Skip to main content
Top
Published in: Translational Neurodegeneration 1/2015

Open Access 01-12-2015 | Review

Transcranial magnetic stimulation to understand pathophysiology and as potential treatment for neurodegenerative diseases

Authors: Zhen Ni, Robert Chen

Published in: Translational Neurodegeneration | Issue 1/2015

Login to get access

Abstract

Common neurodegenerative diseases include Parkinson’s disease (PD), Alzheimer’s disease (AD), amyotrophic lateral sclerosis (ALS) and Huntington’s disease (HD). Transcranial magnetic stimulation (TMS) is a noninvasive and painless method to stimulate the human brain. Single- and paired-pulse TMS paradigms are powerful ways to study the pathophysiological mechanisms of neurodegenerative diseases. Motor evoked potential studied with single-pulse TMS is increased in PD, AD and ALS, but is decreased in HD. Changes in motor cortical excitability in neurodegenerative diseases may be related to functional deficits in cortical circuits or to compensatory mechanisms. Reduction or even absence of short interval intracortical inhibition induced by paired-pulse TMS is common in neurodegenerative diseases, suggesting that there are functional impairments of inhibitory cortical circuits. Decreased short latency afferent inhibition in AD, PD and HD may be related to the cortical cholinergic deficits in these conditions. Cortical plasticity tested by paired associative stimulation or theta burst stimulation is impaired in PD, AD and HD. Repetitive TMS (rTMS) refers to the application of trains of regularly repeating TMS pulses. High-frequency facilitatory rTMS may improve motor symptoms in PD patients whereas low-frequency inhibitory stimulation is a potential treatment for levodopa induced dyskinesia. rTMS delivered both to the left and right dorsolateral prefrontal cortex improves memory in AD patients. Supplementary motor cortical stimulation in low frequency may be useful for HD patients. However, the effects of treatment with multiple sessions of rTMS for neurodegenerative diseases need to be tested in large, sham-controlled studies in the future before they can be adopted for routine clinical practice.
Literature
1.
3.
go back to reference Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, et al. Amyotrophic lateral sclerosis. Lancet. 2011;377:942–55.CrossRefPubMed Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, et al. Amyotrophic lateral sclerosis. Lancet. 2011;377:942–55.CrossRefPubMed
4.
go back to reference The Huntington's Disease Collaborative Research Group (MacDonald ME, et al.) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 1993. 72:971–83. The Huntington's Disease Collaborative Research Group (MacDonald ME, et al.) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 1993. 72:971–83.
5.
go back to reference Barker AT, Jalinous R, Freeston IL. Non-invasive stimulation of the human motor cortex. Lancet. 1985;II:1106–7.CrossRef Barker AT, Jalinous R, Freeston IL. Non-invasive stimulation of the human motor cortex. Lancet. 1985;II:1106–7.CrossRef
6.
go back to reference Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2008;119:504–32.CrossRefPubMed Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2008;119:504–32.CrossRefPubMed
8.
go back to reference Ni Z, Charab S, Gunraj C, Nelson AJ, Udupa K, Yeh IJ, et al. Transcranial magnetic stimulation in different current directions activates separate cortical circuits. J Neurophysiol. 2011;105:749–56.CrossRefPubMed Ni Z, Charab S, Gunraj C, Nelson AJ, Udupa K, Yeh IJ, et al. Transcranial magnetic stimulation in different current directions activates separate cortical circuits. J Neurophysiol. 2011;105:749–56.CrossRefPubMed
9.
go back to reference Wassermann EM. Risk and safety in repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalography and Clinical Neurophysiology. 1998;108:1–16.CrossRefPubMed Wassermann EM. Risk and safety in repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalography and Clinical Neurophysiology. 1998;108:1–16.CrossRefPubMed
10.
go back to reference Ridding MC, Rothwell JC. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci. 2007;8:559–67.CrossRefPubMed Ridding MC, Rothwell JC. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci. 2007;8:559–67.CrossRefPubMed
11.
go back to reference Ni Z, Bahl N, Gunraj C, Mazzella F, Chen R. Increased motor cortical facilitation and decreased inhibition in Parkinson disease. Neurology. 2013;80:1746–53.PubMedCentralCrossRefPubMed Ni Z, Bahl N, Gunraj C, Mazzella F, Chen R. Increased motor cortical facilitation and decreased inhibition in Parkinson disease. Neurology. 2013;80:1746–53.PubMedCentralCrossRefPubMed
12.
go back to reference Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol. 1995;37:181–8.CrossRefPubMed Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol. 1995;37:181–8.CrossRefPubMed
13.
go back to reference MacKinnon CD, Gilley EA, Weis-McNulty A, Simuni T. Pathways mediating abnormal intracortical inhibition in Parkinson's disease. Ann Neurol. 2005;58:516–24.CrossRefPubMed MacKinnon CD, Gilley EA, Weis-McNulty A, Simuni T. Pathways mediating abnormal intracortical inhibition in Parkinson's disease. Ann Neurol. 2005;58:516–24.CrossRefPubMed
14.
