State-dependent and timing-dependent bidirectional associative plasticity in the human SMA-M1 network

Journal of Neuroscience

Volumn 31, Issue 43, 2011, Pages 15376-15383

  Arai, Noritoshi ^a,b   Müller Dahlhaus, Florian ^a   Murakami, Takenobu ^a   Bliem, Barbara ^a   Lu, Ming Kuei ^a,c,d   Ugawa, Yoshikazu ^e   Ziemann, Ulf ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF TOKYO   (Japan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FEMALE; HAND MUSCLE; HUMAN; HUMAN EXPERIMENT; INTERHEMISPHERIC TRANSFER; MALE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIRED ASSOCIATE LEARNING; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; STATE DEPENDENT LEARNING; SUPPLEMENTARY MOTOR AREA; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; ANALYSIS OF VARIANCE; BIOPHYSICS; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; MOTOR CORTEX; NEURONAL PLASTICITY; REACTION TIME; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 80054914629     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2271-11.2011     Document Type: Article

References (47)

1. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2003) Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRITMS. Neuroimage 20:1685-1696.
2. Bi G, Poo M (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24:139-166.
3. Brinkman C (1984) Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4:918-929.
4. Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31:25-46.
5. Cincotta M, Borgheresi A, Jung P, Balestrieri F, Giovannelli F, Zaccara G, Ziemann U (2005) Physical interactions between induced electrical fields can have substantial effects on neuronal excitation during simultaneous TMS of two brain areas. Clin Neurophysiol 116:1733-1742.
6. 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.
7. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23-30.
8. Di Lazzaro V, Ziemann U, Lemon RN (2008) State of the art: physiology of transcranial motor cortex stimulation. Brain Stimul 1:345-362.
9. 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.
10. Fink GR, Frackowiak RS, Pietrzyk U, Passingham RE (1997) Multiple nonprimary motor areas in the human cortex. J Neurophysiol 77:2164-2174.
11. Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8:2787-2791.
12. Geyer S, Matelli M, Luppino G, Zilles K (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol (Berl) 202:443-474.
13. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Küst J, Karbe H, Fink GR (2008) Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:236-246.
14. Grefkes C, Nowak DA, Wang LE, Dafotakis M, Eickhoff SB, Fink GR (2010) Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modelling. Neuroimage 50:234-243.
15. Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci U S A 101:13335-13340.
16. Kermadi I, Liu Y, Tempini A, Calciati E, Rouiller EM (1998) Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens Mot Res 15:287-308.
17. Kim JH, Lee JM, Jo HJ, Kim SH, Lee JH, Kim ST, Seo SW, Cox RW, Na DL, Kim SI, Saad ZS (2010) Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: functional connectivitybased parcellation method. Neuroimage 49:2375-2386.
18. Koganemaru S, Mima T, Nakatsuka M, Ueki Y, Fukuyama H, Domen K (2009) Human motor associative plasticity induced by paired bihemispheric stimulation. J Physiol 587:4629-4644.
19. Liu J, Morel A, Wannier T, Rouiller EM (2002) Origins of callosal projections to the supplementary motor area (SMA): a direct comparison between pre-SMA and SMA-proper in macaque monkeys. J Comp Neurol 443:71-85.
20. Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114-140.
21. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
22. Mars RB, Klein MC, Neubert FX, Olivier E, Buch ER, Boorman ED, Rushworth MF (2009) Short-latency influence of medial frontal cortex on primary motor cortex during action selection under conflict. J Neurosci 29:6926-6931.
23. Matsumoto R, Nair DR, LaPresto E, Bingaman W, Shibasaki H, Lüders HO (2007) Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. Brain 130:181-197.
24. Matsunaga K, Maruyama A, Fujiwara T, Nakanishi R, Tsuji S, Rothwell JC (2005) Increased corticospinal excitability after 5 Hz rTMS over the human supplementary motor area. J Physiol 562:295-306.
25. Muakkassa KF, Strick PL (1979) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized 'premotor' areas. Brain Res 177:176-182.
26. Müller-Dahlhaus F, Ziemann U, Classen J (2010) Plasticity resembling spike-timing dependent synaptic plasticity: the evidence in human cortex. Front Syn Neurosci 2:1-11.
27. Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9:856-869.
28. Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MF (2010) Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc Natl Acad Sci U S A 107:13240-13245.
29. Obhi SS, Haggard P, Taylor J, Pascual-Leone A (2002) rTMS to the supplementary motor area disrupts bimanual coordination. Motor Control 6:319-332.
30. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.
31. Perez MA, Tanaka S, Wise SP, Willingham DT, Cohen LG (2008) Timespecific contribution of the supplementary motor area to intermanual transfer of procedural knowledge. J Neurosci 28:9664-9669.
32. Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342-353.
33. 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 19:907-915.
34. 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.
35. Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997) Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight shaped coil. Exp Brain Res 113:24-32.
36. Sarfeld AS, Diekhoff S, Wang LE, Liuzzi G, Uludag K, Eickhoff SB, Fink GR, Grefkes C (2011) Convergence of human brain mapping tools: Neuronavigated TMS Parameters and fMRI activity in the hand motor area. Hum Brain Mapp. Advance online publication. Retrieved April 29, 2011. doi:10.1002/hbm.21272.
37. Serrien DJ, Strens LH, Oliviero A, Brown P (2002) Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans. Neurosci Lett 328:89-92.
38. Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341-2356.
39. Steyvers M, Etoh S, Sauner D, Levin O, Siebner HR, Swinnen SP, Rothwell JC (2003) High-frequency transcranial magnetic stimulation of the supplementary motor area reduces bimanual coupling during anti-phase but not in-phase movements. Exp Brain Res 151:309-317.
40. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system. An approach to cerebral imaging. New York: Thieme.
41. Tokuno H, Nambu A (2000) 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 10:58-68.
42. Vorobiev V, Govoni P, Rizzolatti G, Matelli M, Luppino G (1998) Parcellation of human mesial area 6: cytoarchitectonic evidence for three separate areas. Eur J Neurosci 10:2199-2203.
43. Wang LE, Fink GR, Diekhoff S, Rehme AK, Eickhoff SB, Grefkes C (2011) Noradrenergic enhancement improves motor network connectivity in stroke patients. Ann Neurol 69:375-388.
44. Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J (2003) Atemporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89:2339-2345.
45. Wolters A, Schmidt A, Schramm A, Zeller D, Naumann M, Kunesch E, Benecke R, Reiners K, Classen J (2005) Timing-dependent plasticity in human primary somatosensory cortex. J Physiol 565:1039-1052.
46. Ziemann U, Rothwell JC, Ridding MC (1996) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496:873-881.
47. Zilles K, Schlaug G, Geyer S, Luppino G, Matelli M, Qü M, Schleicher A, Schormann T (1996) Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. Adv Neurol 70:29-43.