Functional implications of age differences in motor system connectivity

Frontiers in Systems Neuroscience

Volumn 4, Issue , 2010, Pages

  Langan, Jeanne ^a   Peltier, Scott J ^a   Bo, Jin ^a   Fling, Brett W ^a   Welsh, Robert C ^b,c   Seidler, Rachael D ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Aging; Corpus callosum; fMRI; Functional connectivity; Motor cortex

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; INTERHEMISPHERIC TRANSFER; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; MOTOR SYSTEM; NERVE CELL INHIBITION; NERVE DEGENERATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RESPONSE TIME; REST; TASK PERFORMANCE;

EID: 78951489620     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2010.00017     Document Type: Article

References (91)

1. Addamo, P. K., Farrow, M., Hoy, K. E., Bradshaw, J. L., and Georgiou-Karistianis, N. (2007). The effects of age and attention on motor overflow production-a review. Brain Res. Rev. 54, 189-204.
2. Bartels, C., Mertens, N., Hofer, S., Merboldt, K. D., Dietrich, J., Frahm, J., and Ehreneich, H. (2008). Callosal dysfunction in amyotrophic lateral sclerosis correlates with diffusion tensor imaging of the central motor system. Neuromuscul. Disord. 18, 398-407.
3. Biswal, B. B., Mennes, M., Zuo, X., Gohel, S., Kelly, C., Smith, S. M., Beckmann, C. F., Adelstein, J. S., Buckner, R. L., Colcombe, S., Dogonowski, A., Ernst, M., Fair, D., Hampson, M., Hoptman, M. J., Hyde, J. S., Kiviniemi, V. J., Kötter, R., Li, S., Lin, C., Lowe, M. J., Mackay, C., Madden, D. J., Madsen, K. H., Margulies, D. S., Mayberg, H. S., McMahon, K., Monk, C. S., Mostofsky, S. H., Nagel, B. J., Pekar, J. J., Peltier, S. J., Petersen, S. E., Riedl, V., Rombouts, S. A., Rypma, B., Schlaggar, B. L., Seidler, R. D., Siegle, G. J., Sorg, C., Teng, G., Veijola, J., Villringer, A., Walter, M., Wang, L., Weng, X., Whitfield-Gabrieli, S., Williamson, P., Windischberger, C., Zang, Y., Zhang, H., Castellanos, F. X., and Milham, M. P. (2010). Towards discovery science of human brain function. PNAS 107, 4734-4739.
4. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541.
5. Cabeza, R. (2001). Cognitive neuroscience of aging: contributions of functional neuroimaging. Scand. J. Psychol. 42, 277-286.
6. Cabeza, R., Anderson, N. D., Locantore, J. K., and McIntosh, A. R. (2002). Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17, 1394-1402.
7. Chen, R. (2004). Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp. Brain Res. 154, 1-10.
8. Colcombe, S. J., Kramer, A. F., Erickson, K. I., and Scalf, P. (2005). The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans. Psychol. Aging 20, 363-375.
9. Cordes, D., Haughton, V. M., Arfanakis, K., Wendt, G. J., Turski, P. A., Moritz, C. H., Quigley, M. A., and Meyerand, M. E. (2000). Mapping functionally related regions of brain with functional connectivity MR imaging. Am. J. Neuroradiol. 21, 1636-1644.
10. De Gennaro, L., Cristiani, R., Bertini, M., Curcio, G., Ferrara, M., Fratello, F., Romei, V., and Rossini, P. M. (2004). Handedness is mainly associated with an asymmetry of corticospinal excitability and not of transcallosal inhibition. Clin. Neurophysiol. 115, 1305-1312.
11. De Luca, M., Smith, S., De Stefano, N., Federico, A., and Matthews, P. M. (2005). Blood oxygenation level dependent contrast resting state networks are relevant to functional activity in the neocortical sensorimotor system. Exp. Brain Res. 167, 587-594.
12. Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Shehzad, Z., Biswal, B., Walters, J. R., Castellanos, F. X., and Milham, M. P. (2008). Functional connectivity of human striatum: a resting state FMRI study. Cereb. Cortex 18, 2735-2747.