go back to reference Ellaway PH, Davey NJ, Maskill DW, Dick JP. The relation between bradykinesia and excitability of the motor cortex assessed using transcranial magnetic stimulation in normal and parkinsonian subjects. Electroencephalogr Clin Neurophysiol. 1995;97:169–78.CrossRefPubMed Ellaway PH, Davey NJ, Maskill DW, Dick JP. The relation between bradykinesia and excitability of the motor cortex assessed using transcranial magnetic stimulation in normal and parkinsonian subjects. Electroencephalogr Clin Neurophysiol. 1995;97:169–78.CrossRefPubMed
15.
go back to reference Chen R, Garg RR, Lozano AM, Lang AE. Effects of internal globus pallidus stimulation on motor cortex excitability. Neurology. 2001;56:716–23.CrossRefPubMed Chen R, Garg RR, Lozano AM, Lang AE. Effects of internal globus pallidus stimulation on motor cortex excitability. Neurology. 2001;56:716–23.CrossRefPubMed
16.
go back to reference Cunic D, Roshan L, Khan FI, Lozano AM, Lang AE, Chen R. Effects of subthalamic nucleus stimulation on motor cortex excitability in Parkinson's disease. Neurology. 2002;58:1665–72.CrossRefPubMed Cunic D, Roshan L, Khan FI, Lozano AM, Lang AE, Chen R. Effects of subthalamic nucleus stimulation on motor cortex excitability in Parkinson's disease. Neurology. 2002;58:1665–72.CrossRefPubMed
17.
go back to reference Cantello R, Gianelli M, Bettucci D, Civardi C, DeAngelis MS, Mutani R. Parkinson's disease rigidity: Magnetic motor evoked potentials in a small hand muscle. Neurology. 1991;91:1449–56.CrossRef Cantello R, Gianelli M, Bettucci D, Civardi C, DeAngelis MS, Mutani R. Parkinson's disease rigidity: Magnetic motor evoked potentials in a small hand muscle. Neurology. 1991;91:1449–56.CrossRef
18.
go back to reference Valls-Sole J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, McShane L, Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson's disease. Neurology. 1994;44:735–41.CrossRefPubMed Valls-Sole J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, McShane L, Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson's disease. Neurology. 1994;44:735–41.CrossRefPubMed
19.
go back to reference Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517:591–7.PubMedCentralCrossRefPubMed Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517:591–7.PubMedCentralCrossRefPubMed
20.
go back to reference Cantello R. Applications of transcranial magnetic stimulation in movement disorders. J Clin Neurophysiol. 2002;19:272–93.CrossRefPubMed Cantello R. Applications of transcranial magnetic stimulation in movement disorders. J Clin Neurophysiol. 2002;19:272–93.CrossRefPubMed
21.
go back to reference Lee RG, Stein RB. Resetting of tremor by mechanical perturbations: a comparison of essential tremor and parkinsonian tremor. Ann Neurol. 1981;10:523–31.CrossRefPubMed Lee RG, Stein RB. Resetting of tremor by mechanical perturbations: a comparison of essential tremor and parkinsonian tremor. Ann Neurol. 1981;10:523–31.CrossRefPubMed
22.
go back to reference Pascual-Leone A, Valls-Sole J, Toro C, Wassermann EM, Hallett M. Resetting of essential tremor and postural tremor in Parkinson's disease with transcranial magnetic stimulation. Muscle Nerve. 1994;17:800–7.CrossRefPubMed Pascual-Leone A, Valls-Sole J, Toro C, Wassermann EM, Hallett M. Resetting of essential tremor and postural tremor in Parkinson's disease with transcranial magnetic stimulation. Muscle Nerve. 1994;17:800–7.CrossRefPubMed
23.
go back to reference Ni Z, Pinto AD, Lang AE, Chen R. Involvement of the cerebellothalamocortical pathway in Parkinson disease. Ann Neurol. 2010;68:816–24.CrossRefPubMed Ni Z, Pinto AD, Lang AE, Chen R. Involvement of the cerebellothalamocortical pathway in Parkinson disease. Ann Neurol. 2010;68:816–24.CrossRefPubMed
24.
go back to reference Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471:501–19.PubMedCentralCrossRefPubMed Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471:501–19.PubMedCentralCrossRefPubMed
25.
go back to reference Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996;109:127–35.CrossRefPubMed Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996;109:127–35.CrossRefPubMed
26.
go back to reference Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol (Lond). 2002;545:153–67.CrossRef Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol (Lond). 2002;545:153–67.CrossRef
27.
go back to reference Müller-Dahlhaus F, Liu Y, Ziemann U. Inhibitory circuits and the nature of their interactions in the human motor cortex a pharmacological TMS study. J Physiol. 2008;586:495–514.PubMedCentralCrossRefPubMed Müller-Dahlhaus F, Liu Y, Ziemann U. Inhibitory circuits and the nature of their interactions in the human motor cortex a pharmacological TMS study. J Physiol. 2008;586:495–514.PubMedCentralCrossRefPubMed
28.
go back to reference Chu J, Wagle-Shukla A, Gunraj C, Lang AE, Chen R. Impaired presynaptic inhibition in the motor cortex in Parkinson disease. Neurology. 2009;72:842–9.CrossRefPubMed Chu J, Wagle-Shukla A, Gunraj C, Lang AE, Chen R. Impaired presynaptic inhibition in the motor cortex in Parkinson disease. Neurology. 2009;72:842–9.CrossRefPubMed
29.
