Fundamental differences in callosal structure, neurophysiologic function, and bimanual control in young and older adults

Cerebral Cortex

Volumn 22, Issue 11, 2012, Pages 2643-2652

  Fling, B W ^a,b   Seidler, R D ^a,b,c  

^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; bimanual; corpus callosum; diffusion tensor imaging; transcranial magnetic stimulation

Indexed keywords

AGED; AGING; ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; HAND MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; MOVEMENT (PHYSIOLOGY); NEUROIMAGING; NEUROPHYSIOLOGY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TASK PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION;

ADOLESCENT; ADULT; AGED; AGING; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MOTOR CORTEX; MOTOR SKILLS; NERVE FIBERS; NERVOUS SYSTEM; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; PHYSICAL EXERTION; PSYCHOMOTOR PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84867313919     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr349     Document Type: Article

References (56)

1. Aboitiz F. 1992. Brain connections: interhemispheric fiber systems and anatomical brain asymmetries in humans. Biol Res. 25:51-61. (Pubitemid 24231870)
2. Bangert AS, Reuter-Lorenz PA, Walsh CM, Schachter AB, Seidler RD. 2009. Bimanual coordination and aging: neurobehavioral implications. Neuropsychologia. 48:1165-1170.
3. Bartels C, Mertens N, Hofer S, Merboldt KD, Dietrich J, Frahm J, Ehrenreich H. 2008. Callosal dysfunction in amyotrophic lateral sclerosis correlates with diffusion tensor imaging of the central motor system. Neuromuscul Disord. 18(5):398-407.
4. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. 2000. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 44:625-632.
5. Basser PJ, Pierpaoli C. 1996. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 111:209-219. (Pubitemid 126758682)
6. Bloom JS, Hynd GW. 2005. The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol Rev. 15:59-71. (Pubitemid 41428109)
7. Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M. 2008. Callosal contributions to simultaneous bimanual finger movements. J Neurosci. 28(12):3227-3233. (Pubitemid 351442291)
8. Boroojerdi B, Hungs M, Mull M, Topper R, Noth J. 1998. Interhemispheric inhibition in patients with multiple sclerosis. Electroencephalogr Clin Neurophysiol. 109:230-237.
9. Carey JR, Allison JD, Mundale MO. 1983. Electromyographic study of muscular overflow during precision handgrip. Phys Ther. 63:505-511. (Pubitemid 13119019)
10. Carson RG. 2005. Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Brain Res Rev. 49:641-662. (Pubitemid 41548449)
11. Carson RG, Riek S, Mackey DC, Meichenbaum DP, Willms K, Forner M, Byblow WD. 2004. Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb. J Physiol. 560:929-940. (Pubitemid 39530129)
12. Chen R, Yung D, Li JY. 2003. Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol. 89:1256-1264. (Pubitemid 36323973)
13. De Gennaro L, Cristiani R, Bertini M, Curcio G, Ferrara M, Fratello F, Romei V, Rossini PM. 2004. Handedness is mainly associated with an asymmetry of corticospinal excitability and not of transcallosal inhibition. Clin Neurophysiol. 115(6):1305-1312. (Pubitemid 38596714)
14. Fang PC, Stepniewska I, Kaas JH. 2008. Corpus callosum connections of subdivisions of motor and premotor cortex, and frontal eye field in a prosimian primate, Otolemur garnetti. J Comp Neurol. 508(4):565-578. (Pubitemid 351656385)
15. Fling BW, Benson BL, Seidler RD. Forthcoming 2011. Transcallosal sensorimotor fiber tract structure-function relationships. Hum Brain Mapp. doi: 10.1002/hbm.21437.
16. Fling BW, Chapekis M, Reuter-Lorenz PA, Anguera J, Bo J, Langan J, Welsh RC, Seidler RD. 2011. Age differences in callosal contributions to cognitive processes. Neuropsychologia. 49(9):2564-2569.
17. Fling BW, Walsh CM, Bangert AS, Reuter-Lorenz PA, Welsh RC, Seidler RD. 2011. Differential callosal contributions to bimanual control in young and older adults. J Cogn Neurosci. 23(9):2151-2165.
18. Fujiyama H, Garry MI, Levin O, Swinnen SP, Summers JJ. 2009. Agerelated differences in inhibitory processes during interlimb coordination. Brain Res. 1262:38-47.
19. Garvey MA, Ziemann U, Becker DA, Barker CA, Bartko JJ. 2001. New graphical method to measure silent periods evoked by transcranial magnetic stimulation. Clin Neurophysiol. 112:1451-1460. (Pubitemid 32673714)
20. Giovannelli F, Borgheresi A, Balestrieri F, Zaccara G, Viggiano MP, Cincotta M, Ziemann U. 2009. Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study. J Physiol. 587:5393-5410.
21. Johansen-Berg H, Della-Maggiore V, Behrens TE, Smith SM, Paus T. 2007. Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage. 36(Suppl 2):T16-T21. (Pubitemid 46702723)
22. Jung P, Ziemann U. 2006. Differences of the ipsilateral silent period in small hand muscles. Muscle Nerve. 34:431-436. (Pubitemid 44506710)
23. Kanai R, Rees G. 2011. The structural basis of inter-individual differences in human behaviour and cognition. Nat Rev Neurosci. 12(4):231-242.
24. Kern KC, Sarcona J, Montag M, Giesser BS, Sicotte NL. 2011. Corpus callosal diffusivity predicts motor impairment in relapsingremitting multiple sclerosis: a TBSS tractography study. Neuroimage. 55(3):1169-1177.
