Physical activity and neural correlates of aging: A combined TMS/fMRI study

Behavioural Brain Research

Volumn 222, Issue 1, 2011, Pages 158-168

  McGregor, Keith M ^a,b,c   Zlatar, Zvinka ^a,b   Kleim, Erin ^a,d   Sudhyadhom, Atchar ^d   Bauer, Andrew ^a   Phan, Stephanie ^a   Seeds, Lauren ^a   Ford, Anastasia ^a,c   Manini, Todd M ^b   White, Keith D ^a,b,c   Kleim, Jeffrey ^a,d   Crosson, Bruce ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c University of Florida   (United States)

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

Author keywords

Aging; FMRI; Interhemispheric communication; Physical activity; TMS

Indexed keywords

ADULT; AGE; AGED; AGING; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HUMAN; HUMAN EXPERIMENT; INTERHEMISPHERIC TRANSFER; MALE; NORMAL HUMAN; PHYSICAL ACTIVITY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SEDENTARY LIFESTYLE; TRANSCRANIAL MAGNETIC STIMULATION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; AREA UNDER CURVE; BACTERIA, AEROBIC; BRAIN; BRAIN MAPPING; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR ACTIVITY; MOVEMENT; MUSCLE CONTRACTION; OXYGEN; QUESTIONNAIRES; REACTION TIME; SEASONS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 79955112102     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.042     Document Type: Article

References (74)

