Skip to main content
Top
Published in: Journal of Neurology 8/2015

01-08-2015 | Original Communication

Normalization of sensorimotor integration by repetitive transcranial magnetic stimulation in cervical dystonia

Authors: S. Zittel, R. C. Helmich, C. Demiralay, A. Münchau, T. Bäumer

Published in: Journal of Neurology | Issue 8/2015

Login to get access

Abstract

Previous studies indicated that sensorimotor integration and plasticity of the sensorimotor system are impaired in dystonia patients. We investigated motor evoked potential amplitudes and short latency afferent inhibition to examine corticospinal excitability and cortical sensorimotor integration, before and after inhibitory 1 Hz repetitive transcranial magnetic stimulation over primary sensory and primary motor cortex in patients with cervical dystonia (n = 12). Motor evoked potentials were recorded from the right first dorsal interosseous muscle after application of unconditioned transcranial magnetic test stimuli and after previous conditioning electrical stimulation of the right index finger at short interstimulus intervals of 25, 30 and 40 ms. Results were compared to a group of healthy age-matched controls. At baseline, motor evoked potential amplitudes did not differ between groups. Short latency afferent inhibition was reduced in cervical dystonia patients compared to healthy controls. Inhibitory 1 Hz sensory cortex repetitive transcranial magnetic stimulation but not motor cortex repetitive transcranial magnetic stimulation increased motor evoked potential amplitudes in cervical dystonia patients. Additionally, both 1 Hz repetitive transcranial magnetic stimulation over primary sensory and primary motor cortex normalized short latency afferent inhibition in these patients. In healthy subjects, sensory repetitive transcranial magnetic stimulation had no influence on motor evoked potential amplitudes and short latency afferent inhibition. Plasticity of sensorimotor circuits is altered in cervical dystonia patients.
Literature
1.
go back to reference Albanese A, Bhatia K, Bressman SB, Delong MR, Fahn S, Fung VS et al (2013) Phenomenology and classification of dystonia: a consensus update. Mov Disord 28:863–873PubMedCentralCrossRefPubMed Albanese A, Bhatia K, Bressman SB, Delong MR, Fahn S, Fung VS et al (2013) Phenomenology and classification of dystonia: a consensus update. Mov Disord 28:863–873PubMedCentralCrossRefPubMed
2.
go back to reference Ruge D, Tisch S, Hariz MI, Zrinzo L, Bhatia KP, Quinn NP et al (2011) Deep brain stimulation effects in dystonia: time course of electrophysiological changes in early treatment. Mov Disord 26:1913–1921PubMedCentralCrossRefPubMed Ruge D, Tisch S, Hariz MI, Zrinzo L, Bhatia KP, Quinn NP et al (2011) Deep brain stimulation effects in dystonia: time course of electrophysiological changes in early treatment. Mov Disord 26:1913–1921PubMedCentralCrossRefPubMed
3.
go back to reference Quartarone A, Rizzo V, Terranova C, Morgante F, Schneider S, Ibrahim N et al (2009) Abnormal sensorimotor plasticity in organic but not in psychogenic dystonia. Brain 132:2871–2877PubMedCentralCrossRefPubMed Quartarone A, Rizzo V, Terranova C, Morgante F, Schneider S, Ibrahim N et al (2009) Abnormal sensorimotor plasticity in organic but not in psychogenic dystonia. Brain 132:2871–2877PubMedCentralCrossRefPubMed
4.
go back to reference Beck S, Richardson SP, Shamim EA, Dang N, Schubert M, Hallett M (2008) Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia. J Neurosci 28:10363–10369CrossRefPubMed Beck S, Richardson SP, Shamim EA, Dang N, Schubert M, Hallett M (2008) Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia. J Neurosci 28:10363–10369CrossRefPubMed
5.
go back to reference Benninger DH, Lomarev M, Lopez G, Pal N, Luckenbaugh DA, Hallett M (2011) Transcranial direct current stimulation for the treatment of focal hand dystonia. Mov Dis 26:1698–1702CrossRef Benninger DH, Lomarev M, Lopez G, Pal N, Luckenbaugh DA, Hallett M (2011) Transcranial direct current stimulation for the treatment of focal hand dystonia. Mov Dis 26:1698–1702CrossRef
6.
go back to reference Buttkus F, Weidenmüller M, Schneider S, Jabusch HC, Nitsche MA, Paulus W et al (2010) Failure of cathodal direct current stimulation to improve fine motor control in musician’s dystonia. Mov Dis 25:389–394CrossRef Buttkus F, Weidenmüller M, Schneider S, Jabusch HC, Nitsche MA, Paulus W et al (2010) Failure of cathodal direct current stimulation to improve fine motor control in musician’s dystonia. Mov Dis 25:389–394CrossRef