13. Dittmar, M. (2002). Functional and postural lateral preferences in humans: interrelations and life-span age differences. Human Biol. 74, 569-585.
14. Duque, J., Murase, N., Celnik, P., Hummel, F., Harris-Love, M., Mazzocchio, R., Olivier, E., and Cohen, L. G. (2007). Intermanual differences in movement-related interhemispheric inhibition. J. Cogn. Neurosci. 19, 204-213.
15. Duque, J., Hummel, F., Celnik, P., Murase, N., Mazzocchio, R., and Cohen, L. G. (2005). Transcallosal inhibition in chronic subcortical stroke. Neuroimage 28, 940-946.
16. Eccles, J. C. (1989). Evolution of the Brain: Creation of the Self. London: Routledge.
17. Fabri, M., Polonara, G., Quattrini, A., Salvolini, U., Del Pesce, M., and Manzoni, T. (1999). Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients. Eur. J. Neurosci. 11, 3983-3994.
18. Ferbert, A., Priori, A., Rothwell, J. C., Day, B. L., Colebatch, J. G., and Marsden, C. D. (1992). Interhemispheric inhibition of the human motor cortex. J. Phys. 453, 525-546.
19. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975).Mini-mental state A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198.
20. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711.
21. Glover, G. H., Li, T. Q., and Ress, D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 44, 162-167.
22. Hagmann, P., Thiran, J. P., Jonasson, L., Vandergheynst, P., Clarke, S., Maeder, P., and Meuli, R. (2003). DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection. Neuroimage 19, 545-554.
23. Harris, L. J. (1990). "Cultural influences on handedness: historical and contemporary theory and evidence," in Left-Handedness: Behavioral Implications and Anomalies, ed. S. Coren (Amsterdam, North-Holland: Elsevier) 195-258.
24. Hayes, A., and Krippendorff, K. (2007). Answering the call for a standard reliability measure for coding data. Commun. Methods Meas. 1, 77-89.
25. Head, D., Buckner, R. L., Shimony, J. S., Williams, L. E., Akbudak, E., Conturo, T. E., McAvoy, M., Morris, J. C., and Snyder, A. Z. (2004). Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb. Cortex 14, 410-423.
26. Heuninckx, S., Wenderoth, N., Debaere, F., Peeters, R., and Swinnen, S. P. (2005). Neural basis of aging: the penetration of cognition into action control. J. Neurosci. 25, 6787-6796.
27. Heuninckx, S., Wenderoth, N., and Swinnen, S. P. (2008). Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J. Neurosci. 28, 91-99.
28. Hofer, S., and Frahm, J. (2006). Topography of the human corpus callosum revisited-comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 32, 989-994.
29. Hoppner, J., Kunesch, E., Buchmann, J., Hess, A., Grossmann, A., and Benecke, R. (1999). Demyelination and axonal degeneration in corpus callosum assessed by analysis of transcallosally mediated inhibition in multiple sclerosis. Clin. Neurophysiol. 110, 748-756.
30. Hutchinson, S., Kobayashi, M., Horkan, C. M., Pascual-Leone, A., Alexander, M. P., and Schlaug, G. (2002). Age-related differences in movement representation. Neuroimage 17, 1720-1728.
31. Johnston, J. M., Vaishnavi, S. N., Smyth, M. D., Zhang, D. Y., He, B. J., Zempel, J. M., Shimony, J. S., Snyder, A. Z., and Raichle, M. E. (2008). Loss of resting interhemispheric functional connectivity after complete section of the corpus callosum. J. Neurosci. 28, 6453-6458.
32. Lenzi, D., Conte, A., Mainero, C., Frasca, V., Fubelli, F., Totaro, P., Cararnia, F., Inghilleri, M., Pozzilli, C., and Pantano, P. (2007). Effect of corpus callosum damage on ipsilateral motor activation in patients with multiple sclerosis: a functional and anatomical study. Hum. Brain Mapp. 28, 636-644.
