Are studies of motor cortex plasticity relevant in human patients with Parkinson's disease?

Clinical Neurophysiology

Volumn 127, Issue 1, 2016, Pages 50-59

  Bologna, Matteo ^a   Suppa, Antonio ^a   Conte, Antonella ^a   Latorre, Anna ^b   Rothwell, John C ^c   Berardelli, Alfredo ^a,b  

^a IRCCS NEUROMED   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Neurophysiology; Parkinson's disease; Synaptic transmission and plasticity; Transcranial magnetic stimulation

Indexed keywords

BIOLOGICAL MARKER;

BASAL GANGLION; BRAIN ELECTROPHYSIOLOGY; DENERVATION; DISEASE SEVERITY; DOPAMINERGIC SYSTEM; HUMAN; MOTOR CORTEX; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; TRANSCRANIAL MAGNETIC STIMULATION; ANIMAL; MOTOR EVOKED POTENTIAL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; EVOKED POTENTIALS, MOTOR; HUMANS; MOTOR CORTEX; NEURONAL PLASTICITY; PARKINSON DISEASE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84924794997     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2015.02.009     Document Type: Review

References (141)

1. Ahmed Z., Asi Y.T., Sailer A., Lees A.J., Houlden H., Revesz T., et al. The neuropathology, pathophysiology and genetics of multiple system atrophy. Neuropathol Appl Neurobiol 2012, 38:4-24.
2. Alexander G.E., Crutcher M.D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 1990, 13:266-271.
3. Bagnato S., Agostino R., Modugno N., Quartarone A., Berardelli A. Plasticity of the motor cortex in Parkinson's disease patients on and off therapy. Mov Disord 2006, 21:639-645.
4. Barbin L., Leux C., Sauleau P., Meyniel C., Nguyen J.M., Pereon Y., et al. Non-homogeneous effect of levodopa on inhibitory circuits in Parkinson's disease and dyskinesia. Parkinsonism Relat Disord 2013, 19:165-170.
5. Bateup H.S., Santini E., Shen W., Birnbaum S., Valjent E., Surmeier D.J., et al. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci U S A 2010, 107:14845-14850.
6. Benninger D.H., Lomarev M., Wassermann E.M., Lopez G., Houdayer E., Fasano R.E., et al. Safety study of 50 Hz repetitive transcranial magnetic stimulation in patients with Parkinson's disease. Clin Neurophysiol 2009, 120:809-815.
7. Berardelli A., Rona S., Inghilleri M., Manfredi M. Cortical inhibition in Parkinson's disease. A study with paired magnetic stimulation. Brain 1996, 119:71-77.
8. Berardelli A., Inghilleri M., Rothwell J.C., Romeo S., Currà A., Gilio F., et al. Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res 1998, 122:79-84.
9. Berardelli A., Inghilleri M., Gilio F., Romeo S., Pedace F., Currà A., et al. Effects of repetitive cortical stimulation on the silent period evoked by magnetic stimulation. Exp Brain Res 1999, 125:82-86.
10. Berardelli A., Abbruzzese G., Chen R., Orth M., Ridding M.C., Stinear C., et al. Consensus paper on short-interval intracortical inhibition and other transcranial magnetic stimulation intracortical paradigms in movement disorders. Brain Stimul 2008, 1:183-191.
11. Berardelli A., Wenning G.K., Antonini A., Berg D., Bloem B.R., Bonifati V., et al. EFNS/MDS-ES/ENS recommendations for the diagnosis of Parkinson's disease. Eur J Neurol 2013, 20:16-34.
12. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973, 232:331-356.
13. Bologna M., Conte A., Suppa A., Berardelli A. Motor cortex plasticity in Parkinson's disease: advances and controversies. Clin Neurophysiol 2012, 123:640-641.
14. Brusa L., Versace V., Koch G., Iani C., Stanzione P., Bernardi G., et al. Low frequency rTMS of the SMA transiently ameliorates peak-dose LID in Parkinson's disease. Clin Neurophysiol 2006, 117:1917-1921.