7.
go back to reference Furuya S, Nitsche MA, Paulus W, Altenmüller E (2014) Surmounting retraining limits in musicians’ dystonia by transcranial stimulation. Ann Neurol 75:700–707CrossRefPubMed Furuya S, Nitsche MA, Paulus W, Altenmüller E (2014) Surmounting retraining limits in musicians’ dystonia by transcranial stimulation. Ann Neurol 75:700–707CrossRefPubMed
8.
go back to reference Amadio S, Houdayer E, Bianchi F, Tesfaghebriel Tekle H, Urban IP et al (2014) Sensory tricks and brain excitability in cervical dystonia: a transcranial magnetic stimulation study. Mov Disord 29:1185–1188CrossRefPubMed Amadio S, Houdayer E, Bianchi F, Tesfaghebriel Tekle H, Urban IP et al (2014) Sensory tricks and brain excitability in cervical dystonia: a transcranial magnetic stimulation study. Mov Disord 29:1185–1188CrossRefPubMed
9.
go back to reference McDonnell MN, Thompson PD, Ridding MC (2007) The effect of cutaneous input on intracortical inhibition in focal task-specific dystonia. Mov Disord 22:1286–1292CrossRefPubMed McDonnell MN, Thompson PD, Ridding MC (2007) The effect of cutaneous input on intracortical inhibition in focal task-specific dystonia. Mov Disord 22:1286–1292CrossRefPubMed
10.
go back to reference Kessler KR, Ruge D, Ilic TV, Ziemann U (2005) Short latency afferent inhibition and facilitation in patients with writer’s cramp. Mov Disord 20:238–242CrossRefPubMed Kessler KR, Ruge D, Ilic TV, Ziemann U (2005) Short latency afferent inhibition and facilitation in patients with writer’s cramp. Mov Disord 20:238–242CrossRefPubMed
11.
go back to reference Tamura Y, Ueki Y, Lin P, Vorbach S, Mima T, Kakigi R et al (2009) Disordered plasticity in the primary somatosensory cortex in focal hand dystonia. Brain 132:749–755PubMedCentralCrossRefPubMed Tamura Y, Ueki Y, Lin P, Vorbach S, Mima T, Kakigi R et al (2009) Disordered plasticity in the primary somatosensory cortex in focal hand dystonia. Brain 132:749–755PubMedCentralCrossRefPubMed
12.
go back to reference Tamburin S, Manganotti P, Marzi CA, Fiaschi A, Zanette G (2002) Abnormal somatotopic arrangement of sensorimotor interactions in dystonic patients. Brain 125:2719–2730CrossRefPubMed Tamburin S, Manganotti P, Marzi CA, Fiaschi A, Zanette G (2002) Abnormal somatotopic arrangement of sensorimotor interactions in dystonic patients. Brain 125:2719–2730CrossRefPubMed
13.
go back to reference Baumer T, Demiralay C, Hidding U, Bikmullina R, Helmich RC, Wunderlich S et al (2007) Abnormal plasticity of the sensorimotor cortex to slow repetitive transcranial magnetic stimulation in patients with writer’s cramp. Mov Disord 22:81–90CrossRefPubMed Baumer T, Demiralay C, Hidding U, Bikmullina R, Helmich RC, Wunderlich S et al (2007) Abnormal plasticity of the sensorimotor cortex to slow repetitive transcranial magnetic stimulation in patients with writer’s cramp. Mov Disord 22:81–90CrossRefPubMed
14.
go back to reference Muller-Dahlhaus F, Ziemann U (2015) Metaplasticity in human cortex. Neuroscientist 2014. Neuroscientist 21:185–202CrossRefPubMed Muller-Dahlhaus F, Ziemann U (2015) Metaplasticity in human cortex. Neuroscientist 2014. Neuroscientist 21:185–202CrossRefPubMed
15.
go back to reference Murakami T, Muller-Dahlhaus F, Lu MK, Ziemann U (2012) Homeostatic metaplasticity of corticospinal excitatory and intracortical inhibitory neural circuits in human motor cortex. J Physiol 590:5765–5781PubMedCentralCrossRefPubMed Murakami T, Muller-Dahlhaus F, Lu MK, Ziemann U (2012) Homeostatic metaplasticity of corticospinal excitatory and intracortical inhibitory neural circuits in human motor cortex. J Physiol 590:5765–5781PubMedCentralCrossRefPubMed
16.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed
18.
19.
go back to reference Baumer T, Lange R, Liepert J, Weiller C, Siebner HR, Rothwell JC et al (2003) Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 20:550–560CrossRefPubMed Baumer T, Lange R, Liepert J, Weiller C, Siebner HR, Rothwell JC et al (2003) Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 20:550–560CrossRefPubMed
20.
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 108:1–16CrossRefPubMed 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 108:1–16CrossRefPubMed
21.
go back to reference Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403CrossRefPubMed Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403CrossRefPubMed
22.