go back to reference Kojovic M, Bologna M, Kassavetis P, Murase N, Palomar FJ, Berardelli A, et al. Functional reorganization of sensorimotor cortex in early Parkinson disease. Neurology. 2012;78:1441–8.PubMedCentralCrossRefPubMed Kojovic M, Bologna M, Kassavetis P, Murase N, Palomar FJ, Berardelli A, et al. Functional reorganization of sensorimotor cortex in early Parkinson disease. Neurology. 2012;78:1441–8.PubMedCentralCrossRefPubMed
30.
go back to reference Kojovic M, Kassavetis P, Bologna M, Parees I, Rubio-Agusti I, Beraredelli A, et al. Transcranial magnetic stimulation follow-up study in early Parkinson's disease: A decline in compensation with disease progression? Mov Disord. 2015;30:1098–106.CrossRefPubMed Kojovic M, Kassavetis P, Bologna M, Parees I, Rubio-Agusti I, Beraredelli A, et al. Transcranial magnetic stimulation follow-up study in early Parkinson's disease: A decline in compensation with disease progression? Mov Disord. 2015;30:1098–106.CrossRefPubMed
31.
go back to reference Ni Z, Gunraj C, Nelson AJ, Yeh IJ, Castillo G, Hoque T, et al. Two phases of interhemispheric inhibition between motor related cortical areas and the primary motor cortex in human. Cereb Cortex. 2009;19:1654–65.CrossRefPubMed Ni Z, Gunraj C, Nelson AJ, Yeh IJ, Castillo G, Hoque T, et al. Two phases of interhemispheric inhibition between motor related cortical areas and the primary motor cortex in human. Cereb Cortex. 2009;19:1654–65.CrossRefPubMed
32.
go back to reference Li JY, Espay AJ, Gunraj CA, Pal PK, Cunic DI, Lang AE, et al. Interhemispheric and ipsilateral connections in Parkinson's disease: Relation to mirror movements. Mov Disord. 2007;22:813–21.CrossRefPubMed Li JY, Espay AJ, Gunraj CA, Pal PK, Cunic DI, Lang AE, et al. Interhemispheric and ipsilateral connections in Parkinson's disease: Relation to mirror movements. Mov Disord. 2007;22:813–21.CrossRefPubMed
33.
go back to reference Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R. Short and long latency afferent inhibition in Parkinson's disease. Brain. 2003;126:1883–94.CrossRefPubMed Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R. Short and long latency afferent inhibition in Parkinson's disease. Brain. 2003;126:1883–94.CrossRefPubMed
34.
go back to reference Sailer A, Cunic DI, Paradiso GO, Gunraj CA, Wagle-Shukla A, Moro E, et al. Subthalamic nucleus stimulation modulates afferent inhibition in Parkinson disease. Neurology. 2007;68:356–63.CrossRefPubMed Sailer A, Cunic DI, Paradiso GO, Gunraj CA, Wagle-Shukla A, Moro E, et al. Subthalamic nucleus stimulation modulates afferent inhibition in Parkinson disease. Neurology. 2007;68:356–63.CrossRefPubMed
35.
go back to reference Wagle-Shukla A, Moro E, Gunraj C, Lozano A, Hodaie M, Lang A, et al. Long-term subthalamic nucleus stimulation improves sensorimotor integration and proprioception. J Neurol Neurosurg Psychiatry. 2013;84:1020–8.CrossRefPubMed Wagle-Shukla A, Moro E, Gunraj C, Lozano A, Hodaie M, Lang A, et al. Long-term subthalamic nucleus stimulation improves sensorimotor integration and proprioception. J Neurol Neurosurg Psychiatry. 2013;84:1020–8.CrossRefPubMed
36.
go back to reference Kuriakose R, Saha U, Castillo G, Udupa K, Ni Z, Gunraj C, et al. The nature and time course of cortical activation following subthalamic stimulation in Parkinson's disease. Cereb Cortex. 2010;20:1926–36.CrossRefPubMed Kuriakose R, Saha U, Castillo G, Udupa K, Ni Z, Gunraj C, et al. The nature and time course of cortical activation following subthalamic stimulation in Parkinson's disease. Cereb Cortex. 2010;20:1926–36.CrossRefPubMed
37.
go back to reference Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000;123:572–84.CrossRefPubMed Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000;123:572–84.CrossRefPubMed
38.
go back to reference Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R. Motor cortex plasticity in Parkinson's disease and levodopa-induced dyskinesias. Brain. 2006;129:1059–69.CrossRefPubMed Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R. Motor cortex plasticity in Parkinson's disease and levodopa-induced dyskinesias. Brain. 2006;129:1059–69.CrossRefPubMed
39.
go back to reference Kim SJ, Udupa K, Ni Z, Moro E, Gunraj C, Mazzella F, et al. Effects of subthalamic nucleus stimulation on motor cortex plasticity in Parkinson disease. Neurology. 2015;85:425–32.CrossRefPubMed Kim SJ, Udupa K, Ni Z, Moro E, Gunraj C, Mazzella F, et al. Effects of subthalamic nucleus stimulation on motor cortex plasticity in Parkinson disease. Neurology. 2015;85:425–32.CrossRefPubMed
40.
go back to reference Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45:201–6.CrossRefPubMed Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45:201–6.CrossRefPubMed
41.
