Distinct temporospatial interhemispheric interactions in the human primary and premotor cortex during movement preparation

Cerebral Cortex

Volumn 20, Issue 6, 2010, Pages 1323-1331

  Liuzzi, Gianpiero ^a   Hörniß, Vanessa ^a   Hoppe, Julia ^a   Heise, Kirstin ^a   Zimerman, Maximo ^a   Gerloff, Christian ^a   Hummel, Friedhelm C ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Interhemispheric interaction; Movement preparation; Premotor cortex; Primary motor cortex; Transcranial magnetic stimulation

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DECISION MAKING; ELECTROPHYSIOLOGY; FEMALE; FRONTAL CORTEX; HAND MOVEMENT; HUMAN; HYPOTHESIS; INDEX FINGER; INTERHEMISPHERIC TRANSFER; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; NORMAL HUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; TEMPORAL CORTEX; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; BRAIN MAPPING; DOMINANCE, CEREBRAL; EVOKED POTENTIALS, MOTOR; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; MODELS, NEUROLOGICAL; MOTOR CORTEX; MOVEMENT; NEURAL INHIBITION; NEURAL PATHWAYS; PSYCHOMOTOR PERFORMANCE; REACTION TIME; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 77952795882     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp196     Document Type: Article

References (89)

1. Andres FG, Mima T, Schulman AE, Dichgans J, Hallett M, Gerloff C. 1999. Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. Brain. 122(Pt 5):855-870.
2. Ball T, Schreiber A, Feige B, Wagner M, Lucking CH, Kristeva-Feige R. 1999. The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage. 10:682-694.
3. Bestmann S, Swayne O, Blankenburg F, Ruff CC, Haggard P, Weiskopf N, Josephs O, Driver J, Rothwell JC, Ward NS. 2008. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex. 18:1281-1291.
4. Boroojerdi B, Diefenbach K, Ferbert A. 1996. Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci. 144:160-170.
5. Boroojerdi B, Hungs M, Mull M, Topper R, Noth J. 1998. Interhemi-spheric inhibition in patients with multiple sclerosis. Electro-encephalogr Clin Neurophysiol. 109:230-237.
6. Boussaoud D, Tanne-Gariepy J, Wannier T, Rouiller EM. 2005. Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study. BMC Neurosci. 6:67.
7. Bucy PC. 1933. Representation of ipsilateral-extremities in the cerebral cortex. Science. 78:418.
8. Cardoso de Oliveira S, Gribova A, Donchin O, Bergman H, Vaadia E. 2001. Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements. Eur J Neurosci. 14:1881-1896
9. Cavina-Pratesi C, Valyear KF, Culham JC, Kohler S, Obhi SS, Marzi CA, Goodale MA. 2006. Dissociating arbitrary stimulus-response mapping from movement planning during preparatory period: evidence from event-related functional magnetic resonance imaging. J Neurosci. 26:2704-2713.
10. Chen R. 2004. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res. 154:1-10.
11. Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR, Mills K, Rosler KM, Triggs WJ, Ugawa Y, et al. 2008. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 119:504-532.
12. Chen R, Yaseen Z, Cohen LG, Hallett M. 1998. Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol. 44:317-325.
13. Cheyne D, Bakhtazad L, Gaetz W. 2006. Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event-related beamforming approach. Hum Brain Mapp. 27:213-229.
14. Cisek P, Kalaska JF. 2005. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron. 45:801-814.
15. Colebatch JG. 2007. Bereitschafts potential and movement-related potentials: origin, significance, and application in disorders of human movement. Mov Disord. 22:601-610.
16. Cui RQ, Huter D, Egkher A, Lang W, Lindinger G, Deecke L. 2000. High resolution DC-EEG mapping of the Bereitschafts potential preceding simple or complex bimanual sequential finger movement. Exp Brain Res. 134:49-57.
17. Cui RQ, Huter D, Lang W, Deecke L. 1999. Neuroimage of voluntary movement: topography of the Bereitschafts potential, a 64-channel DC current source density study. Neuroimage. 9:124-134.
18. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R. 2002. The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol (Lond). 543:317-326.
19. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC. 1999. Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp Brain Res. 124:520-524.
20. Dum RP, Strick PL. 1991. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11:667-689.
21. Dum RP, Strick PL. 2005. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci. 25:1375-1386.
22. Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. 2005. Transcallosal inhibition in chronic subcortical stroke. Neuroimage. 28:940-946.