15. Buhmann C., Gorsler A., Bäumer T., Hidding U., Demiralay C., Hinkelmann K., et al. Abnormal excitability of premotor-motor connections in de novo Parkinson's disease. Brain 2004, 127:2732-2746.
16. Cabin D.E., Shimazu K., Murphy D., Cole N.B., Gottschalk W., McIlwain K.L., et al. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 2002, 22:8797-8807.
17. Calabresi P., Castrioto A., Di Filippo M., Picconi B. New experimental and clinical links between the hippocampus and the dopaminergic system in Parkinson's disease. Lancet Neurol 2013, 12:811-821.
18. Calabresi P., Mercuri N.B., Di Filippo M. Synaptic plasticity, dopamine and Parkinson's disease: one step ahead. Brain 2009, 132:285-287.
19. Cantello R., Tarletti R., Civardi C. Transcranial magnetic stimulation and Parkinson's disease. Brain Res Brain Res Rev 2002, 38:309-327.
20. Carson R.G., Kennedy N.C. Modulation of human corticospinal excitability by paired associative stimulation. Front Hum Neurosci 2013, 3(7):823.
21. Castro-Alamancos M.A., Connors B.W. Short-term synaptic enhancement and long-term potentiation in neocortex. Proc Natl Acad Sci U S A 1996, 93:1335-1339.
22. Chen R., Cros D., Curra A., Di Lazzaro V., Lefaucheur J.P., Magistris M.R., et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 2008, 119:504-532.
23. Chouinard P.A., Paus T. The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 2006, 12:143-152.
24. Cisek P., Kalaska J.F. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Ann Rev Neurosci 2010, 33:269-298.
25. Conte A., Belvisi D., Bologna M., Ottaviani D., Fabbrini G., Colosimo C., et al. Abnormal cortical synaptic plasticity in primary motor area in progressive supranuclear palsy. Cereb Cortex 2012, 22:693-700.
26. Conte A., Gilio F., Iezzi E., Frasca V., Inghilleri M., Berardelli A. Attention influences the excitability of cortical motor areas in healthy humans. Exp Brain Res 2007, 182:109-117.
27. Cooke S.F., Bliss T.V. Plasticity in the human central nervous system. Brain 2006, 129:1659-1673.
28. Cui G., Jun S.B., Jin X., Pham M.D., Vogel S.S., Lovinger D.M., et al. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 2013, 494:238-242.
29. Cummings J.A., Mulkey R.M., Nicoll R.A., Malenka R.C. Ca2+ signaling requirements for long-term depression in the hippocampus. Neuron 1996, 16:825-833.
30. Currà A., Modugno N., Inghilleri M., Manfredi M., Hallett M., Berardelli A. Transcranial magnetic stimulation techniques in clinical investigation. Neurology 2002, 9:1851-1859.
31. Dayan E., Censor N., Buch E.R., Sandrini M., Cohen L.G. Noninvasive brain stimulation: from physiology to network dynamics and back. Nat Neurosci 2013, 16:838-844.
32. Degardin A., Devos D., Defebvre L., Destée A., Plomhause L., Derambure P., et al. Effect of intermittent theta-burst stimulation on akinesia and sensorimotor integration in patients with Parkinson's disease. Eur J Neurosci 2012, 36:2669-2678.
33. DeLong M.R., Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch Neurol 2007, 64:20-24.
34. Di Lazzaro V., Oliviero A., Berardelli A., Mazzone P., Insola A., Pilato F., et al. Direct demonstration of the effects of repetitive transcranial magnetic stimulation on the excitability of the human motor cortex. Exp Brain Res 2002, 144:549-553.
35. Di Lazzaro V., Oliviero A., Saturno E., Dileone M., Pilato F., Nardone R., Ranieri F., Musumeci G., Fiorilla T., Tonali P. Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 2005, 564:661-668.
36. Di Lazzaro V., Pilato F., Saturno E., Oliviero A., Dileone M., Mazzone P., et al. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 2005, 565:945-950.