33. Leocani, L., Cohen, L. G., Wassermann, E. M., Ikoma, K., and Hallett, M. (2000). Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123, 1161-1173.
34. Li, S. C., Lindenberger, U., and Sikstrom, S. (2001). Aging cognition: from neuromodulation to representation. Trends Cogn. Sci. (Regul. Ed.) 5, 479-486.
35. Li, S. C., and Sikstrom, S. (2002). Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neurosci. Biobehav. Rev. 26, 795-808.
36. Liepert, J., Classen, J., Cohen, L. G., and Hallett, M. (1998). Task-dependent changes of intracortical inhibition. Exp. Brain Res. 118, 421-426.
37. Logan, J. M., Sanders, A. L., Snyder, A. Z., Morris, J. C., and Buckner, R. L. (2002). Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron 33, 827-840.
38. Lowe, M. J., Beall, E. B., Sakaie, K. E., Koenig, K. A., Stone, L., Marrie, R. A., and Phillips, M. D. (2008). Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum. Brain Mapp. 29, 818-827.
39. Lowe, M. J., Mock, B. J., and Sorenson, J. A. (1998). Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. NeuroImage 7, 119-132.
40. Madden, D. J., Turkington, T. G., Provenzale, J. M., Denny, L. L., Hawk, T. C., Gottlob, L. R., and Coleman, R. E. (1999). Adult age differences in the functional neuroanatomy of verbal recognition memory. Hum. Brain Mapp. 7, 115-135.
41. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239.
42. Mattay, V. S., Fera, F., Tessitore, A., Hariri, A. R., Das, S., Callicott, J. H., and Weinberger, D. R. (2002). Neurophysiological correlates of age-related changes in human motor function. Neurology 58, 630-635.
43. Mattis, S. (1976). "Mental status examination for organic mental syndrome in the elderly patient," in Geriatric Psychiatry, eds L. Bellak and T. B. Karasu (New York: Grune & Stratton), 77-121.
44. Mazziotta, J. C., Toga, A. W., Evans, A., Fox, P., and Lancaster, J. (1995). A probabilistic atlas of the human brain-theory and rationale for its development. Neuroimage 2, 89-101.
45. Murase, N., Duque, J., Mazzocchio, R., and Cohen, L. G. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 55, 400-409.
46. Muller-Oehring, E. M., Schulte, T., Raassi, C., Pfefferbaum, A., and Sullivan, E. V. (2007). Local-global interference is modulated by age, sex and anterior corpus callosum size. Brain Res. 1142, 189-205.
47. Netz, J. (1999). Asymmetry in transcallosal inhibition. Electroencephalogr. Clin. Neurophysiol. Suppl. 51, 137-144.
48. Nudo, R. J., Milliken, G. W., Jenkins, W. M., and Merzenich, M. M. (1996). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16, 2, 785-807.
49. Obleser, J., Wise, R. J. S., Dresner, M. A., and Scott, S. K. (2007). Functional integration across brain regions improves speech perception under adverse listening conditions. J. Neurosci. 27, 2283-2289.
50. Oldfield, R. C. (1971). Assessment and analysis of handedness-Edinburgh inventory. Neuropsychologia 9, 97-113.
51. Ota, M., Obata, T., Akine, Y., Ito, H., Ikehira, H., Asada, T., and Suhara, T. (2006). Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage 31, 1445-1452.
52. Pantano, P., Mainero, C., and Caramia, F. (2006). Functional brain reorganization in multiple sclerosis: evidence from fMRI studies. J. Neuroimaging 16, 104-114.
53. Paxton, J. L., Barch, D. M., Racine, C. A., and Braver, T. S. (2008). Cognitive control, goal maintenance, and prefrontal function in healthy aging. Cereb. Cortex 18, 1010-1028.
54. Peltier, S. J., LaConte, S. M., Niyazov, D. M., Liu, J. Z., Sahgal, V., Yue, G. H., and Hu, X. P. (2005). Reductions in interhemispheric motor cortex functional connectivity after muscle fatigue. Brain Res. 1057, 10-16.
