kaplan E, Libon DJ (2004) Clock drawing errors in dementia: Neuropsychological and neuroanatomical considerations. Cogn Behav Neurol 17, 74-84.
59. American College of Sports Medicine (2010) ACSM's guidelines for exercise testing and prescription, Lippincott Williams, amp; Wilkins, Philadelphia.
60. Borg G (1998), Borg's Perceived Exertion and Pain Scales, Human Kinetics, Champaign, IL.
61. Cook D, O'Connor P, Eubanks S, Smith J, Lee M (1997) Naturally occurring muscle pain during exercise: Assessment and experimental evidence. Med Sci Sports Exerc 29, 999-1012.
62. Mazzeo RS, Tanaka H (2001) Exercise prescription for the elderly: Current recommendations. Sports Med 31, 809-818.
63. Cox RW (1996) AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29, 162-173.
64. Chen G, Saad ZS, Britton JC, Pine DS, Cox RW (2013) Linear mixed-effects modeling approach to FMRI group analysis. Neuroimage 73, 176-190.
65. Barulli D, Stern Y (2013) Efficiency, capacity, compensation, maintenance, plasticity: Emerging concepts in cognitive reserve. Trends Cogn Sci 17, 502-509.
66. Ward AM, Schultz AP, Huijbers W, Van Dijk KR, Hedden T, Sperling RA (2014) The parahippocampal gyrus links the default-mode cortical network with the medial temporal lobe memory system. Hum Brain Mapp 35, 1061-1073.
67. Xie C, Bai F, Yu H, Shi Y, Yuan Y, Chen G, Li W, Zhang Z, Li SJ (2012) Abnormal insula functional network is associated with episodic memory decline in amnestic mild cognitive impairment. Neuroimage 63, 320-327.
68. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT (2011) The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106, 2322-2345.
69. Foster PP (2015) Role of physical and mental training in brain network configuration. Front Aging Neurosci 7, 117.
70. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E, Kramer AF (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 108, 3017-3022.
71. Smith JC, Nielson KA, Woodard JL, Seidenberg M, Durgerian S, Hazlett KE, Figueroa CM, Kandah CC, Kay CD, Matthews MA, Rao SM (2014) Physical activity reduces hippocampal atrophy in elders at genetic risk for Alzheimer's disease. Front Aging Neurosci 6, 61.
72. Smith JC, Lancaster MA, Nielson KA, Woodard JL, Seidenberg M, Durgerian S, Sakaie K, Rao SM (2016) Interactive effects of physical activity and APOE-, epsi; 4 on white matter tract diffusivity in healthy elders. Neuroimage 131, 102-112.
73. Head D, Bugg JM, Goate AM, Fagan AM, Mintun MA, Benzinger T, Holtzman DM, Morris JC (2012) Exercise engagement as a moderator of the effects of APOE genotype on amyloid deposition. Arch Neurol 69, 636-643.
74. Pihlajamaki M, Sperling RA (2009) Functional MRI assessment of task-induced deactivation of the default mode network in Alzheimer's disease and at-risk older individuals. Behav Neurol 21, 77-91.
75. Reiter K, Nielson KA, Smith TJ, Weiss LR, Alfini AJ, Smith JC (2015) Improved cardiorespiratory fitness is associated with increased cortical thickness in mild cognitive impairment. J Int Neuropsychol Soc 21, 757-767.
76. Persson J, Pudas S, Nilsson LG, Nyberg L (2014) Longitudinal assessment of default-mode brain function in aging. Neurobiol Aging 35, 2107-2117.
77. Middleton LE, Manini TM, Simonsick EM, Harris TB, Barnes DE, Tylavsky F, Brach JS, Everhart JE, Yaffe K (2011) Activity energy expenditure and incident cognitive impairment in older adults. Arch Intern Med 171, 1251-1257.
78. Etgen T, Sander D, Huntgeburth U, Poppert H, Förstl H, Bickel H (2010) Physical activity and incident cognitive impairment in elderly persons: The INVADE study. Arch Intern Med 170, 186-193.
79. Hedden T, Gabrieli JD (2004) Insights into the ageing mind: A view from cognitive neuroscience. Nat Rev Neurosci 5, 87-96.
80. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12, 585-601.