37. Eggers C., Fink G.R., Nowak D.A. Theta burst stimulation over the primary motor cortex does not induce cortical plasticity in Parkinson's disease. J Neurol 2010, 257:1669-1674.
38. Elahi B., Elahi B., Chen R. Effect of transcranial magnetic stimulation on Parkinson motor function-systematic review of controlled clinical trials. Mov Disord 2009, 24:357-363.
39. Elahi B., Gunraj C., Chen R. Short-interval intracortical inhibition blocks long-term potentiation induced by paired associative stimulation. J Neurophysiol 2012 Apr, 107(7):1935-1941. Epub 2012 Jan 11. 10.1152/jn.00202.2011.
40. Errico F., Bonito-Oliva A., Bagetta V., Vitucci D., Romano R., Zianni E., et al. Higher free D-aspartate and N-methyl-D-aspartate levels prevent striatal depotentiation and anticipate L-DOPA-induced dyskinesia. Exp Neurol 2011, 232:240-250.
41. Filipović S.R., Rothwell J.C., Bhatia K. Low-frequency repetitive transcranial magnetic stimulation and off-phase motor symptoms in Parkinson's disease. J Neurol Sci 2010, 291:1-4.
42. Fitzgerald P.B., Benitez J., Oxley T., Daskalakis J.Z., de Castella A.R., Kulkarni J. A study of the effects of lorazepam and dextromethorphan on the response to cortical 1 Hz repetitive transcranial magnetic stimulation. NeuroReport 2005, 16:1525-1528.
43. Gerschlager W., Siebner H.R., Rothwell J.C. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 2001, 57:449-455.
44. Ghiglieri V., Pendolino V., Sgobio C., Bagetta V., Picconi B., Calabresi P. Θ-burst stimulation and striatal plasticity in experimental parkinsonism. Exp Neurol 2012, 236:395-398.
45. Gilio F., Currà A., Inghilleri M., Lorenzano C., Manfredi M., Berardelli A. Repetitive magnetic stimulation of cortical motor areas in Parkinson's disease: implications for the pathophysiology of cortical function. Mov Disord 2002, 17:467-473.
46. González-García N., Armony J.L., Soto J., Trejo D., Alegría M.A., Drucker-Colín R. Effects of rTMS on Parkinson's disease: a longitudinal fMRI study. J Neurol 2011, 258:1268-1280.
47. Groppa S., Oliviero A., Eisen A., Quartarone A., Cohen L.G., Mall V., et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 2012, 123:858-882.
48. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007, 55:187-199.
49. Hallett M., Rothwell J. Milestones in clinical neurophysiology. Mov Disord 2011, 26:958-967.
50. Halliday G.M., Macdonald V., Henderson J.M. A comparison of degeneration in motor thalamus and cortex between progressive supranuclear palsy and Parkinson's disease. Brain 2005, 128:2272-2280.
51. Halliday G., Lees A., Stern M. Milestones in Parkinson's disease-clinical and pathologic features. Mov Disord 2011, 26:1015-1021.
52. Hamada M., Ugawa Y., Tsuji S. Effectiveness of rTMS on Parkinson's Disease Study Group, Japan. High-frequency rTMS over the supplementary motor area for treatment of Parkinson's disease. Mov Disord 2008, 23:1524-1531.
53. Hamada M., Hanajima R., Terao Y., Okabe S., Nakatani-Enomoto S., Furubayashi T., et al. Primary motor cortical metaplasticity induced by priming over the supplementary motor area. J Physiol 2009, 587:4845-4862.
54. Hamada M., Strigaro G., Murase N., Sadnicka A., Galea J.M., Edwards M.J., et al. Cerebellar modulation of human associative plasticity. J Physiol 2012, 590:2365-2374.
55. Hamada M., Murase N., Hasan A., Balaratnam M., Rothwell J.C. The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 2013, 23:1593-1605.
56. Hosp J.A., Luft A.R. Dopaminergic meso-cortical projections to m1: role in motor learning and motor cortex plasticity. Front Neurol 2013, 4:145.