23. Duque J, Mazzocchio R, Dambrosia J, Murase N, Olivier E, Cohen LG. 2005. Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. Cereb Cortex. 15:588-593.
24. Duque J, Murase N, Celnik P, Hummel F, Harris-Love M, Mazzocchio R, Olivier E, Cohen LG. 2007. Intermanual differences in movement-related interhemispheric inhibition. J Cogn Neurosci. 19:204-213.
25. 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. 508:565-578.
26. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. 1992. Interhemispheric inhibition of the human motor cortex. J Physiol. 453:525-546.
27. Fink GR, Frackowiak RS, Pietrzyk U, Passingham RE. 1997. Multiple nonprimary motor areas in the human cortex. J Neurophysiol. 77:2164-2174.
28. Fries P. 2005. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 10:474-480.
29. Gerloff C, Andres FG. 2002. Bimanual coordination and interhemi-spheric interaction. Acta Psychol (Amst). 110:161-186.
30. Gerloff C, Cohen LG, Floeter MK, Chen R, Corwell B, Hallett M. 1998. Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. J Physiol. 510(Pt 1):249-259.
31. Gerloff C, Grodd W, Altenmuller E, Kolb R, Nagele T, Klose U, Voigt K, Dichgans J. 1996. Coregistration of EEG and fMRI in a simple motor task. Hum Brain Mapp. 4:199-209.
32. Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, Hallett M. 1998. Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain. 121:1513-1531
33. Godschalk M, Lemon RN, Nijs HG, Kuypers HG. 1981. Behaviourofneurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp Brain Res. 44:113-116.
34. Grafton ST, Hamilton AF. 2007. Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci. 26:590-616.
35. Graziano MS, Taylor CS, Moore T. 2002. Complex movements evoked by microstimulation of precentral cortex. Neuron. 34:841-851.
36. Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR. 2008. Dynamic intra-and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage. 41:1382-1394.
37. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Kust J, Karbe H, Fink GR. 2008. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol. 63:236-246.
38. Hallett M. 1994. Movement-related cortical potentials. Electromyogr Clin Neurophysiol. 34:5-13.
39. Hallett M. 2000. Transcranial magnetic stimulation and the human brain. Nature. 406:147-150.
40. Halsband U, Matsuzaka Y, Tanji J. 1994. Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements. Neuro-sci Res. 20:149-155.
41. Harris-Love ML, Perez MA, Chen R, Cohen LG. 2007. Interhemispheric inhibition in distal and proximal arm representations in the primary motor cortex. J Neurophysiol. 97:2511-2515.
42. Hoshi E, Tanji J. 2004. Functional specialization in dorsal and ventral premotor areas. Prog Brain Res. 143:507-511.
43. Hoshi E, Tanji J. 2007. Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Curr Opin Neurobiol. 17:234-242.
44. Huang MX, Harrington DL, Paulson KM, Weisend MP, Lee RR. 2004. Temporal dynamics of ipsilateral and contralateral motor activity during voluntary finger movement. Hum Brain Mapp. 23:26-39.
45. Hummel FC, Cohen LG. 2006. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol. 5:708-712.
46. Hummel FC, Gerloff C. 2006. Chapter 15 Interregional long-range and short-range synchrony: a basis for complex sensorimotor processing. Prog Brain Res. 159:223-236.
47. Hummel FC, Steven B, Hoppe J, Heise K, Thomalla G, Cohen LG, Gerloff C. 2009. Deficient intracortical inhibition (SICI) during movement preparation after chronic stroke. Neurology. 72:1766-1772.
48. Jankowska E, Stecina K. 2007. Uncrossed actions of feline corticospinal tract neurones on lumbar interneurones evoked via ipsilaterally descending pathways. J Physiol. 580:133-147. (Pubitemid 46470649)
49. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. 2002. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA. 99:14518-14523.
50. Koch G, Franca M, Del Olmo MF, Cheeran B, Milton R, Alvarez Sauco M, Rothwell JC. 2006. Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J Neurosci. 26:7452-7459.
51. Koch G, Franca M, Mochizuki H, Marconi B, Caltagirone C, Rothwell JC. 2007. Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J Physiol. 578:551-562.
52. Kurata K, Tanji J. 1986. Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci. 6: 403-411.
53. Marconi B, Genovesio A, Giannetti S, Molinari M, Caminiti R. 2003. Callosal connections of dorso-lateral premotor cortex. Eur J Neurosci. 18:775-788.
54. Meyer-Lindenberg A, Ziemann U, Hajak G, Cohen L, Berman KF. 2002. Transitions between dynamical states of differing stability in the human brain. Proc Natl Acad Sci USA. 99:10948-10953.
