Skip to main content
Top
Published in: Experimental Brain Research 4/2006

01-11-2006 | Research Article

Role of the right dorsal premotor cortex in “physiological” mirror EMG activity

Authors: F. Giovannelli, A. Borgheresi, F. Balestrieri, A. Ragazzoni, G. Zaccara, M. Cincotta, U. Ziemann

Published in: Experimental Brain Research | Issue 4/2006

Login to get access

Abstract

A distributed cortical network enables the lateralization of intended unimanual movements, i.e., the transformation from a default mirror movement to a unimanual movement. Little is known about the exact functional organization of this “non-mirror transformation” network. Involvement of the right dorsal premotor cortex (dPMC) was suggested because its virtual lesion by high-frequency repetitive transcranial magnetic stimulation (rTMS) increased the excitability of the left primary motor cortex (M1) during unilateral isometric contraction of a left hand muscle (Cincotta et al., Neurosci Lett 367: 189–93, 2004). However, no behavioural effects were observed in that experimental protocol. Here we tested behaviourally twelve healthy volunteers to find out whether focal disruption of the right dPMC by “off-line” One Hz rTMS (900 pulses, 115% of resting motor threshold) enhances “physiological” mirroring.This was measured by an established protocol (Mayston et al., Ann Neurol 45: 583–94, 1999) that quantifies the mirror increase in the electromyographic (EMG) level in the isometrically contracting abductor pollicis brevis (APB) muscle of one hand during brief phasic contractions performed with the APB of the other hand. Mirroring in the right APB significantly increased after real rTMS of the right dPMC. In contrast, no change in mirroring was seen with sham rTMS of the right dPMC, real rTMS of the right M1, or real rTMS of the left dPMC. These findings strongly support the hypothesis that the right dPMC is part of the non-mirror transformation cortical network.
Literature
go back to reference Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16:405–413PubMed Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16:405–413PubMed
go back to reference Bäumer T, Lange R, Liepert J, Weiller C, Siebner HR, Rothwell JC, Münchau A (2003) Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 20:550–560PubMedCrossRef Bäumer T, Lange R, Liepert J, Weiller C, Siebner HR, Rothwell JC, Münchau A (2003) Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 20:550–560PubMedCrossRef
go back to reference Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson's disease. Brain 124:2131–2146PubMedCrossRef Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson's disease. Brain 124:2131–2146PubMedCrossRef
go back to reference van den Berg C, Beek PJ, Wagenaar RC, van Wieringen PC (2000) Coordination disorders in patients with Parkinson's disease: a study of paced rhythmic forearm movements. Exp Brain Res 134:174–186PubMedCrossRef van den Berg C, Beek PJ, Wagenaar RC, van Wieringen PC (2000) Coordination disorders in patients with Parkinson's disease: a study of paced rhythmic forearm movements. Exp Brain Res 134:174–186PubMedCrossRef
go back to reference Boroojerdi B, Prager A, Muellbacher W, Cohen LG (2000) Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 54:1529–1531PubMed Boroojerdi B, Prager A, Muellbacher W, Cohen LG (2000) Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 54:1529–1531PubMed
go back to reference 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 4:918–929PubMed 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 4:918–929PubMed
go back to reference Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Brain Res Rev, May 16 [Epub ahead of print] Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Brain Res Rev, May 16 [Epub ahead of print]
go back to reference Chan JL, Ross ED (1988) Left-handed mirror writing following right anterior cerebral artery infarction: evidence for nonmirror transformation of motor programs by right supplementary motor area. Neurology 38:59–63PubMed Chan JL, Ross ED (1988) Left-handed mirror writing following right anterior cerebral artery infarction: evidence for nonmirror transformation of motor programs by right supplementary motor area. Neurology 38:59–63PubMed
go back to reference Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMed Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMed
go back to reference Cincotta M, Borgheresi A, Balzini L, Vannucchi L, Zeloni G. Ragazzoni A, Benvenuti F, Zaccara G, Ziemann U (2003) Separate ipsilateral and contralateral corticospinal projections in congenital mirror movements: neurophysiological evidence and significance for motor rehabilitation. Mov Disord 18: 1294–1300PubMedCrossRef Cincotta M, Borgheresi A, Balzini L, Vannucchi L, Zeloni G. Ragazzoni A, Benvenuti F, Zaccara G, Ziemann U (2003) Separate ipsilateral and contralateral corticospinal projections in congenital mirror movements: neurophysiological evidence and significance for motor rehabilitation. Mov Disord 18: 1294–1300PubMedCrossRef
go back to reference Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Rossi S, Ragazzoni A, Zaccara G, Ziemann U (2004) Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation. Neurosci Lett 367:189–193PubMedCrossRef Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Rossi S, Ragazzoni A, Zaccara G, Ziemann U (2004) Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation. Neurosci Lett 367:189–193PubMedCrossRef
go back to reference Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Ragazzoni A, Vanni P, Benvenuti F, Zaccara G, Ziemann U (2006a) Mechanisms underlying mirror movements in Parkinson’s disease: a transcranial magnetic stimulation study. Mov Disord, Mar 17; [Epub ahead of print] Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Ragazzoni A, Vanni P, Benvenuti F, Zaccara G, Ziemann U (2006a) Mechanisms underlying mirror movements in Parkinson’s disease: a transcranial magnetic stimulation study. Mov Disord, Mar 17; [Epub ahead of print]