57. Hsieh T.H., Huang Y.Z., Rotenberg A., Pascual-Leone A., Chiang Y.H., Wang J.Y., et al. Functional dopaminergic neurons in substantia nigra are required for transcranial magnetic stimulation-induced motor plasticity. Cereb Cortex 2014, Jan 22. [Epub ahead of print]. 10.1093/cercor/bht421.
58. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
59. Huang Y.Z., Chen R.S., Rothwell J.C., Wen H.Y. The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 2007, 118:1028-1032.
60. Huang Y.Z., Rothwell J.C., Lu C.S., Chuang W.L., Chen R.S. Abnormal bidirectional plasticity-like effects in Parkinson's disease. Brain 2011, 134:2312-2320.
61. Hughes A.J., Daniel S.E., Kilford L., Lees A.J. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992, 55:181-184.
62. Iezzi E., Suppa A., Conte A., Li Voti P., Bologna M., Berardelli A. Short-term and long-term plasticity interaction in human primary motor cortex. Eur J Neurosci 2011, 33:1908-1915.
63. Jankovic J. Parkinson's disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008, 79:368-376.
64. Jennum P., Winkel H., Fuglsang-Frederiksen A. Repetitive magnetic stimulation and motor evoked potentials. Electroencephalogr Clin Neurophysiol 1995, 97:96-101.
65. Kačar A., Filipović S.R., Kresojević N., Milanović S.D., Ljubisavljević M., Kostić V.S., Rothwell J.C. History of exposure to dopaminergic medication does not affect motor cortex plasticity and excitability in Parkinson's disease. Clin Neurophysiol 2013, 124:697-707.
66. Kanno M., Matsumoto M., Togashi H., Yoshioka M., Mano Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J Neurol Sci 2004, 217:73-81.
67. Kawashima S., Ueki Y., Mima T., Fukuyama H., Ojika K., Matsukawa N. Differences in dopaminergic modulation to motor cortical plasticity between Parkinson's disease and multiple system atrophy. PLoS ONE 2013, 8:e62515.
68. Keck M.E., Welt T., Müller M.B., Erhardt A., Ohl F., Toschi N., et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology 2002, 43:101-109.
69. Khedr E.M., Rothwell J.C., Shawky O.A., Ahmed M.A., Hamdy A. Effect of daily repetitive transcranial magnetic stimulation on motor performance in Parkinson's disease. Mov Disord 2006, 21:2201-2205.
70. Khedr E.M., Rothwell J.C., Shawky O.A., Ahmed M.A., Foly N., Hamdy A. Dopamine levels after repetitive transcranial magnetic stimulation of motor cortex in patients with Parkinson's disease: preliminary results. Mov Disord 2007, 22:1046-1050.
71. Kishore A., Joseph T., Velayudhan B., Popa T., Meunier S. Early, severe and bilateral loss of LTP and LTD-like plasticity in motor cortex (M1) in de novo Parkinson's disease. Clin Neurophysiol 2012, 123:822-828.
72. Kishore A., Popa T., Velayudhan B., Joseph T., Balachandran A., Meunier S. Acute dopamine boost has a negative effect on plasticity of the primary motor cortex in advanced Parkinson's disease. Brain 2012, 135:2074-2088.
73. Kishore A., Popa T., Balachandran A., Chandran S., Pradeep S., Backer F., et al. Cerebellar sensory processing alterations impact motor cortical plasticity in Parkinson's disease: clues from dyskinetic patients. Cereb Cortex 2014, 24:2055-2067.
74. Koch G., Brusa L., Caltagirone C., Peppe A., Oliveri M., Stanzione P., et al. RTMS of supplementary motor area modulates therapy-induced dyskinesias in Parkinson disease. Neurology 2005, 65:623-625.
75. Koch G., Brusa L., Carrillo F., Lo Gerfo E., Torriero S., Oliveri M., et al. Cerebellar magnetic stimulation decreases levodopa-induced dyskinesias in Parkinson disease. Neurology 2009, 73:113-119.