go back to reference Benninger DH, Berman BD, Houdayer E, Pal N, Luckenbaugh DA, Schneider L, et al. Intermittent theta-burst transcranial magnetic stimulation for treatment of Parkinson disease. Neurology. 2011;76:601–9.PubMedCentralCrossRefPubMed Benninger DH, Berman BD, Houdayer E, Pal N, Luckenbaugh DA, Schneider L, et al. Intermittent theta-burst transcranial magnetic stimulation for treatment of Parkinson disease. Neurology. 2011;76:601–9.PubMedCentralCrossRefPubMed
42.
go back to reference Zamir O, Gunraj C, Ni Z, Mazzella F, Chen R. Effects of theta burst stimulation on motor cortex excitability in Parkinson's disease. Clin Neurophysiol. 2012;123:815–21.CrossRefPubMed Zamir O, Gunraj C, Ni Z, Mazzella F, Chen R. Effects of theta burst stimulation on motor cortex excitability in Parkinson's disease. Clin Neurophysiol. 2012;123:815–21.CrossRefPubMed
43.
go back to reference Suppa A, Marsili L, Belvisi D, Conte A, Iezzi E, Modugno N, et al. Lack of LTP-like plasticity in primary motor cortex in Parkinson's disease. Exp Neurol. 2011;227:296–301.CrossRefPubMed Suppa A, Marsili L, Belvisi D, Conte A, Iezzi E, Modugno N, et al. Lack of LTP-like plasticity in primary motor cortex in Parkinson's disease. Exp Neurol. 2011;227:296–301.CrossRefPubMed
44.
go back to reference Elahi B, Elahi B, Chen R. Effect of transcranial magnetic stimulation on Parkinson motor function--systematic review of controlled clinical trials. Mov Disord. 2009;24:357–63.CrossRefPubMed Elahi B, Elahi B, Chen R. Effect of transcranial magnetic stimulation on Parkinson motor function--systematic review of controlled clinical trials. Mov Disord. 2009;24:357–63.CrossRefPubMed
45.
go back to reference Okabe S, Ugawa Y, Kanazawa I. 0.2-Hz repetitive transcranial magnetic stimulation has no add-on effects as compared to a realistic sham stimulation in Parkinson's disease. Mov Disord. 2003;18:382–8.CrossRefPubMed Okabe S, Ugawa Y, Kanazawa I. 0.2-Hz repetitive transcranial magnetic stimulation has no add-on effects as compared to a realistic sham stimulation in Parkinson's disease. Mov Disord. 2003;18:382–8.CrossRefPubMed
46.
go back to reference Zanjani A, Zakzanis KK, Daskalakis ZJ, Chen R. Repetitive transcranial magnetic stimulation of the primary motor cortex in the treatment of motor signs in Parkinson's disease: A quantitative review of the literature. Mov Disord. 2015;30:750–8.CrossRefPubMed Zanjani A, Zakzanis KK, Daskalakis ZJ, Chen R. Repetitive transcranial magnetic stimulation of the primary motor cortex in the treatment of motor signs in Parkinson's disease: A quantitative review of the literature. Mov Disord. 2015;30:750–8.CrossRefPubMed
47.
go back to reference Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–403.CrossRefPubMed Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–403.CrossRefPubMed
48.
go back to reference Wagle-Shukla A, Angel MJ, Zadikoff C, Enjati M, Gunraj C, Lang AE, et al. Low-frequency repetitive transcranial magnetic stimulation for treatment of levodopa-induced dyskinesias. Neurology. 2007;68:704–5.CrossRefPubMed Wagle-Shukla A, Angel MJ, Zadikoff C, Enjati M, Gunraj C, Lang AE, et al. Low-frequency repetitive transcranial magnetic stimulation for treatment of levodopa-induced dyskinesias. Neurology. 2007;68:704–5.CrossRefPubMed
49.
go back to reference Filipovic SR, Rothwell JC, van de Warrenburg BP, Bhatia K. Repetitive transcranial magnetic stimulation for levodopa-induced dyskinesias in Parkinson's disease. Mov Disord. 2009;24:246–53.CrossRefPubMed Filipovic SR, Rothwell JC, van de Warrenburg BP, Bhatia K. Repetitive transcranial magnetic stimulation for levodopa-induced dyskinesias in Parkinson's disease. Mov Disord. 2009;24:246–53.CrossRefPubMed
50.
go back to reference Hamada M, Ugawa Y, Tsuji S. High-frequency rTMS over the supplementary motor area for treatment of Parkinson's disease. Mov Disord. 2008;11:1524–31.CrossRef Hamada M, Ugawa Y, Tsuji S. High-frequency rTMS over the supplementary motor area for treatment of Parkinson's disease. Mov Disord. 2008;11:1524–31.CrossRef
51.
go back to reference Koch G, Brusa L, Carrillo F, Lo GE, Torriero S, Oliveri M, et al. Cerebellar magnetic stimulation decreases levodopa-induced dyskinesias in Parkinson disease. Neurology. 2009;73:113–9.CrossRefPubMed Koch G, Brusa L, Carrillo F, Lo GE, Torriero S, Oliveri M, et al. Cerebellar magnetic stimulation decreases levodopa-induced dyskinesias in Parkinson disease. Neurology. 2009;73:113–9.CrossRefPubMed
52.
