Premotor-Motor Interhemispheric Inhibition Is Released during Movement Initiation in Older but Not Young Adults

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Hinder, Mark R ^a   Fujiyama, Hakuei ^a   Summers, Jeffery J ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE DISTRIBUTION; AGED; AGING; ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; BRAIN REGION; CELL INTERACTION; COGNITION; CORPUS CALLOSUM; FEMALE; HUMAN; HUMAN EXPERIMENT; INDEX FINGER; INTERHEMISPHERIC INHIBITION; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NERVE CELL NETWORK; NERVE PROJECTION; NEUROMODULATION; NORMAL HUMAN; PREMOTOR CORTEX; PYRAMIDAL TRACT; RESPONSE TIME; SIGNAL TRANSDUCTION; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL STIMULATION;

ADULT; AGED; BEHAVIOR; CEREBRUM; EVOKED POTENTIALS, MOTOR; HUMANS; INHIBITION (PSYCHOLOGY); MOTOR ACTIVITY; MOTOR CORTEX; MOVEMENT; REGRESSION ANALYSIS; TASK PERFORMANCE AND ANALYSIS; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84871310363     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052573     Document Type: Article

References (55)

1. Gazzaniga MS, (2005) Forty-five years of split-brain research and still going strong. Nature Reviews Neuroscience 6: 653-U651.
2. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, et al. (1992) Interhemispheric inhibition of the human motor cortex. Journal of Physiology-London 453: 525-546.
3. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, et al. (1999) Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Experimental Brain Research 124: 520-524.
4. Duque J, Murase N, Celnik P, Hummel F, Harris-Love M, et al. (2007) Intermanual differences in movement-related interhemispheric inhibition. Journal of Cognitive Neuroscience 19: 204-213.
5. Liuzzi G, Horniss V, Hoppe J, Heise K, Zimerman M, et al. (2010) Distinct Temporospatial Interhemispheric Interactions in the Human Primary and Premotor Cortex during Movement Preparation. Cerebral Cortex 20: 1323-1331.
6. Liuzzi G, Horniss V, Zimerman M, Gerloff C, Hummel FC, (2011) Coordination of Uncoupled Bimanual Movements by Strictly Timed Interhemispheric Connectivity. Journal of Neuroscience 31: 9111-9117.
7. Hinder MR, Schmidt MW, Garry MI, Summers JJ, (2010) Unilateral contractions modulate interhemispheric inhibition most strongly and most adaptively in the homologous muscle of the contralateral limb. Experimental Brain Research 205: 423-433.
8. Schambra HM, Sawaki L, Cohen LG, (2003) Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clinical Neurophysiology 114: 130-133.
9. Carson RG, (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Research Reviews 49: 641-662.
10. Riehle A, Requin J, (1989) Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. Journal of Neurophysiology 61: 534-549.
11. Cisek P, Crammond DJ, Kalaska JF, (2003) Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. Journal of Neurophysiology 89: 922-942.
12. Crammond DJ, Kalaska JF, (1996) Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task. Experimental Brain Research 108: 45-61.
13. Schluter ND, Rushworth MFS, Passingham RE, Mills KR, (1998) Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements- A study using transcranial magnetic stimulation. Brain 121: 785-799.
14. Mochizuki H, Franca M, Huang YZ, Rothwell J, (2005) The role of dorsal premotor area in reaction task: comparing the "virtual lesion" effect of paired pulse or theta burst transcranial magnetic stimulation. Experimental Brain Research 167: 414-421.
15. Bäumer T, Bock F, Koch G, Lange R, Rothwell JC, et al. (2006) Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. Journal of Physiology 572: 857-868.
16. Koch G, Franca M, Del Olmo MF, Cheeran B, Milton R, et al. (2006) Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. Journal of Neuroscience 26: 7452-7459.
17. O'Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MFS, (2007) Functional specificity of human premotor-motor cortical interactions during action selection. European Journal of Neuroscience 26: 2085-2095.
18. Gerloff C, Cohen LG, Floeter MK, Chen R, Corwell B, et al. (1998) Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. Journal of Physiology-London 510: 249-259.
19. Hinder MR, Schmidt MW, Garry MI, Summers JJ, (2010) Unilateral contractions modulate interhemispheric inhibition most strongly and most adaptively in the homologous muscle of the contralateral limb. Experimental Brain Research 205: 423-433.
20. Perez MA, Cohen LG, (2008) Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. Journal of Neuroscience 28: 5631-5640.
21. Vercauteren K, Pleysier T, Van Belle L, Swinnen SP, Wenderoth N, (2008) Unimanual muscle activation increases interhemispheric inhibition from the active to the resting hemisphere. Neuroscience Letters 445: 209-213.
22. Chen R, Yung D, Li JY, (2003) Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. Journal of Neurophysiology 89: 1256-1264.
23. Kukaswadia S, Wagle-Shukla A, Morgante F, Gunraj C, Chen R, (2005) Interactions between long latency afferent inhibition and interhemispheric inhibitions in the human motor cortex. Journal of Physiology-London 563: 915-924.
24. Lee H, Gunraj C, Chen R, (2007) The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. Journal of Physiology-London 580: 1021-1032.
25. Ni Z, Gunraj C, Nelson AJ, Yeh IJ, Castillo G, et al. (2009) Two Phases of Interhemispheric Inhibition between Motor Related Cortical Areas and the Primary Motor Cortex in Human. Cerebral Cortex 19: 1654-1665.