76. Kojovic M., Bologna M., Kassavetis P., Murase N., Palomar F.J., Berardelli A., et al. Functional reorganization of sensorimotor cortex in early Parkinson disease. Neurology 2012, 78:1441-1448.
77. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
78. Lefaucheur J.P. Motor cortex dysfunction revealed by cortical excitability studies in Parkinson's disease: influence of antiparkinsonian treatment and cortical stimulation. Clin Neurophysiol 2005, 116:244-253.
79. Lefaucheur J.P., Drouot X., Von Raison F., Menard-Lefaucheur I., Cesaro P., Nguyen J.P. Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson's disease. Clin Neurophysiol 2004, 115:2530-2541.
80. Li Voti P., Conte A., Suppa A., Iezzi E., Bologna M., Aniello M.S., et al. Correlation between cortical plasticity, motor learning and BDNF genotype in healthy subjects. Exp Brain Res 2011, 212:91-99.
81. López-Alonso V., Cheeran B., Río-Rodríguez D., Fernández-Del-Olmo M. Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul 2014, 7:372-380.
82. Lovinger D.M., Mathur B.N. Endocannabinoids in striatal plasticity. Parkinsonism Relat Disord 2012, 18(Suppl. 1):S132-S134.
83. MacKinnon C.D., Gilley E.A., Weis-McNulty A., Simuni T. Pathways mediating abnormal intracortical inhibition in Parkinson's disease. Ann Neurol 2005, 58:516-524.
84. Maeda F., Keenan J.P., Tormos J.M., Topka H., Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 2000, 133:425-430.
85. Mak M.K. Repetitive transcranial magnetic stimulation combined with treadmill training can modulate corticomotor inhibition and improve walking performance in people with Parkinson's disease. J Physiother 2013, 59:128.
86. Matsunaga K., Maruyama A., Fujiwara T., Nakanishi R., Tsuji S., Rothwell J.C. Increased corticospinal excitability after 5 Hz rTMS over the human supplementary motor area. J Physiol 2005, 562:295-306.
87. McDonnell M.N., Orekhov Y., Ziemann U. Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen. Exp Brain Res 2007, 180:181-186.
88. Mink J.W. The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol 2003, 60:1365-1368.
89. Mir P., Matsunaga K., Gilio F., Quinn N.P., Siebner H.R., Rothwell J.C. Dopaminergic drugs restore facilitatory premotor-motor interactions in Parkinson disease. Neurology 2005, 64:1906-1912.
90. Modugno N., Currà A., Conte A., Inghilleri M., Fofi L., Agostino R., et al. Depressed intracortical inhibition after long trains of subthreshold repetitive magnetic stimuli at low frequency. Clin Neurophysiol 2003, 114:2416-2422.
91. Modugno N., Nakamura Y., MacKinnon C.D., Filipovic S.R., Bestmann S., Berardelli A., et al. Motor cortex excitability following short trains of repetitive magnetic stimuli. Exp Brain Res 2001, 140:453-459.
92. Molina-Luna K., Pekanovic A., Röhrich S., Hertler B., Schubring-Giese M., Rioult-Pedotti M.S., et al. Dopamine in motor cortex is necessary for skill learning and synaptic plasticity. PLoS ONE 2009, 4:e7082.
93. Morgante F., Espay A.J., Gunraj C., Lang A.E., Chen R. Motor cortex plasticity in Parkinson's disease and levodopa-induced dyskinesias. Brain 2006, 129:1059-1069.
94. Münchau A., Orth M., Rothwell J.C., Di Lazzaro V., Oliviero A., Profice P., et al. Intracortical inhibition is reduced in a patient with a lesion in the posterolateral thalamus. Mov Disord 2002, 17:208-212.
95. Murase N., Cengiz B., Rothwell J.C. Inter-individual variation in the after-effect of paired associative stimulation can be predicted from short-interval intracortical inhibition with the threshold tracking method. Brain Stimul 2014, 42. Oct 2. [Epub ahead of print]. 10.1016/j.brs.2014.09.010.