go back to reference Mir P, Matsunaga K, Gilio F, Quinn NP, Siebner HR, Rothwell JC. Dopaminergic drugs restore facilitatory premotor-motor interactions in Parkinson disease. Neurology. 2005;64:1906–12.CrossRefPubMed Mir P, Matsunaga K, Gilio F, Quinn NP, Siebner HR, Rothwell JC. Dopaminergic drugs restore facilitatory premotor-motor interactions in Parkinson disease. Neurology. 2005;64:1906–12.CrossRefPubMed
53.
go back to reference Coyle JT, Price DL, DeLong MR. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 1983;219:1184–90.CrossRefPubMed Coyle JT, Price DL, DeLong MR. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 1983;219:1184–90.CrossRefPubMed
54.
go back to reference Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, et al. Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology. 2002;59:392–7.CrossRefPubMed Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, et al. Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology. 2002;59:392–7.CrossRefPubMed
55.
go back to reference Pierantozzi M, Panella M, Palmieri MG, Koch G, Giordano A, Marciani MG, et al. Different TMS patterns of intracortical inhibition in early onset Alzheimer dementia and frontotemporal dementia. Clin Neurophysiol. 2004;115:2410–8.CrossRefPubMed Pierantozzi M, Panella M, Palmieri MG, Koch G, Giordano A, Marciani MG, et al. Different TMS patterns of intracortical inhibition in early onset Alzheimer dementia and frontotemporal dementia. Clin Neurophysiol. 2004;115:2410–8.CrossRefPubMed
56.
go back to reference Sakuma K, Murakami T, Nakashima K. Short latency afferent inhibition is not impaired in mild cognitive impairment. Clin Neurophysiol. 2007;118:1460–3.CrossRefPubMed Sakuma K, Murakami T, Nakashima K. Short latency afferent inhibition is not impaired in mild cognitive impairment. Clin Neurophysiol. 2007;118:1460–3.CrossRefPubMed
57.
go back to reference Pepin JL, Bogacz D, De PV, Delwaide P. Motor cortex inhibition is not impaired in patients with Alzheimer's disease: evidence from paired transcranial magnetic stimulation. J Neurol Sci. 1999;170:119–23.CrossRefPubMed Pepin JL, Bogacz D, De PV, Delwaide P. Motor cortex inhibition is not impaired in patients with Alzheimer's disease: evidence from paired transcranial magnetic stimulation. J Neurol Sci. 1999;170:119–23.CrossRefPubMed
58.
go back to reference Ferreri F, Pauri F, Pasqualetti P, Fini R, Dal Forno G, Rossini PM. Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation study. Ann Neurol. 2003;53:102–8.CrossRefPubMed Ferreri F, Pauri F, Pasqualetti P, Fini R, Dal Forno G, Rossini PM. Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation study. Ann Neurol. 2003;53:102–8.CrossRefPubMed
59.
go back to reference Perretti A, Grossi D, Fragassi N, Lanzillo B, Nolano M, Pisacreta AI, et al. Evaluation of the motor cortex by magnetic stimulation in patients with Alzheimer disease. J Neurol Sci. 1996;135:31–7.CrossRefPubMed Perretti A, Grossi D, Fragassi N, Lanzillo B, Nolano M, Pisacreta AI, et al. Evaluation of the motor cortex by magnetic stimulation in patients with Alzheimer disease. J Neurol Sci. 1996;135:31–7.CrossRefPubMed
60.
go back to reference Di Lazzaro V, Pilato F, Dileone M, Saturno E, Profice P, Marra C, et al. Functional evaluation of cerebral cortex in dementia with Lewy bodies. Neuroimage. 2007;37:422–9.CrossRefPubMed Di Lazzaro V, Pilato F, Dileone M, Saturno E, Profice P, Marra C, et al. Functional evaluation of cerebral cortex in dementia with Lewy bodies. Neuroimage. 2007;37:422–9.CrossRefPubMed
61.
go back to reference Marra C, Quaranta D, Profice P, Pilato F, Capone F, Iodice F, et al. Central cholinergic dysfunction measured "in vivo" correlates with different behavioral disorders in Alzheimer's disease and dementia with Lewy body. Brain Stimul. 2012;5:533–8.CrossRefPubMed Marra C, Quaranta D, Profice P, Pilato F, Capone F, Iodice F, et al. Central cholinergic dysfunction measured "in vivo" correlates with different behavioral disorders in Alzheimer's disease and dementia with Lewy body. Brain Stimul. 2012;5:533–8.CrossRefPubMed
62.
go back to reference Nardone R, Bergmann JM,K, Kunz A, Klein S, Caleri F, et al. Abnormal short latency afferent inhibition in early Alzheimer's disease: a transcranial magnetic demonstration. J Neural Transm. 2008;115:1557–62.CrossRefPubMed Nardone R, Bergmann JM,K, Kunz A, Klein S, Caleri F, et al. Abnormal short latency afferent inhibition in early Alzheimer's disease: a transcranial magnetic demonstration. J Neural Transm. 2008;115:1557–62.CrossRefPubMed
63.