1. Spirduso W.W. Reaction and movement time as a function of age and physical activity level. J Gerontol 1975, 30:435-440.
2. Elsayed M., Ismail A.H., Young R.J. Intellectual differences of adult men related to age and physical fitness before and after an exercise program. J Gerontol 1980, 35:383-387.
3. Colcombe S.J., Erickson K.I., Scalf P.E., Kim J.S., Prakash R., McAuley E., et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006, 61:1166-1170.
4. Colcombe S.J., Erickson K.I., Raz N., Webb A.G., Cohen N.J., McAuley E., et al. Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci 2003, 58:176-180.
5. Marks B.L., Madden D.J., Bucur B., Provenzale J.M., White L.E., Cabeza R., et al. Role of aerobic fitness and aging on cerebral white matter integrity. Ann NY Acad Sci 2007, 1097:171-174.
6. Gordon B.A., Rykhlevskaia E.I., Brumback C.R., Lee Y., Elavsky S., Konopack J.F., et al. Neuroanatomical correlates of aging, cardiopulmonary fitness level, and education. Psychophysiology 2008, 45:825-838.
7. Chaddock L, Erickson KI, Prakash RS, Kim JS, Voss MW, Vanpatter M, et al. A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res 2011;1358:172-83.
8. Chaddock L, Erickson KI, Prakash RS, VanPatter M, Voss MW, Pontifex MB, et al. Basal ganglia volume is associated with aerobic fitness in preadolescent children. Dev Neurosci 2011;32:249-56.
9. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P., McAuley E., Cohen N.J., et al. Proc Natl Acad Sci USA. Cardiovascular fitness, cortical plasticity, and aging 2004, 3316-3321.
10. Voelcker-Rehage C., Godde B., Staudinger U.M. Physical and motor fitness are both related to cognition in old age. Eur J Neurosci 2010, 31:167-176.
11. Prakash R.S., Voss M.W., Erickson K.I., Lewis J.M., Chaddock L., Malkowski E., et al. Cardiorespiratory fitness and attentional control in the aging brain. Front Hum Neurosci 2011, 4:229.
12. McGregor K.M., Craggs J.G., Benjamin M.L., Crosson B., White K.D. Age-related changes in motor control during unimanual movements. Brain Imaging Behav 2009, 3:317-331.
13. Rao S.M., Binder J.R., Bandettini P.A., Hammeke T.A., Yetkin F.Z., Jesmanowicz A., et al. Functional magnetic resonance imaging of complex human movements. Neurology 1993, 43:2311-2318.
14. Newton J.M., Sunderland A., Gowland P.A. fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement. Neuroimage 2005, 24:1080-1087.
15. Allison J.D., Meador K.J., Loring D.W., Figueroa R.E., Wright J.C. Functional MRI cerebral activation and deactivation during finger movement. Neurology 2000, 54:135-142.
16. Riecker A., Groschel K., Ackermann H., Steinbrink C., Witte O., Kastrup A. Functional significance of age-related differences in motor activation patterns. Neuroimage 2006, 32:1345-1354.
17. Stefanovic B., Warnking J.M., Pike G.B. Hemodynamic and metabolic responses to neuronal inhibition. Neuroimage 2004, 22:771-778.
18. Langan J., Peltier S.J., Bo J., Fling B.W., Welsh R.C., Seidler R.D. Functional implications of age differences in motor system connectivity. Front Syst Neurosci 2010, 4:17.
19. Ward N.S., Swayne O.B., Newton J.M. Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol Aging 2008, 29:1434-1446.
20. Naccarato M., Calautti C., Jones P.S., Day D.J., Carpenter T.A., Baron J.C. Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. Neuroimage 2006, 32:1250-1256.
21. Hlushchuk Y., Hari R. Transient suppression of ipsilateral primary somatosensory cortex during tactile finger stimulation. J Neurosci 2006, 26:5819-5824.
22. Ferbert A., Priori A., Rothwell J.C., Day B.L., Colebatch J.G., Marsden C.D. Interhemispheric inhibition of the human motor cortex. J Physiol 1992, 453:525-546.
23. Kobayashi M., Hutchinson S., Schlaug G., Pascual-Leone A. Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions. Neuroimage 2003, 20:2259-2270.
24. Muellbacher W., Facchini S., Boroojerdi B., Hallett M. Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 2000, 111:344-349.
25. Giovannelli F., Borgheresi A., Balestrieri F., Zaccara G., Viggiano M.P., Cincotta M., et al. Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study. J Physiol 2009, 587:5393-5410.
26. Peinemann A., Lehner C., Conrad B., Siebner H.R. Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci Lett 2001, 313:33-36.
27. Talelli P., Ewas A., Waddingham W., Rothwell J.C., Ward N.S. Neural correlates of age-related changes in cortical neurophysiology. Neuroimage 2008, 40:1772-1781.
28. Talelli P., Waddingham W., Ewas A., Rothwell J.C., Ward N.S. The effect of age on task-related modulation of interhemispheric balance. Exp Brain Res 2008, 186:59-66.
29. Sale M.V., Semmler J.G. Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 2005, 99:1483-1493.
30. Fujiyama H., Garry M.I., Levin O., Swinnen S.P., Summers J.J. Age-related differences in inhibitory processes during interlimb coordination. Brain Res 2009, 1262:38-47.
31. Cirillo J., Lavender A.P., Ridding M.C., Semmler J.G. Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J Physiol 2009, 587:5831-5842.
32. Krampe R.T., Engbert R., Kliegl R. The effects of expertise and age on rhythm production: adaptations to timing and sequencing constraints. Brain Cogn 2002, 48:179-194.
33. Jancke L., Shah N.J., Peters M. Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Brain Res Cogn Brain Res 2000, 10:177-183.
34. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
35. Cooper K.H. Testing and developing cardiovascular fitness within the United States Air Force. J Occup Med 1968, 10:636-639.
36. Godin G., Shephard R.J. A simple method to assess exercise behavior in the community. Can J Appl Sport Sci 1985, 10:141-146.