96. Nakano T., Doi T., Yoshimoto J., Doya K. A kinetic model of dopamine- and calcium-dependent striatal synaptic plasticity. PLoS Comput Biol 2010, 6. e1000670.
97. Nakano T., Yoshimoto J., Doya K. A model-based prediction of the calcium responses in the striatal synaptic spines depending on the timing of cortical and dopaminergic inputs and post-synaptic spikes. Front Comput Neurosci 2013, 7:119.
98. Ni Z., Bahl N., Gunraj C.A., Mazzella F., Chen R. Increased motor cortical facilitation and decreased inhibition in Parkinson disease. Neurology 2013, 80:1746-1753.
99. Paulus W., Classen J., Cohen L.G., Large C.H., Di Lazzaro V., Nitsche M., et al. State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul 2008, 1:151-163.
100. Paillé V., Picconi B., Bagetta V., Ghiglieri V., Sgobio C., Di Filippo M., et al. Distinct levels of dopamine denervation differentially alter striatal synaptic plasticity and NMDA receptor subunit composition. J Neurosci 2010, 30:14182-14193.
101. Pascual-Leone A., Valls-Solé J., Wassermann E.M., Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994, 117:847-858.
102. Pascual-Leone A., Valls-Solé J., Brasil-Neto J.P., Cammarota A., Grafman J., Hallett M. Akinesia in Parkinson's disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology 1994, 44:892-898.
103. Picconi B., Centonze D., Håkansson K., Bernardi G., Greengard P., Fisone G., et al. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 2003, 6:501-506.
104. Picconi B., Paillé V., Ghiglieri V., Bagetta V., Barone I., Lindgren H.S., et al. L-DOPA dosage is critically involved in dyskinesia via loss of synaptic depotentiation. Neurobiol Dis 2008, 29:327-335.
105. Popa T., Velayudhan B., Hubsch C., Pradeep S., Roze E., Vidailhet M., Meunier S., Kishore A. Cerebellar processing of sensory inputs primes motor cortex plasticity. Cereb Cortex 2013, 23:305-314.
106. Prescott I.A., Dostrovsky J.O., Moro E., Hodaie M., Lozano A.M., Hutchison W.D. Levodopa enhances synaptic plasticity in the substantia nigra pars reticulata of Parkinson's disease patients. Brain 2009, 132:309-318.
107. Priori A., Berardelli A., Inghilleri M., Accornero N., Manfredi M. Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. Brain 1994, 117:317-323.
108. Remy P., Samson Y. The role of dopamine in cognition: evidence from functional imaging studies. Curr Opin Neurol 2003, 16(Suppl 2):S37-S41.
109. Ridding M.C., Inzelberg R., Rothwell J.C. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 1995, 37:181-188.
110. Romeo S., Gilio F., Pedace F., Ozkaynak S., Inghilleri M., Manfredi M., et al. Changes in the cortical silent period after repetitive magnetic stimulation of cortical motor areas. Exp Brain Res 2000, 135:504-510.
111. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009, 120:2008-2039.
112. Rothkegel H., Sommer M., Rammsayer T., Trenkwalder C., Paulus W. Training effects outweigh effects of single-session conventional rTMS and theta burst stimulation in PD patients. Neurorehabil Neural Repair 2009, 23:373-381.
113. Rothwell J.C. Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 1997, 74:113-122.
114. Rylander D., Bagetta V., Pendolino V., Zianni E., Grealish S., Gardoni F., et al. Region-specific restoration of striatal synaptic plasticity by dopamine grafts in experimental parkinsonism. Proc Natl Acad Sci U S A 2013, 110:E4375-E4384.
115. Sailer A., Molnar G.F., Paradiso G., Gunraj C.A., Lang A.E., Chen R. Short and long latency afferent inhibition in Parkinson's disease. Brain 2003, 126:1883-1894.
