A novel dual-site transcranial magnetic stimulation paradigm to probe fast facilitatory inputs from ipsilateral dorsal premotor cortex to primary motor cortex

NeuroImage

Volumn 62, Issue 1, 2012, Pages 500-509

  Groppa, Sergiu ^a   Werner Petroll, Nicole ^a   Münchau, Alexander ^b   Deuschl, Günther ^a   Ruschworth, Matthew F S ^c   Siebner, Hartwig R ^a,d  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d HVIDOVRE HOSPITAL   (Denmark)

Author keywords

Dorsal premotor cortex; DTI; Functional connectivity; Primary motor cortex; Structural connectivity; TMS

Indexed keywords

ADULT; ANISOTROPY; ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; EVOKED MUSCLE RESPONSE; FEMALE; HAND FUNCTION; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; MOTOR CORTEX; NORMAL HUMAN; PREMOTOR CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; REACTION TIME; SUPERIOR FRONTAL GYRUS; TRANSCRANIAL MAGNETIC STIMULATION; WHITE MATTER;

ADULT; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; LONG-TERM POTENTIATION; MALE; MOTOR CORTEX; NERVE NET; PREFRONTAL CORTEX; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84861654796     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.05.023     Document Type: Article

References (57)

1. Amassian V., Stewart M., Quirk G., Rosenthal J. Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 1987, 20:74.
2. Baumer T., Bock F., Koch G., Lange R., Rothwell J.C., Siebner H.R., Munchau A. Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. J. Physiol. 2006, 572:857-868.
3. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
4. Boorman E.D., O'Shea J., Sebastian C., Rushworth M.F.S., Johansen-Berg H. Individual differences in white-matter microstructure reflect variation in functional connectivity during choice. Curr. Biol. 2007, 17:1426-1431.
5. Cattaneo L., Voss M., Brochier T., Prabhu G., Wolpert D.M., Lemon R.N. A cortico-cortical mechanism mediating object-driven grasp in humans. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:898-903.
6. Cisek P., Kalaska J.F. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 2005, 45:801-814.
7. Civardi C., Cantello R., Asselman P., Rothwell J.C. Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 2001, 14:1444-1453.
8. Davare M., Lemon R., Olivier E. Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J. Physiol. 2008, 586:2735-2742.
9. Descoteaux M., Angelino E., Fitzgibbons S., Deriche R. Apparent diffusion coefficients from high angular resolution diffusion imaging: estimation and applications. Magn. Reson. Med. 2006, 56:395-410.
10. Di Lazzaro V., Oliviero A., Profice P., Saturno E., Pilato F., Insola A., Mazzone P., Tonali P., Rothwell J.C. Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr. Clin. Neurophysiol. 1998, 109:397-401.
11. Di Lazzaro V., Restuccia D., Oliviero A., Profice P., Ferrara L., Insola A., Mazzone P., Tonali P., Rothwell J.C. Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J. Physiol. 1998, 508(Pt 2):625-633.
12. Di Lazzaro, V., Profice, P., Ranieri, F., Capone, F., Dileone, M., Oliviero, A., Pilato, F., in press. I-wave origin and modulation. Brain Stimul. http://dx.doi.org/10.1016/j.brs.2011.07.008.
13. Dum R.P., Strick P.L. Motor areas in the frontal lobe of the primate. Physiol. Behav. 2002, 77:677-682.
14. Dum R., Strick P. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J. Neurosci. 2005, 25:1375.
15. Ferbert A., Priori A., Rothwell J., Day B., Colebatch J., Marsden C. Interhemispheric inhibition of the human motor cortex. J. Physiol. 1992, 453:525.
16. Ghosh S., Porter R. Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J. Physiol. 1988, 400:617-629.
17. Giorgio A., Watkins K.E., Chadwick M., James S., Winmill L., Douaud G., De Stefano N., Matthews P.M., Smith S.M., Johansen-Berg H., James A.C. Longitudinal changes in grey and white matter during adolescence. Neuroimage 2010, 49:94-103.
18. Grafton S.T., Fagg A.H., Arbib M.A. Dorsal premotor cortex and conditional movement selection: a PET functional mapping study. J. Neurophysiol. 1998, 79:1092-1097.
19. Groppa S., Oliviero A., Eisen A., Quartarone A., Cohen L.G., Mall V., Kaelin-Lang A., Mima T., Rossi S., Thickbroom G.W., Rossini P.M., Ziemann U., Valls-Sole J., Siebner H.R. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin. Neurophysiol. 2012, 123:858-882.
20. Groppa S., Schlaak B.H., Munchau A., Werner-Petroll N., Dunnweber J., Baumer T., van Nuenen B.F., Siebner H.R. The human dorsal premotor cortex facilitates the excitability of ipsilateral primary motor cortex via a short latency cortico-cortical route. Hum. Brain Mapp. 2012, 33:419-430.
21. Holsapple J.W., Preston J.B., Strick P.L. The origin of thalamic inputs to the "hand" representation in the primary motor cortex. J. Neurosci. 1991, 11:2644-2654.
22. Hoshi E., Tanji J. Functional specialization in dorsal and ventral premotor areas. Prog. Brain Res. 2004, 143:507-511.
23. Jones E.G., Coulter J.D., Hendry S.H. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J. Comp. Neurol. 1978, 181:291-347.
24. Julkunen P., Säisänen L., Danner N., Niskanen E., Hukkanen T., Mervaala E., Könönen M. Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 2009, 44:790-795.