go back to reference Nardone R, Bergmann J, Christova M, Caleri F, Tezzon FG,L, et al. Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. J Neural Transm. 2012;119:463–71.CrossRefPubMed Nardone R, Bergmann J, Christova M, Caleri F, Tezzon FG,L, et al. Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. J Neural Transm. 2012;119:463–71.CrossRefPubMed
64.
go back to reference Tsutsumi R, Hanajima R, Hamada M, Shirota Y, Matsumoto H, Terao Y, et al. Reduced interhemispheric inhibition in mild cognitive impairment. Exp Brain Res. 2012;218:21–6.CrossRefPubMed Tsutsumi R, Hanajima R, Hamada M, Shirota Y, Matsumoto H, Terao Y, et al. Reduced interhemispheric inhibition in mild cognitive impairment. Exp Brain Res. 2012;218:21–6.CrossRefPubMed
65.
go back to reference Liepert J, Bar KJ, Meske U, Weiller C. Motor cortex disinhibition in Alzheimer's disease. Clin Neurophysiol. 2001;112:1436–41.CrossRefPubMed Liepert J, Bar KJ, Meske U, Weiller C. Motor cortex disinhibition in Alzheimer's disease. Clin Neurophysiol. 2001;112:1436–41.CrossRefPubMed
66.
go back to reference Inghilleri M, Conte A, Frasca V, Scaldaferri N, Gilio F, Santini M, et al. Altered response to rTMS in patients with Alzheimer's disease. Clin Neurophysiol. 2006;117:103–9.CrossRefPubMed Inghilleri M, Conte A, Frasca V, Scaldaferri N, Gilio F, Santini M, et al. Altered response to rTMS in patients with Alzheimer's disease. Clin Neurophysiol. 2006;117:103–9.CrossRefPubMed
67.
go back to reference Battaglia F, Wang HY, Ghilardi MF, Gashi E, Quartarone A, Friedman E, et al. Cortical plasticity in Alzheimer's disease in humans and rodents. Biol Psychiatry. 2007;62:1405–12.CrossRefPubMed Battaglia F, Wang HY, Ghilardi MF, Gashi E, Quartarone A, Friedman E, et al. Cortical plasticity in Alzheimer's disease in humans and rodents. Biol Psychiatry. 2007;62:1405–12.CrossRefPubMed
68.
go back to reference Koch G, Di Lorenzo F, Bonnì S, Ponzo V, Caltagirone C, Martorana A. Impaired LTP- but not LTD-like cortical plasticity in Alzheimer's disease patients. J Alzheimers Dis. 2012;31:593–9.PubMed Koch G, Di Lorenzo F, Bonnì S, Ponzo V, Caltagirone C, Martorana A. Impaired LTP- but not LTD-like cortical plasticity in Alzheimer's disease patients. J Alzheimers Dis. 2012;31:593–9.PubMed
69.
go back to reference Koch G, Esposito Z, Codecà CF, Mori F, Kusayanagi H, Monteleone F, et al. Altered dopamine modulation of LTD-like plasticity in Alzheimer's disease patients. Clin Neurophysiol. 2011;122:703–7.CrossRefPubMed Koch G, Esposito Z, Codecà CF, Mori F, Kusayanagi H, Monteleone F, et al. Altered dopamine modulation of LTD-like plasticity in Alzheimer's disease patients. Clin Neurophysiol. 2011;122:703–7.CrossRefPubMed
70.
go back to reference Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV, et al. Functional alterations in memory networks in early Alzheimer's disease. Neruomol Med. 2010;12:22–43.CrossRef Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV, et al. Functional alterations in memory networks in early Alzheimer's disease. Neruomol Med. 2010;12:22–43.CrossRef
71.
go back to reference Cotelli M, Manenti R, Cappa SF, Zanetti O, Miniussi C. Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. Eur J Neurol. 2008;15:1286–92.CrossRefPubMed Cotelli M, Manenti R, Cappa SF, Zanetti O, Miniussi C. Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. Eur J Neurol. 2008;15:1286–92.CrossRefPubMed
72.
go back to reference Cotelli M, Calabria M, Manenti R, Rosini S, Zanetti O, Cappa SF, et al. Improved language performance in Alzheimer disease following brain stimulation. J Neurol Neurosurg Psychiatry. 2011;82:794–7.CrossRefPubMed Cotelli M, Calabria M, Manenti R, Rosini S, Zanetti O, Cappa SF, et al. Improved language performance in Alzheimer disease following brain stimulation. J Neurol Neurosurg Psychiatry. 2011;82:794–7.CrossRefPubMed
73.
go back to reference Ahmed MA, Darwish ES, Khedr EM, El Serogy YM, Ali AM. Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer's dementia. J Neurol. 2012;259:83–92.CrossRefPubMed Ahmed MA, Darwish ES, Khedr EM, El Serogy YM, Ali AM. Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer's dementia. J Neurol. 2012;259:83–92.CrossRefPubMed
74.
go back to reference Turriziani P, Smirni D, Zappalà G, Mangano GR, Oliveri M, Cipolotti, L. Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: the role of the right dorsolateral prefrontal cortex. Front Hum Neurosci 2012. 6:doi: 10.3389/fnhum.2012.00062. Turriziani P, Smirni D, Zappalà G, Mangano GR, Oliveri M, Cipolotti, L. Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: the role of the right dorsolateral prefrontal cortex. Front Hum Neurosci 2012. 6:doi: 10.​3389/​fnhum.​2012.​00062.