116. Schwingenschuh P., Ruge D., Edwards M.J., Terranova C., Katschnig P., Carrillo F., et al. Distinguishing SWEDDs patients with asymmetric resting tremor from Parkinson's disease: a clinical and electrophysiological study. Mov Disord 2010 Apr 15, 25(5):560-569.
117. Shirota Y., Ohtsu H., Hamada M., Enomoto H., Ugawa Y. Research Committee on rTMS Treatment of Parkinson's Disease. Supplementary motor area stimulation for Parkinson disease: a randomized controlled study. Neurology 2013, 80:1400-1405.
118. Siebner H.R. A primer on priming the human motor cortex. Clin Neurophysiol 2010, 121:461-463.
119. Siebner H.R., Mentschel C., Auer C., Conrad B. Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson's disease. NeuroReport 1999, 10:589-594.
120. Stefan K., Kunesch E., Cohen L.G., Benecke R., Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000, 123:572-584.
121. Stefan K., Kunesch E., Benecke R., Cohen L.G., Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 2002, 543:699-708.
122. Strafella A.P., Paus T., Fraraccio M., Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 2003, 126:2609-2615.
123. Su M., Yoshida Y., Hirata Y., Watahiki Y., Nagata K. Primary involvement of the motor area in association with the nigrostriatal pathway in multiple system atrophy: neuropathological and morphometric evaluations. Acta Neuropathol 2001, 101:57-64.
124. Suppa A., Iezzi E., Conte A., Belvisi D., Marsili L., Modugno N., et al. Dopamine influences primary motor cortex plasticity and dorsal premotor-to-motor connectivity in Parkinson's disease. Cereb Cortex 2010, 20:2224-2233.
125. Suppa A., Ortu E., Zafar N., Deriu F., Paulus W., Berardelli A., et al. Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. J Physiol 2008, 586:4489-4500.
126. 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.
127. Suppa A., Bologna M., Berardelli A. L-DOPA and cortical associative plasticity in Parkinson's disease. Clin Neurophysiol 2013, 124:638-639.
128. Suppa A., Marsili L., Di Stasio F., Latorre A., Parvez A.K., Colosimo C., et al. Primary motor cortex long-term plasticity in multiple system atrophy. Mov Disord 2014, 29:97-104.
129. Teo J.T., Swayne O.B., Rothwell J.C. Further evidence for NMDA-dependence of the after-effects of human theta burst stimulation. Clin Neurophysiol 2007, 118:1649-1651.
130. Tseng K.Y., O'Donnell P. Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 2004, 24:5131-5139.
131. Udupa K., Chen R. Motor cortical plasticity in Parkinson's disease. Front Neurol 2013, 4:128.
132. Ueki Y., Mima T., Kotb M.A., Sawada H., Saiki H., Ikeda A., et al. Altered plasticity of the human motor cortex in Parkinson's disease. Ann Neurol 2006, 59:60-71.
133. Vacherot F., Attarian S., Eusebio A., Azulay J.P. Excitability of the lower-limb area of the motor cortex in Parkinson's disease. Neurophysiol Clin 2010, 40:201-208.
134. Wang J., O'Donnell P. D1 dopamine receptors potentiate NMDA-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 2001, 11:452-462.
135. Wichmann T., DeLong M.R., Guridi J., Obeso J.A. Milestones in research on the pathophysiology of Parkinson's disease. Mov Disord 2011, 26:1032-1041.
136. Wolters A., Sandbrink F., Schlottmann A., Kunesch E., Stefan K., Cohen L.G., et al. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 2003, 89:2339-2345.
137. Yang S.N., Tang Y.G., Zucker R.S. Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol 1999, 81:781-787.
138. 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, 123:815-821.
139. Ziemann U. LTP-like plasticity in human motor cortex. Suppl Clin Neurophysiol 2004, 57:702-707.
140. Ziemann U., Paulus W., Nitsche M.A., Pascual-Leone A., Byblow W.D., Berardelli A., et al. Consensus: motor cortex plasticity protocols. Brain Stimul 2008, 1:164-182.
141. Ziemann U., Siebner H.R. Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul 2008, 1:60-66.