go back to reference Siebner HR, Auer C, Conrad B (1999) Abnormal increase in the corticomotor output to the affected hand during repetitive transcranial magnetic stimulation of the primary motor cortex in patients with writer’s cramp. Neurosci Lett 262:133–136CrossRefPubMed Siebner HR, Auer C, Conrad B (1999) Abnormal increase in the corticomotor output to the affected hand during repetitive transcranial magnetic stimulation of the primary motor cortex in patients with writer’s cramp. Neurosci Lett 262:133–136CrossRefPubMed
23.
go back to reference Meunier S, Russmann H, Shamim E, Lamy JC, Hallett M (2012) Plasticity of cortical inhibition in dystonia is impaired after motor learning and paired-associative stimulation. Eur J Neurosci 35:975–986PubMedCentralCrossRefPubMed Meunier S, Russmann H, Shamim E, Lamy JC, Hallett M (2012) Plasticity of cortical inhibition in dystonia is impaired after motor learning and paired-associative stimulation. Eur J Neurosci 35:975–986PubMedCentralCrossRefPubMed
24.
go back to reference Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A et al (2003) Abnormal associative plasticity of the human motor cortex in writer’s cramp. Brain 126:2586–2596CrossRefPubMed Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A et al (2003) Abnormal associative plasticity of the human motor cortex in writer’s cramp. Brain 126:2586–2596CrossRefPubMed
25.
go back to reference Weise D, Schramm A, Stefan K, Wolters A, Reiners K, Naumann M et al (2006) The two sides of associative plasticity in writer’s cramp. Brain 129:2709–2721CrossRefPubMed Weise D, Schramm A, Stefan K, Wolters A, Reiners K, Naumann M et al (2006) The two sides of associative plasticity in writer’s cramp. Brain 129:2709–2721CrossRefPubMed
26.
go back to reference Artola A, Brocher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69–72CrossRefPubMed Artola A, Brocher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69–72CrossRefPubMed
27.
go back to reference Bliem B, Muller-Dahlhaus JF, Dinse HR, Ziemann U (2008) Homeostatic metaplasticity in the human somatosensory cortex. J Cogn Neurosci 20:1517–1528CrossRefPubMed Bliem B, Muller-Dahlhaus JF, Dinse HR, Ziemann U (2008) Homeostatic metaplasticity in the human somatosensory cortex. J Cogn Neurosci 20:1517–1528CrossRefPubMed
28.
go back to reference Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G et al (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455–461CrossRefPubMed Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G et al (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455–461CrossRefPubMed
29.
go back to reference Di Lazzaro V, Oliviero A, Saturno E, Dileone M, Pilato F, Nardone R et al (2005) Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 564:661–668PubMedCentralCrossRefPubMed Di Lazzaro V, Oliviero A, Saturno E, Dileone M, Pilato F, Nardone R et al (2005) Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 564:661–668PubMedCentralCrossRefPubMed
30.
go back to reference Patel N, Jankovic J, Hallett M (2014) Sensory aspects of movement disorders. Lancet Neurol 13:100–112CrossRefPubMed Patel N, Jankovic J, Hallett M (2014) Sensory aspects of movement disorders. Lancet Neurol 13:100–112CrossRefPubMed
31.
go back to reference Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C (2001) Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain 124:537–545CrossRefPubMed Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C (2001) Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain 124:537–545CrossRefPubMed
32.
go back to reference Siggelkow S, Kossev A, Moll C, Dauper J, Dengler R, Rollnik JD (2002) Impaired sensorimotor integration in cervical dystonia: a study using transcranial magnetic stimulation and muscle vibration. J Clin Neurophysiol 19:232–239CrossRefPubMed Siggelkow S, Kossev A, Moll C, Dauper J, Dengler R, Rollnik JD (2002) Impaired sensorimotor integration in cervical dystonia: a study using transcranial magnetic stimulation and muscle vibration. J Clin Neurophysiol 19:232–239CrossRefPubMed
33.
go back to reference Chan J, Brin MF, Fahn S (1991) Idiopathic cervical dystonia: clinical characteristics. Mov Disord 6:119–126CrossRefPubMed Chan J, Brin MF, Fahn S (1991) Idiopathic cervical dystonia: clinical characteristics. Mov Disord 6:119–126CrossRefPubMed
Metadata
Title
Normalization of sensorimotor integration by repetitive transcranial magnetic stimulation in cervical dystonia
Authors
S. Zittel
R. C. Helmich
C. Demiralay
A. Münchau
T. Bäumer
Publication date
01-08-2015
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 8/2015
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-015-7789-1

Other articles of this Issue 8/2015

Journal of Neurology 8/2015 Go to the issue