55. Persson, J., Nyberg, L., Lind, J., Larsson, A., Nilsson, L. G., Ingvar, M., and Buckner, R. L. (2006). Structure-function correlates of cognitive decline in aging. Cereb. Cortex 16, 907-915.
56. Porac, C. (1993). Are age trends in adult hand preference best explained by developmental shifts orgenerational-differences. Can. J. Exp. Psychol. Revue Canadienne De Psychologie Experimentale 47, 697-713.
57. Putnam, M. C., Wig, G. S., Grafton, S. T., Kelley, W. M., and Gazzaniga, M. S. (2008). Structural organization of the corpus callosum predicts the extent and impact of cortical activity in the nondominant hemisphere. J. Neurosci. 28, 2912-2918.
58. Quigley, M., Cordes, D., Turski, P., Moritz, C., Haughton, V., Seth, R., and Meyerand, M. E. (2003). Role of the corpus callosum in functional connectivity. Am. J. Neuroradiol. 24, 208-212.
59. Reuter-Lorenz, P. A., Jonides, J., Smith, E. E., Hartley, A., Miller, A., Marshuetz, C., and Koeppe, R. A. (2000). Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J. Cogn. Neurosci. 12, 174-187.
60. Reuter-Lorenz, P. A., and Lustig, C. (2005). Brain aging: reorganizing discoveries about the aging mind. Curr. Opin. Neurobiol. 15, 245-251.
61. Riecker, A., Groschel, K., Ackermann, H., Steinbrink, C., Witte, O., and Kastrup A. (2006). Functional significance of age-related differences in motor activation patterns. Neuroimage 32, 1345-1354.
62. Rogers, B. P., Morgan, V. L., Newton, A. T., and Gore, J. C. (2007). Assessing functional connectivity in the human brain by fMRI. Magn. Reson. Imaging 25, 1347-1357.
63. Schmierer, K., Irlbacher, K., Grosse, P., Roricht, S., and Meyer, B. U. (2002). Correlates of disability in multiple sclerosis detected by transcranial magnetic stimulation. Neurology 59, 1218-1224.
64. Seidler, R. D., Bernard, J. A., Burutolu, T. B., Fling, B. W., Gordon, M. T., Gwin, J. T., Kwak, Y., and Lipps, D. B. (2010). Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 34, 721-733.
65. Seidler, R. D., Noll, D. C., and Thiers, G. (2004). Feedforward and feedback processes in motor control. Neuroimage 22, 1775-1783.
66. Smith, E. E., Geva, A., Jonides, J., Miller, A., Reuter-Lorenz, P., and Koeppe, R. A. (2001). The neural basis of task-switching in working memory: effects of performance and aging. Proc. Natl. Acad. Sci. USA 98, 2095-2100.
67. Sohn, Y. H., Jung, H. Y., Kaelin-Lang, A., and Hallett, M. (2003). Excitability of the ipsilateral motor cortex during phasic voluntary hand movement. Exp. Brain Res. 148, 176-185.
68. Stancak, A., Lucking, C. H., and Kristeva-Feige, R. (2000). Lateralization of movement-related potentials and the size of corpus callosum. Neuroreport 11, 329-332.
69. Stancak, A., and C. H. Lucking, et al. (2002). The size of corpus callosum and functional connectivities of cortical regions in finger and shoulder movements. Brain Res. Cogn. Brain Res. 13, 61-74.
70. Stancak, A., Cohen, E., Seidler, R. D., Duong, T. Q., and Kim, S. (2003). The size of corpus callosum and the functional activation of motor cortical areas in bimanual and unimanual movements. Cereb. Cortex 13, 475-485.
71. Stancak, A., and J. Svoboda, et al. (2003b). Desynchronization of cortical rhythms following cutaneous stimulation: effects of stimulus repetition and intensity, and of the size of corpus callosurn. Clin. Neurophysiol. 114, 1936-1947.
72. Stinear, J. W., and Byblow, W. D. (2002). Disinhibition in the human motor cortex is enhanced by synchronous upper limb movements. J. Physiol. 543, 307-316.