go back to reference Cincotta M, Giovannelli F, Borgheresi A, Balestrieri F, Vanni P, Ragazzoni A, Zaccara G, Ziemann U (2006b) Surface electromyography shows increased mirroring in Parkinson’s disease patients without overt mirror movements. Mov Disord, May 16; [Epub ahead of print] Cincotta M, Giovannelli F, Borgheresi A, Balestrieri F, Vanni P, Ragazzoni A, Zaccara G, Ziemann U (2006b) Surface electromyography shows increased mirroring in Parkinson’s disease patients without overt mirror movements. Mov Disord, May 16; [Epub ahead of print]
go back to reference Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E (1998) Primary motor cortex is involved in bimanual coordination. Nature 395:274–278PubMedCrossRef Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E (1998) Primary motor cortex is involved in bimanual coordination. Nature 395:274–278PubMedCrossRef
go back to reference Espay AJ, Li JY, Johnston L, Chen R, Lang AE (2005) Mirror movements in Parkinsonism: evaluation of a new clinical sign. J Neurol Neurosurg Psychiatr 76:1355–1359PubMedCrossRef Espay AJ, Li JY, Johnston L, Chen R, Lang AE (2005) Mirror movements in Parkinsonism: evaluation of a new clinical sign. J Neurol Neurosurg Psychiatr 76:1355–1359PubMedCrossRef
go back to reference Gerschlager W, Siebner HR, Rothwell JC (2001) Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 57:449–455PubMed Gerschlager W, Siebner HR, Rothwell JC (2001) Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 57:449–455PubMed
go back to reference Mayston MJ, Harrison LM, Stephens JA (1999) A neurophysiological study of mirror movements in adults and children. Ann Neurol 45:583–594PubMedCrossRef Mayston MJ, Harrison LM, Stephens JA (1999) A neurophysiological study of mirror movements in adults and children. Ann Neurol 45:583–594PubMedCrossRef
go back to reference 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 99:10948–10953PubMedCrossRef 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 99:10948–10953PubMedCrossRef
go back to reference Mottaghy FM, Gangitano M, Horkan C, Chen Y, Pascual-Leone A, Schlaug G (2003) Repetitive TMS temporarily alters brain diffusion. Neurology 60:1539–1541PubMed Mottaghy FM, Gangitano M, Horkan C, Chen Y, Pascual-Leone A, Schlaug G (2003) Repetitive TMS temporarily alters brain diffusion. Neurology 60:1539–1541PubMed
go back to reference Muellbacher W, Facchini S, Boroojerdi B, Hallett M (2000) Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 111:344–349PubMedCrossRef Muellbacher W, Facchini S, Boroojerdi B, Hallett M (2000) Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 111:344–349PubMedCrossRef
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychol 9:97–113CrossRef Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychol 9:97–113CrossRef
go back to reference Reitz M, Muller K (1998) Differences between 'congenital mirror movements' and 'associated movements' in normal children: a neurophysiological case study. Neurosci Lett 256:69–72PubMedCrossRef Reitz M, Muller K (1998) Differences between 'congenital mirror movements' and 'associated movements' in normal children: a neurophysiological case study. Neurosci Lett 256:69–72PubMedCrossRef
go back to reference Rizzo V, Siebner HR, Modugno N, Pesenti A, Munchau A, Gerschlager W, Webb RM, Rothwell JC (2003) Shaping the excitability of human motor cortex with premotor rTMS. J Physiol 554:483–495PubMedCrossRef Rizzo V, Siebner HR, Modugno N, Pesenti A, Munchau A, Gerschlager W, Webb RM, Rothwell JC (2003) Shaping the excitability of human motor cortex with premotor rTMS. J Physiol 554:483–495PubMedCrossRef
go back to reference Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic´ MR, Hallett M, Katayama Y, Lücking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (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. Electroenceph Clin Neurophysiol 91:79–92PubMedCrossRef Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic´ MR, Hallett M, Katayama Y, Lücking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (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. Electroenceph Clin Neurophysiol 91:79–92PubMedCrossRef
go back to reference Sadato N, Yonekura Y, Waki A, Yamada H, Ishii Y (1997) Role of the supplementary motor area and the right premotor cortex in the coordination of bimanual finger movements. J Neurosci 17:9667–9674PubMed Sadato N, Yonekura Y, Waki A, Yamada H, Ishii Y (1997) Role of the supplementary motor area and the right premotor cortex in the coordination of bimanual finger movements. J Neurosci 17:9667–9674PubMed
go back to reference Siebner HR, Filipovic SR, Rowe JB, Cordivari C, Gerschlager W, Rothwell JC, Frackowiak RSJ, Bhatia KP (2003) Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126:2710–2725PubMedCrossRef Siebner HR, Filipovic SR, Rowe JB, Cordivari C, Gerschlager W, Rothwell JC, Frackowiak RSJ, Bhatia KP (2003) Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126:2710–2725PubMedCrossRef
go back to reference Vidal JS, Derkinderen P, Vidailhet M, Thobois S, Broussolle E (2003) Mirror movements of the non-affected hand in hemiparkinsonian patients: a reflection of ipsilateral motor overactivity? J Neurol Neurosurg Psychiatr 74:1352–1353PubMedCrossRef Vidal JS, Derkinderen P, Vidailhet M, Thobois S, Broussolle E (2003) Mirror movements of the non-affected hand in hemiparkinsonian patients: a reflection of ipsilateral motor overactivity? J Neurol Neurosurg Psychiatr 74:1352–1353PubMedCrossRef
go back to reference Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1-16PubMedCrossRef Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1-16PubMedCrossRef
Metadata
Title
Role of the right dorsal premotor cortex in “physiological” mirror EMG activity
Authors
F. Giovannelli
A. Borgheresi
F. Balestrieri
A. Ragazzoni
G. Zaccara
M. Cincotta
U. Ziemann
Publication date
01-11-2006
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 4/2006
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-006-0581-9

Other articles of this Issue 4/2006

Experimental Brain Research 4/2006 Go to the issue