55. Meyer BU, Roricht S, Woiciechowsky C. 1998. Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices. Ann Neurol. 43:360-369.
56. Mochizuki H, Huang YZ, Rothwell JC. 2004. Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. Journal of Physiology-London. 561:331-338.
57. Murase N, Duque J, Mazzocchio R, Cohen LG. 2004. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 55:400-409.
58. Ni Z, Gunraj C, Nelson AJ, Yeh IJ, Castillo G, Hoque T, Chen R. 2009. Two phases of interhemispheric inhibition between motor related cortical areas and the primary motor cortex in human. Cereb Cortex. 7:1654-1665.
59. O'Shea J, Johansen-Berg H, Trief D, Gobel S, Rushworth MF. 2007. Functionally specific reorganization in human premotor cortex. Neuron. 54:479-490.
60. O'Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MF. 2007. Functional specificity of human premotor-motor cortical interactions during action selection. Eur J Neurosci. 26:2085-2095.
61. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 9:97-113.
62. Pascual-Leone A, Walsh V, Rothwell J. 2000. Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol. 10:232-237.
63. Pedersen JR, Johannsen P, Bak CK, Kofoed B, Saermark K, Gjedde A. 1998. Origin of human motor readiness field linked to left middle frontal gyrus by MEG and PET. Neuroimage. 8:214-220.
64. Perez MA, Cohen LG. 2008. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci. 28:5631-5640.
65. Picard N, Strick PL. 1996. Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex. 6:342-353.
66. Picard N, Strick PL. 2001. Imaging the premotor areas. Curr Opin Neurobiol. 11:663-672.
67. ReisJ,Swayne OB, VandermeerenY,CamusM,DimyanMA, Harris-Love M, Perez MA, Ragert P, Rothwell JC, Cohen LG. 2008. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol. 586:325-351.
68. Rektor I, Sochurkova D, Bockova M. 2006. Intracerebral ERD/ERS in voluntary movement and in cognitive visuomotor task. Prog Brain Res. 159:311-330.
69. Rizzo V, Siebner HS, Morgante F, Mastroeni C, Girlanda P, Quartarone A. 2009. Paired associative stimulation of left and right human motor cortex shapes interhemispheric motor inhibition based on a hebbian mechanism. Cereb Cortex. 4:907-915.
70. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, et al. 1994. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 91:79-92.
71. 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. 102:227-243.
72. Rushworth MF, Johansen-Berg H, Gobel SM, Devlin JT. 2003. The left parietal and premotor cortices: motor attention and selection. Neuroimage. 20(Suppl. 1):S89-S100.
73. Schluter ND, Rushworth MF, Mills KR, Passingham RE. 1999. Signal-, set-, and movement-related activity in the human premotor cortex. Neuropsychologia. 37:233-243.
74. Schluter ND, Rushworth MF, 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.
75. Scott SH, Sergio LE, Kalaska JF. 1997. Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol. 78:2413-2426.
76. Serrien DJ. 2008. Coordination constraints during bimanual versus unimanual performance conditions. Neuropsychologia. 46:419-425.
77. Serrien DJ, Ivry RB, Swinnen SP. 2006. Dynamics of hemispheric specialization and integration in the context of motor control. Nat Rev Neurosci. 7:160-166.
78. Stecina K, Jankowska E, Cabaj A, Pettersson LG, Bannatyne BA, Maxwell DJ. 2008. Premotor interneurones contributing to actions of feline pyramidal tract neurones on ipsilateral hindlimb moto-neurones. J Physiol. 586:557-574.
79. Sterr A, Dean P. 2008. Neural correlates of movement preparation in healthy ageing. Eur J Neurosci. 27:254-260.
80. Swinnen SP. 2002. Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci. 3: 348-359.
81. Swinnen SP, Wenderoth N. 2004. Two hands, one brain: cognitive neuroscience of bimanual skill. Trends Cogn Sci. 8:18-25.
82. Tanji J, Okano K, Sato KC. 1988. Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol. 60:325-343.
83. Urbano A, Babiloni C, Onorati P, Babiloni F. 1996. Human cortical activity related to unilateral movements. A high resolution EEG study. Neuroreport. 8:203-206.
84. 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 microstruc-ture and function. J Neurosci. 27:12132-12138.
85. Walsh V, Cowey A. 2000. Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci. 1:73-79.
86. Weinrich M, Wise SP. 1982. The premotor cortex of the monkey. J Neurosci. 2:1329-1345.
87. Weinrich M, Wise SP, Mauritz KH. 1984. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain. 107(Pt 2): 385-414.
88. Wise SP. 1985. The primate premotor cortex: past, present, and preparatory. Annu Rev Neurosci. 8:1-19.
89. Wise SP, Boussaoud D, Johnson PB, Caminiti R. 1997. Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci. 20:25-42.