75.
go back to reference Eisen A, Shytbel W, Murphy K, Hoirch M. Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve. 1990;13:146–51.CrossRefPubMed Eisen A, Shytbel W, Murphy K, Hoirch M. Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve. 1990;13:146–51.CrossRefPubMed
76.
go back to reference Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:1137–41.CrossRefPubMed Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:1137–41.CrossRefPubMed
77.
go back to reference Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain. 2006;129:2436–46.CrossRefPubMed Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain. 2006;129:2436–46.CrossRefPubMed
78.
go back to reference Vucic S, Nicholson GA, Kiernan MC. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain. 2008;131:1540–50.CrossRefPubMed Vucic S, Nicholson GA, Kiernan MC. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain. 2008;131:1540–50.CrossRefPubMed
79.
go back to reference Stefan K, Kunesch E, Benecke R, Classen J. Effects of riluzole on cortical excitability in patients with amyotrophic lateral sclerosis. Ann Neurol. 2001;49:536–9.CrossRefPubMed Stefan K, Kunesch E, Benecke R, Classen J. Effects of riluzole on cortical excitability in patients with amyotrophic lateral sclerosis. Ann Neurol. 2001;49:536–9.CrossRefPubMed
80.
go back to reference Nihei K, McKee AC, Kowall NW. Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathol. 1993;86:55–64.CrossRefPubMed Nihei K, McKee AC, Kowall NW. Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathol. 1993;86:55–64.CrossRefPubMed
81.
go back to reference Karandreas N, Papadopoulou M, Kokotis P, Papapostolou A, Tsivgoulis G, Zambelis T. Impaired interhemispheric inhibition in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis. 2007;8:112–8.CrossRefPubMed Karandreas N, Papadopoulou M, Kokotis P, Papapostolou A, Tsivgoulis G, Zambelis T. Impaired interhemispheric inhibition in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis. 2007;8:112–8.CrossRefPubMed
82.
go back to reference Zanette G, Forgione A, Manganotti P, Fiaschi A, Tamburin S. The effect of repetitive transcranial magnetic stimulation on motor performance, fatigue and quality of life in amyotrophic lateral sclerosis. J Neurol Sci. 2008;270:18–22.CrossRefPubMed Zanette G, Forgione A, Manganotti P, Fiaschi A, Tamburin S. The effect of repetitive transcranial magnetic stimulation on motor performance, fatigue and quality of life in amyotrophic lateral sclerosis. J Neurol Sci. 2008;270:18–22.CrossRefPubMed
83.
go back to reference Di Lazzaro V, Oliviero A, Saturno E, Pilato F, Dileone M, Sabatelli M, et al. Motor cortex stimulation for amyotrophic lateral sclerosis. Time for a therapeutic trial? Clin Neurophysiol. 2004;115:1479–85.CrossRefPubMed Di Lazzaro V, Oliviero A, Saturno E, Pilato F, Dileone M, Sabatelli M, et al. Motor cortex stimulation for amyotrophic lateral sclerosis. Time for a therapeutic trial? Clin Neurophysiol. 2004;115:1479–85.CrossRefPubMed
84.
go back to reference Di Lazzaro V, Dileone M, Pilato F, Profice P, Cioni B, Meglio M, et al. Long-term motor cortex stimulation for amyotrophic lateral sclerosis. Brain Stimul. 2010;3:22–7.CrossRefPubMed Di Lazzaro V, Dileone M, Pilato F, Profice P, Cioni B, Meglio M, et al. Long-term motor cortex stimulation for amyotrophic lateral sclerosis. Brain Stimul. 2010;3:22–7.CrossRefPubMed
85.
go back to reference Di Lazzaro V, Dileone M, Pilato F, Profice P, Ranieri F, Musumeci G, et al. Repetitive transcranial magnetic stimulation for ALS. A preliminary controlled study. Neurosci Lett. 2006;408:135–40.CrossRefPubMed Di Lazzaro V, Dileone M, Pilato F, Profice P, Ranieri F, Musumeci G, et al. Repetitive transcranial magnetic stimulation for ALS. A preliminary controlled study. Neurosci Lett. 2006;408:135–40.CrossRefPubMed
86.
go back to reference Di Lazzaro V, Pilato F, Profice P, Ranieri F, Musumeci G, Florio L, et al. Motor cortex stimulation for ALS: a double blind placebo-controlled study. Neurosci Lett. 2009;464:18–21.CrossRefPubMed Di Lazzaro V, Pilato F, Profice P, Ranieri F, Musumeci G, Florio L, et al. Motor cortex stimulation for ALS: a double blind placebo-controlled study. Neurosci Lett. 2009;464:18–21.CrossRefPubMed
87.
go back to reference Schippling S, Schneider SA, Bhatia KP, Münchau A, Rothwell JC, Tabrizi SJ, et al. Abnormal motor cortex excitability in preclinical and very early Huntington's disease. Biol Psychiatry. 2009;65:959–65.PubMedCentralCrossRefPubMed Schippling S, Schneider SA, Bhatia KP, Münchau A, Rothwell JC, Tabrizi SJ, et al. Abnormal motor cortex excitability in preclinical and very early Huntington's disease. Biol Psychiatry. 2009;65:959–65.PubMedCentralCrossRefPubMed
88.