73. Sullivan, E. V., Pfefferbaum, A., Adalsteinsson, E., Swan, G. E., and Carmelli, D. (2002). Differential rates of regional brain change in callosal and ventricular size: a 4-year longitudinal MRI study of elderly men. Cereb. Cortex 12, 438-445.
74. Talelli, P., Waddingham, W., Ewas, A., Rothwell, J. C., and Ward, N. S. (2008a). The effect of age on task-related modulation of interhemispheric balance. Exp. Brain Res. 186, 59-66.
75. Talelli, P., Ewas, A., Waddingham, W., Rothwell, J. C., and Ward, N. S. (2008b). Neural correlates of age-related changes in cortical neurophysiology. Neuroimage 40, 1772-1781.
76. Taniwaki, T., Okayama, A., Yoshiura, T., Togao, O., Nakamura, Y., Yamasaki, T., Ogata, K., Shigeto, H., Ohyagi, Y., Kira, J., and Tobimatsu, S. (2007). Age-related alterations of the functional interactions within the basal ganglia and cerebellar motor loops in vivo. Neuroimage 36, 1263-1276.
77. Teasdale, N., Bard, C., Fleury, M., Young, D. E., and Proteau, L. (1993). Determining movement onsets from temporal series. J. Mot. Behav. 25, 97-106.
78. Tisserand, D. J., and Jolles, J. (2003). On the involvement of prefrontal networks in cognitive ageing. Cortex 39, 1107-1128.
79. Vercauteren, K., Pleysier, T., Van Belle, L., Swinnen, S. P., and Wenderoth, N. (2008). Unimanual muscle activation increases interhemispheric inhibition from the active to the resting hemisphere. Neurosci. Letters 445, 209-213.
80. Vernooij, M. W., de Groot, M., van der Lugt, A., Ikram, M. A., Krestin, G. P., Hofman, A., Niessen, W. J., and Breteler, M. M. B. (2008). White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging. Neuroimage 43, 470-477.
81. Verstynen, T., Diedrichsen, J., Albert, N., Aparicio, P., and Ivry, R. B. (2005). Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J. Neurophysiol. 93, 1209-1222.
82. Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., Zempel, J. M., Snyder, L. H., Corbetta, M., and Raichle, M. E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447, 83-86.
83. Wahl, M., Lauterbach-Soon, B., Hattingen, E., Jung, P., Singer, O., Volz, S., Klein, J. C., Steinmetz, H., and Ziemann, U. (2007). Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J. Neurosci. 27, 12132-12138.
84. Ward, N. S., and Frackowiak, R. S. J. (2003). Age-related changes in the neural correlates of motor performance. Brain 126, 873-888.
85. Wierenga, C. E., Benjamin, M., Gopinath, K., Perlstein, W. M., Leonard, C. M., Rothi, L. J. G., Conway, T., Cato, M. A., Briggs, R., and Crosson, B. (2008). Age-related changes in word retrieval: role of bilateral frontal and subcortical networks. Neurobiol. Aging 29, 436-451.
86. Winter, D. A. (1990). Biomechanics and Motor Control of Human Movements. New York: John Wiley & Sons.
87. Witelson, S. F. (1989). Hand and sex differences in the isthmus and genu of the human corpus callosum. Brain 112, 799-835.
88. Wu, T., Zang, Y. F., Wang, L., Long, X. Y., Hallett, M., Chen, Y., Li, K. C., and Chan, P. (2007). Aging influence on functional connectivity of the motor network in the resting state. Neurosci. Lett. 422, 164-168.
89. Xiong, J. H., Parsons, L. M., Gao, J. H., and Fox, P. T. (1999). Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum. Brain Mapp. 8, 151-156.
90. Yazgan, M. Y., Wexler, B. E., Kinsbourne, M., Peterson, B., and Leckman, J. F. (1995). Functional-significance of individual variations in callosal area. Neuropsychologia 33, 769-779.
91. Yousry, T. A., Schmid, U. D., Alkadhi, H., Schmidt, D., Peraud, A., Buettner, A., and Winkler, P. (1997). Localization of the motor hand area to a knob on the precentral gyrus-a new landmark. Brain 120, 141-157.