26. Talelli P, Waddingham W, Ewas A, Rothwell JC, Ward NS, (2008) The effect of age on task-related modulation of interhemispheric balance. Experimental Brain Research 186: 59-66.
27. Hinder MR, (2012) Interhemispheric connectivity between distinct motor regions as a window into bimanual coordination. Journal of Neurophysiology 107: 1791-1794.
28. Ward NS, Swayne OBC, Newton JM, (2008) Age-dependent changes in the neural correlates of force modulation: An fMRI study. Neurobiology of Aging 29: 1434-1446.
29. Baliz Y, Armatas C, Farrow M, Hoy KE, Fitzgerald PB, et al. (2005) The influence of attention and age on the occurrence of mirror movements. Journal of the International Neuropsychological Society 11: 855-862.
30. Bodwell JA, Mahurin RK, Waddle S, Price R, Cramer SC, (2003) Age and features of movement influence motor overflow. Journal of the American Geriatrics Society 51: 1735-1739.
31. Hoy KE, Fitzgerald PB, Bradshaw JL, Armatas CA, Georgiou-Karistianis N, (2004) Investigating the cortical origins of motor overflow. Brain Research Reviews 46: 315-327.
32. Fujiyama H, Garry MI, Martin FH, Summers JJ, (2010) An ERP study of age-related differences in the central cost of interlimb coordination. Psychophysiology 47: 501-511.
33. Heuninckx S, Wenderoth N, Debaere F, Peeters R, Swinnen SP, (2005) Neural basis of aging: The penetration of cognition into action control. Journal of Neuroscience 25: 6787-6796.
34. Heuninckx S, Wenderoth N, Swinnen SP, (2008) Systems neuroplasticity in the aging brain: Recruiting additional neural resources for successful motor performance in elderly persons. Journal of Neuroscience 28: 91-99.
35. Oldfield RC, (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-113.
36. Hinder MR, Schmidt MW, Garry MI, Carroll TJ, Summers JJ, (2011) Absence of cross-limb transfer of performance gains following ballistic motor practice in older adults. Journal of Applied Physiology 110: 166-175.
37. Carroll TJ, Lee M, Hsu M, Sayde J, (2008) Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability. Journal of Applied Physiology 104: 1656-1664.
38. Lee M, Hinder MR, Gandevia SC, Carroll TJ, (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. Journal of Physiology-London 588: 201-212.
39. Davranche K, Tandonnet C, Burle B, Meynier C, Vidal F, et al. (2007) The dual nature of time preparation: neural activation and suppression revealed by transcranial magnetic stimulation of the motor cortex. European Journal of Neuroscience 25: 3766-3774.
40. Fujiyama H, Tandonnet C, Summers JJ, (2011) Age-related differences in corticospinal excitability during a Go/NoGo task. Psychophysiology 1148: 1448-1455.
41. Meyer-Lindenberg A, Ziemann U, Hajak G, Cohen L, Berman KF, (2002) Transitions between dynamical states of differing stability in the human brain. Proceedings of the National Academy of Sciences of the United States of America 99: 10948-10953.
42. Garry MI, Loftus A, Summers JJ, (2005) Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Experimental Brain Research 163: 118-122.
43. Hinder MR, Schmidt MW, Garry MI, Summers JJ, (2010) The effect of ballistic thumb contractions on the excitability of the ipsilateral motor cortex. Experimental Brain Research 201: 229-238.
44. Rogasch NC, Dartnall TJ, Cirillo J, Nordstrom MA, Semmler JG, (2009) Corticomotor plasticity and learning of a ballistic thumb training task are diminished in older adults. Journal of Applied Physiology 107: 1874-1883.
45. Kroeger J, Bäumer T, Jonas M, Rothwell JC, Siebner HR, et al. (2010) Charting the excitability of premotor to motor connections while withholding or initiating a selected movement. European Journal of Neuroscience 32: 1771-1779.
46. Chen R, (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Experimental Brain Research 154: 1-10.
47. Cabeza R, Anderson ND, Locantore JK, McIntosh AR, (2002) Aging gracefully: Compensatory brain activity in high-performing older adults. Neuroimage 17: 1394-1402.
48. Civardi C, Cantello R, Asselman P, Rothwell JC, (2001) Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14: 1444-1453.
49. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R, (2002) The mechanisms of interhemispheric inhibition in the human motor cortex. Journal of Physiology-London 543: 317-326.
50. Duque J, Ivry RB, (2009) Role of Corticospinal Suppression during Motor Preparation. Cerebral Cortex 19: 2013-2024.
51. Fujiyama H, Hinder MR, Schmidt MW, Tandonnet C, Garry MI, et al. (2012) Age-related differences in corticomotor excitability and inhibitory processes during a visuomotor RT task. Journal of Cognitive Neuroscience 24: 1253-1263.
52. Sinclair C, Hammond GR, (2008) Reduced intracortical inhibition during the foreperiod of a warned reaction time task. Experimental Brain Research 186: 385-392.
53. Tandonnet C, Garry MI, Summers JJ, (2010) Cortical activation during temporal preparation assessed by transcranial magnetic stimulation. Biological Psychology 85: 481-486.
54. Levin O, Cuypers K, Netz Y, Thijs H, Nuttin B, et al. (2011) Age-related differences in human corticospinal excitability during simple reaction time. Neuroscience Letters 487: 53-57.
55. Jung P, Klein JC, Wibral M, Hoechstetter K, Bliem B, et al. (2012) Spatiotemporal Dynamics of Bimanual Integration in Human Somatosensory Cortex and Their Relevance to Bimanual Object Manipulation. Journal of Neuroscience 32: 5667-5677.