25. Langan J, Peltier SJ, Bo J, Fling BW, Welsh RC, Seidler RD. 2010. Functional implications of age differences in motor system connectivity. Front Syst Neurosci. 4:17.
26. Lenzi D, Conte A, Mainero C, Frasca V, Fubelli F, Totaro P, Caramia F, Inghilleri M, Pozzilli C, 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(7):636-44. (Pubitemid 47052617)
27. Liuzzi G, Hornib V, Zimerman M, Gerloff C, Hummel FC. 2011. Coordination of uncoupled bimanual movements by strictly timed interhemispheric connectivity. J Neurosci. 42:9111-9117.
28. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE. 2006. Threedimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage. 31:1453-1474.
29. Meyer BU, Roricht S, Grafin von Einsiedel H, Kruggel F, Weindl A. 1995. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain. 118(Pt 2):429-440.
30. Mori S, van Zijl PC. 2002. Fiber tracking: principles and strategies-a technical review. NMR Biomed. 15:468-480. (Pubitemid 36054510)
31. Muller-Oehring EM, Schulte T, Raassi C, Pfefferbaum A, Sullivan EV. 2007. Local-global interference is modulated by age, sex and anterior corpus callosum size. Brain Res. 1142:189-205. (Pubitemid 46413200)
32. Netz J. 1999. Asymmetry in transcallosal inhibition. Electroencephalogr Clin Neurophysiol Suppl. 51:137-144.
33. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
34. Peinemann A, Lehner C, Conrad B, Siebner HR. 2001. Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci Lett. 313(1-2):33-36. (Pubitemid 32973888)
35. Raz N, Ghisletta P, Rodrigue KM, Kennedy KM, Lindenberger U. 2010. Trajectories of brain aging in middle-aged and older adults: regional and individual differences. Neuroimage. 51(2):501-511.
36. Reuter-Lorenz PA, Lustig C. 2005. Brain aging: reorganizing discoveries about the aging mind. Curr Opin Neurobiol. 15(2):245-251. (Pubitemid 41569276)
37. Reuter-Lorenz PA, Stanczak L, Miller AC. 1999. Neural recruitment and cognitive aging: two hemispheres are better than one, especially as you age. Psychol Sci. 10:494-500.
38. Ridding MC, Brouwer B, Nordstrom MA. 2000. Reduced interhemispheric inhibition in musicians. Exp Brain Res. 133:249-253. (Pubitemid 30449911)
39. Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M. 1994. Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res. 102(2):227-243.
40. Sale MV, Semmler JG. 2005. Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol. 99:1483-1493. (Pubitemid 43014358)
41. Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB. 2010. Motor control and aging: links to agerelated brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 34:721-733.
42. Shim JK, Kim SW, Oh SJ, Kang N, Zatsiorsky VM, Latash ML. 2005. Plastic changes in interhemispheric inhibition with practice of a two-hand force production task: a transcranial magnetic stimulation study. Neurosci Lett. 374:104-108. (Pubitemid 40092205)
43. Sohn YH, Jung HY, Kaelin-Lang A, Hallett M. 2003. Excitability of the ipsilateral motor cortex during phasic voluntary hand movement. Exp Brain Res. 148(2):176-185. (Pubitemid 36057003)
44. Stancak A, Cohen ER, Seidler RD, Duong TQ, Kim SG. 2003. The size of corpus callosum correlates with functional activation of medial motor cortical areas in bimanual and unimanual movements. Cereb Cortex. 13(5):475-485. (Pubitemid 36460874)
45. Sullivan EV, Rohlfing T, Pfefferbaum A. 2010. Longitudinal study of callosal microstructure in the normal adult aging brain using quantitative DTI fiber tracking. Dev Neuropsychol. 35:233-256.
46. Swinnen SP. 2002. Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci. 3:350-361. (Pubitemid 135706632)
47. Talelli P, Ewas A, Waddingham W, Rothwell JC, Ward NS. 2008. Neural correlates of age-related changes in cortical neurophysiology. Neuroimage. 40:1772-1781.
48. Tournier JD, Mori S, Leemans A. 2011. Diffusion tensor imaging and beyond. Magn Reson Med. 65(6):1532-1556.
49. Triggs WJ, Calvanio R, Macdonell RA, Cros D, Chiappa KH. 1994. Physiological motor asymmetry in human handedness: evidence from transcranial magnetic stimulation. Brain Res. 636:270-276. (Pubitemid 24044644)
50. Vaillancourt DE, Newell KM. 2003. Aging and the time and frequency structure of force output variability. J Appl Physiol. 94:903-912. (Pubitemid 36232002)
51. van den Berg FE, Swinnen SP, Wenderoth N. 2010. Hemispheric asymmetries of the premotor cortex are task specific as revealed by disruptive TMS during bimanual versus unimanual movements. Cereb Cortex. 20(12):2842-2851.
52. Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, Volz S, Klein JC, Steinmetz H, Ziemann U. 2007. Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci. 27:12132-12138. (Pubitemid 350085469)
53. Ward NS, Frackowiak RS. 2003. Age-related changes in the neural correlates of motor performance. Brain. 126:873-888. (Pubitemid 36372986)
54. Ward NS, Swayne OB, Newton JM. 2008. Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol Aging. 29(9):1434-1446. (Pubitemid 351970606)
55. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. 1999. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 517:591-597. (Pubitemid 29296371)
56. Zuo X, Kelly C, DiMartino A, Mennes M, Margulies DS, Bangaru S, Grzadzinski R, Evans AC, Zang Y, Castellanos FX, et al. 2010. Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci. 30(45):15034-15043.