25. Jung N.H., Delvendahl I., Kuhnke N.G., Hauschke D., Stolle S., Mall V. Navigated transcranial magnetic stimulation does not decrease the variability of motor-evoked potentials. Brain Stimul. 2010, 3:87-94.
26. Koch G., Franca M., Del Olmo M.F., Cheeran B., Milton R., Alvarez Sauco M., Rothwell J.C. Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J. Neurosci. 2006, 26:7452-7459.
27. Koch G., Franca M., Mochizuki H., Marconi B., Caltagirone C., Rothwell J.C. Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J. Physiol. 2007, 578:551-562.
28. Koch G., Fernandez Del Olmo M., Cheeran B., Schippling S., Caltagirone C., Driver J., Rothwell J.C. Functional interplay between posterior parietal and ipsilateral motor cortex revealed by twin-coil transcranial magnetic stimulation during reach planning toward contralateral space. J. Neurosci. 2008, 28:5944-5953.
29. Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat. Rev. Neurosci. 2003, 4:469-480.
30. Madsen K.S., Baare W.F., Skimminge A., Vestergaard M., Siebner H.R., Jernigan T.L. Brain microstructural correlates of visuospatial choice reaction time in children. Neuroimage 2011, 58:1090-1100.
31. Marconi B., Genovesio A., Giannetti S., Molinari M., Caminiti R. Callosal connections of dorso lateral premotor cortex. Eur. J. Neurosci. 2003, 18:775-788.
32. Mayka M.A., Corcos D.M., Leurgans S.E., Vaillancourt D.E. Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage 2006, 31:1453-1474.
33. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J. A probabilistic atlas of the human brain: theory and rationale for its development the international consortium for brain mapping (ICBM). Neuroimage 1995, 2:89-101.
34. Mochizuki H., Huang Y.-Z., Rothwell J.C. Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. J. Physiol. 2004, 561:331-338.
35. Mochizuki H., Franca M., Huang Y.-Z., Rothwell J.C. The role of dorsal premotor area in reaction task: comparing the "virtual lesion" effect of paired pulse or theta burst transcranial magnetic stimulation. Exp. Brain Res. 2005, 167:414-421.
36. Muakkassa K.F., Strick P.L. Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized 'premotor' areas. Brain Res. 1979, 177:176-182.
37. Novak K., de Camargo A.B., Neuwirth M., Kothbauer K., Amassian V.E., Deletis V. The refractory period of fast conducting corticospinal tract axons in man and its implications for intraoperative monitoring of motor evoked potentials. Clin. Neurophysiol. 2004, 115:1931-1941.
38. O'Shea J., Johansen-Berg H., Trief D., Gobel S., Rushworth M.F.S. Functionally specific reorganization in human premotor cortex. Neuron 2007, 54:479-490.
39. Patton H.D., Amassian V.E. Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J. Neurophysiol. 1954, 17:345-363.
40. Picard N., Strick P.L. Imaging the premotor areas. Curr. Opin. Neurobiol. 2001, 11:663-672.
41. Rizzo V., Siebner H.R., Modugno N., Pesenti A., Munchau A., Gerschlager W., Webb R.M., Rothwell J.C. Shaping the excitability of human motor cortex with premotor rTMS. J. Physiol. 2004, 554:483-495.
42. Rizzolatti G., Luppino G. The cortical motor system. Neuron 2001, 31:889-901.
43. Rossini P.M., Barker A.T., Berardelli A., Caramia M.D., Caruso G., Cracco R.Q., Dimitrijevic M.R., Hallett M., Katayama Y., Lucking C.H. 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. 1994, 91:79-92.
44. Schluter N.D., Rushworth M.F., Passingham R.E., Mills K.R. Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. Brain 1998, 121(Pt 5):785-799.
45. Schluter N.D., Krams M., Rushworth M.F., Passingham R.E. Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia 2001, 39:105-113.
46. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 2009, 44:83-98.
47. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E.J. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006, 31:1487-1505.
48. Takagi T., Nakamura M., Yamada M., Hikishima K., Momoshima S., Fujiyoshi K., Shibata S., Okano H.J., Toyama Y., Okano H. Visualization of peripheral nerve degeneration and regeneration: monitoring with diffusion tensor tractography. Neuroimage 2009, 44:884-892.
49. Takahashi M., Hackney D.B., Zhang G., Wehrli S.L., Wright A.C., O'Brien W.T., Uematsu H., Wehrli F.W., Selzer M.E. Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:16192-16196.
50. Tokimura H., Ridding M.C., Tokimura Y., Amassian V.E., Rothwell J.C. Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. Electroencephalogr. Clin. Neurophysiol. 1996, 101:263-272.
51. Tokuno H., Nambu A. Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb. Cortex 2000, 10:58-68.
52. Tuch D.S., Reese T.G., Wiegell M.R., Wedeen V.J. Diffusion MRI of complex neural architecture. Neuron 2003, 40:885-895.
53. Tuch D.S., Salat D.H., Wisco J.J., Zaleta A.K., Hevelone N.D., Rosas H.D. Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12212-12217.
54. van Duinen H., Renken R., Maurits N.M., Zijdewind I. Relation between muscle and brain activity during isometric contractions of the first dorsal interosseus muscle. Hum. Brain Mapp. 2008, 29:281-299.
55. Weinrich M., Wise S.P. The premotor cortex of the monkey. J. Neurosci. 1982, 2:1329-1345.
56. Ziemann U., Rothwell J.C. I-waves in motor cortex. J. Clin. Neurophysiol. 2000, 17:397-405.
57. Ziemann U., Tergau F., Wassermann E.M., Wischer S., Hildebrandt J., Paulus W. Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J. Physiol. 1998, 511(Pt 1):181-190.