go back to reference Orth M, Schippling S, Schneider SA, Bhatia KP, Talelli PSJT, et al. Abnormal motor cortex plasticity in premanifest and very early manifest Huntington disease. J Neurol Neurosurg Psychiatry. 2010;81:267–70.PubMedCentralCrossRefPubMed Orth M, Schippling S, Schneider SA, Bhatia KP, Talelli PSJT, et al. Abnormal motor cortex plasticity in premanifest and very early manifest Huntington disease. J Neurol Neurosurg Psychiatry. 2010;81:267–70.PubMedCentralCrossRefPubMed
89.
go back to reference Priori A, Polidori L, Rona S, Manfredi M, Berardelli A. Spinal and cortical inhibition in Huntington's chorea. Mov Disord. 2000;15:938–46.CrossRefPubMed Priori A, Polidori L, Rona S, Manfredi M, Berardelli A. Spinal and cortical inhibition in Huntington's chorea. Mov Disord. 2000;15:938–46.CrossRefPubMed
90.
go back to reference Lefaucheur JP, Ménard-Lefaucheur I, Maison P, Baudic S, Cesaro P, Peschanski M, et al. Electrophysiological deterioration over time in patients with Huntington's disease. Mov Disord. 2006;21:1350–4.CrossRefPubMed Lefaucheur JP, Ménard-Lefaucheur I, Maison P, Baudic S, Cesaro P, Peschanski M, et al. Electrophysiological deterioration over time in patients with Huntington's disease. Mov Disord. 2006;21:1350–4.CrossRefPubMed
91.
go back to reference Hanajima R, Ugawa Y, Terao Y, Furubayashi T, Machii K, Shiio Y, et al. Intracortical inhibition of the motor cortex is normal in chorea. J Neurol Neurosurg Psychiatry. 1999;66:783–6.PubMedCentralCrossRefPubMed Hanajima R, Ugawa Y, Terao Y, Furubayashi T, Machii K, Shiio Y, et al. Intracortical inhibition of the motor cortex is normal in chorea. J Neurol Neurosurg Psychiatry. 1999;66:783–6.PubMedCentralCrossRefPubMed
92.
go back to reference Lorenzano C, Dinapoli L, Gilio F, Suppa A, Bagnato S, Currà A, et al. Motor cortical excitability studied with repetitive transcranial magnetic stimulation in patients with Huntington's disease. Clin Neurophysiol. 2006;117:1677–81.CrossRefPubMed Lorenzano C, Dinapoli L, Gilio F, Suppa A, Bagnato S, Currà A, et al. Motor cortical excitability studied with repetitive transcranial magnetic stimulation in patients with Huntington's disease. Clin Neurophysiol. 2006;117:1677–81.CrossRefPubMed
93.
go back to reference Crupi D, Ghilardi MF, Mosiello C, Di Rocco A, Quartarone A, Battaglia F. Cortical and brainstem LTP-like plasticity in Huntington's disease. Brain Res Bull. 2008;75:107–14.CrossRefPubMed Crupi D, Ghilardi MF, Mosiello C, Di Rocco A, Quartarone A, Battaglia F. Cortical and brainstem LTP-like plasticity in Huntington's disease. Brain Res Bull. 2008;75:107–14.CrossRefPubMed
94.
go back to reference Brusa L, Versace V, Koch G, Bernardi G, Iani C, Stanzione P, et al. Improvement of choreic movements by 1 Hz repetitive transcranial magnetic stimulation in Huntington's disease patients. Ann Neurol. 2005;58:655–6.CrossRefPubMed Brusa L, Versace V, Koch G, Bernardi G, Iani C, Stanzione P, et al. Improvement of choreic movements by 1 Hz repetitive transcranial magnetic stimulation in Huntington's disease patients. Ann Neurol. 2005;58:655–6.CrossRefPubMed
95.
go back to reference Di Lazzaro V, Dileone M, Pilato F, Contarino MF, Musumeci G, Bentivoglio AR, et al. Repetitive transcranial magnetic stimulation of the motor cortex for hemichorea. J Neurol Neurosurg Psychiatry. 2006;77:1095–7.PubMedCentralCrossRefPubMed Di Lazzaro V, Dileone M, Pilato F, Contarino MF, Musumeci G, Bentivoglio AR, et al. Repetitive transcranial magnetic stimulation of the motor cortex for hemichorea. J Neurol Neurosurg Psychiatry. 2006;77:1095–7.PubMedCentralCrossRefPubMed
96.
go back to reference Obeso JA, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, Rodriguez M, et al. Missing pieces in the Parkinson's disease puzzle. Nat Med. 2010;16:653–61.CrossRefPubMed Obeso JA, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, Rodriguez M, et al. Missing pieces in the Parkinson's disease puzzle. Nat Med. 2010;16:653–61.CrossRefPubMed
Metadata
Title
Transcranial magnetic stimulation to understand pathophysiology and as potential treatment for neurodegenerative diseases
Authors
Zhen Ni
Robert Chen
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Translational Neurodegeneration / Issue 1/2015
Electronic ISSN: 2047-9158
DOI
https://doi.org/10.1186/s40035-015-0045-x

Other articles of this Issue 1/2015

Translational Neurodegeneration 1/2015 Go to the issue