37. Jacobs D.R., Ainsworth B.E., Hartman T.J., Leon A.S. A simultaneous evaluation of 10 commonly used physical activity questionnaires. Med Sci Sports Exerc 1993, 25:81-91.
38. Lamb K.L., Brodie D.A. The assessment of physical activity by leisure-time physical activity questionnaires. Sports Med 1990, 10:159-180.
39. Verstynen T., Spencer R., Stinear C.M., Konkle T., Diedrichsen J., Byblow W.D., et al. Ipsilateral corticospinal projections do not predict congenital mirror movements: a case report. Neuropsychologia 2007, 45:844-852.
40. Hermsdorfer J., Danek A., Winter T., Marquardt C., Mai N. Persistent mirror movements: force and timing of " mirroring" are task-dependent. Exp Brain Res 1995, 104:126-134.
41. Garvey M.A., Ziemann U., Becker D.A., Barker C.A., Bartko J.J. New graphical method to measure silent periods evoked by transcranial magnetic stimulation. Clin Neurophysiol 2001, 112:1451-1460.
42. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996, 29:162-173.
43. Saad Z.S., Glen D.R., Chen G., Beauchamp M.S., Desai R., Cox R.W. A new method for improving functional-to-structural MRI alignment using local Pearson correlation. Neuroimage 2009, 44:839-848.
44. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
45. Yousry T.A., Schmid U.D., Alkadhi H., Schmidt D., Peraud A., Buettner A., et al. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 1997, 120(Pt 1):141-157.
46. Lenzi D., Conte A., Mainero C., Frasca V., Fubelli F., Totaro P., et al. Effect of corpus callosum damage on ipsilateral motor activation in patients with multiple sclerosis: a functional and anatomical study. Hum Brain Mapp 2007, 28:636-644.
47. Koenigkam-Santos M, de Castro M, Versiani BR, Diniz PR, Santos AC. Kallmann syndrome and mirror movements: white matter quantitative evaluation with magnetic resonance imaging. J Neurol Sci 2010;292:40-4.
48. Addamo P.K., Farrow M., Hoy K.E., Bradshaw J.L., Georgiou-Karistianis N. The influence of task characteristics on younger and older adult motor overflow. Q J Exp Psychol (Colchester) 2009, 62:239-247.
49. Baliz Y., Armatas C., Farrow M., Hoy K.E., Fitzgerald P.B., Bradshaw J.L., et al. The influence of attention and age on the occurrence of mirror movements. J Int Neuropsychol Soc 2005, 11:855-862.
50. Hoy K.E., Fitzgerald P.B., Bradshaw J.L., Armatas C.A., Georgiou-Karistianis N. Investigating the cortical origins of motor overflow. Brain Res Brain Res Rev 2004, 46:315-327.
51. Ottaviani D., Tiple D., Suppa A., Colosimo C., Fabbrini G., Cincotta M., et al. Mirror movements in patients with Parkinson's disease. Mov Disord 2008, 23:253-258.
52. Uttner I., Kraft E., Nowak D.A., Muller F., Philipp J., Zierdt A., et al. Mirror movements and the role of handedness: isometric grip forces changes. Motor Control 2007, 11:16-28.
53. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 2002, 17:85-100.
54. Wu T., Hallett M. The influence of normal human ageing on automatic movements. J Physiol 2005, 562:605-615.
55. Verstynen T., Diedrichsen J., Albert N., Aparicio P., Ivry R.B. Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol 2005, 93:1209-1222.
56. Hutchinson S., Kobayashi M., Horkan C.M., Pascual-Leone A., Alexander M.P., Schlaug G. Age-related differences in movement representation. Neuroimage 2002, 17:1720-1728.
57. Heuninckx S., Wenderoth N., Swinnen S.P. Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J Neurosci 2008, 28:91-99.
58. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P. The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans. Psychol Aging 2005, 20:363-375.
59. Voss MW, Prakash RS, Erickson KI, Basak C, Chaddock L, Kim JS, et al. Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci 2011;2.
60. Castillo-Garzon M.J., Ruiz J.R., Ortega F.B., Gutierrez A. Anti-aging therapy through fitness enhancement. Clin Interv Aging 2006, 1:213-220.
61. Pontifex M.B., Hillman C.H., Polich J. Age, physical fitness, and attention: P3a and P3b. Psychophysiology 2009, 46:379-387.
62. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 2011;108:3017-22.
63. D'Esposito M., Deouell L.Y., Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 2003, 4:863-872.
64. Marks B, Katz L, Styner M, Smith J. Aerobic fitness and obesity: relationship to cerebral white matter integrity in the brain of active and sedentary older adults. Br J Sports Med 2011.
65. Meyer B.U., Roricht S., Woiciechowsky C. Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices. Ann Neurol 1998, 43:360-369.
66. Meyer B.U., Roricht S., Grafin von Einsiedel H., Kruggel F., Weindl A. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 1995, 118(Pt 2):429-440.
67. Voss MW, Erickson KI, Prakash RS, Chaddock L, Malkowski E, Alves H, et al. Functional connectivity: a source of variance in the association between cardiorespiratory fitness and cognition? Neuropsychologia 2010;48:1394-406.
68. Cotman C.W., Berchtold N.C. Exercise:a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
69. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity - exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 2010;40:765-801.
70. Erickson KI, Prakash RS, Voss MW, Chaddock L, Heo S, McLaren M, et al. Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. J Neurosci 2010;30:5368-75.
71. Erickson K.I., Kramer A.F. Aerobic exercise effects on cognitive and neural plasticity in older adults. Br J Sports Med 2009, 43:22-24.
72. Erickson K.I., Prakash R.S., Voss M.W., Chaddock L., Hu L., Morris K.S., et al. Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 2009, 19:1030-1039.
73. Talairach J., Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain 1988, Georg Thieme Verlag, Stuttgart.
74. Ward BD. Deconvolution analysis of fMRI time series data. 2002. http://afni.nimh.nih.gov/AFNI/doc/3dDeconvolve.ps.