Motor cortical plasticity in Parkinson's disease

Kaviraja Udupa, Robert Chen, Kaviraja Udupa, Robert Chen

Abstract

In Parkinson's disease (PD), there are alterations of the basal ganglia (BG) thalamocortical networks, primarily due to degeneration of nigrostriatal dopaminergic neurons. These changes in subcortical networks lead to plastic changes in primary motor cortex (M1), which mediates cortical motor output and is a potential target for treatment of PD. Studies investigating the motor cortical plasticity using non-invasive transcranial magnetic stimulation (TMS) have found altered plasticity in PD, but there are inconsistencies among these studies. This is likely because plasticity depends on many factors such as the extent of dopaminergic loss and disease severity, response to dopaminergic replacement therapies, development of l-DOPA-induced dyskinesias (LID), the plasticity protocol used, medication, and stimulation status in patients treated with deep brain stimulation (DBS). The influences of LID and DBS on BG and M1 plasticity have been explored in animal models and in PD patients. In addition, many other factors such age, genetic factors (e.g., brain derived neurotropic factor and other neurotransmitters or receptors polymorphism), emotional state, time of the day, physical fitness have been documented to play role in the extent of plasticity induced by TMS in human studies. In this review, we summarize the studies that investigated M1 plasticity in PD and demonstrate how these afore-mentioned factors affect motor cortical plasticity in PD. We conclude that it is important to consider the clinical, demographic, and technical factors that influence various plasticity protocols while developing these protocols as diagnostic or prognostic tools in PD. We also discuss how the modulation of cortical excitability and the plasticity with these non-invasive brain stimulation techniques facilitate the understanding of the pathophysiology of PD and help design potential therapeutic possibilities in this disorder.

Keywords: M1 plasticity; Parkinson’s disease; paired associative stimulation; repetitive transcranial magnetic stimulation; theta burst stimulation; transcranial direct current stimulation; transcranial magnetic stimulation.

Figures

Figure 1
Figure 1
Schematic representation of the cascades of events involved in long-term potentiation (LTP) and depression (LTD). Different neurotransmitters are involved in these cascades. Different changes occur depending on the rate of increase of post-synaptic calcium (Ca++). Rapid influx of Ca++ preferentially promotes binding of Ca++ to the C-terminal of calmodulin, activating the kinase pathways. These reactions lead to increase in AMPA receptor density on the post-synaptic membrane resulting in LTP. On the other hand, slower release of Ca++ leads to Ca++ binding to the N-terminal of calmodulin, activating the phosphatase pathways. This leads to decrease in AMPA receptor density on the post-synaptic membrane, resulting in LTD.
Figure 2
Figure 2
(A) The basal ganglia-thalamocortical loops involved in motor control. The internal globus pallidus (GPi) is the main output nucleus of the basal ganglia and it has inhibitory projection to the thalamus. The direct pathway projects from the striatum to the GPi. Inhibition of the GPi facilitates movement by increasing thalamocortical projections. On the other hand, the indirect pathway through the external globus pallidus (GPe), subthalamic nucleus (STN), GPi, and thalamus inhibits the excitatory thalamocortical output. The hyperdirect pathway through cortico-subthalamic nucleus projection is considered to suppress motor programs through facilitation of the GPi. (B) Schematic diagram showing the center facilitation surround inhibition model. The direct pathway shown in the center facilitates the movement whereas the indirect pathway in periphery of the projection inhibits the competing motor patterns for the specific movement. STN modulates the cortex through both the hyperdirect and the indirect pathways.

References

    1. Butler AJ, Wolf SL. Putting the brain on the map: use of transcranial magnetic stimulation to assess and induce cortical plasticity of upper-extremity movement. Phys Ther (2007) 87:719–3610.2522/ptj.20060274
    1. Bliss TV, 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) 232:331–56
    1. Hebb DO. Temperament in chimpanzees; method of analysis. J Comp Physiol Psychol (1949) 42:192–20610.1037/h0056842
    1. Feldman DE. The spike-timing dependence of plasticity. Neuron (2012) 75:556–7110.1016/j.neuron.2012.08.001
    1. Rossini PM, Altamura C, Ferreri F, Melgari JM, Tecchio F, Tombini M, et al. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eura Medicophys (2007) 43:241–54
    1. Picconi B, Piccoli G, Calabresi P. Synaptic dysfunction in Parkinson’s disease. Adv Exp Med Biol (2012) 970:553–7210.1007/978-3-7091-0932-8_24
    1. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron (2004) 44:5–2110.1016/j.neuron.2004.09.012
    1. Massey PV, Bashir ZI. Long-term depression: multiple forms and implications for brain function. Trends Neurosci (2007) 30:176–8410.1016/j.tins.2007.02.005
    1. Thickbroom GW. Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res (2007) 180:583–9310.1007/s00221-007-0991-3
    1. Lang AE, Lozano AM. Parkinson’s disease. First of two parts. N Engl J Med (1998) 339:1044–5310.1056/NEJM199810153391607
    1. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging (2003) 24:197–21110.1016/S0197-4580(02)00065-9
    1. Bosch C, Mailly P, Degos B, Deniau JM, Venance L. Preservation of the hyperdirect pathway of basal ganglia in a rodent brain slice. Neuroscience (2012) 215:31–4110.1016/j.neuroscience.2012.04.033
    1. Kolomiets BP, Deniau JM, Glowinski J, Thierry AM. Basal ganglia and processing of cortical information: functional interactions between trans-striatal and trans-subthalamic circuits in the substantia nigra pars reticulata. Neuroscience (2003) 117:931–810.1016/S0306-4522(02)00824-2
    1. Nambu A, Tokuno H, Takada M. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res (2002) 43:111–710.1016/S0168-0102(02)00027-5
    1. Mink JW. The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol (2003) 60:1365–810.1001/archneur.60.10.1365
    1. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci (2006) 9:251–910.1038/nn1632
    1. Bagetta V, Ghiglieri V, Sgobio C, Calabresi P, Picconi B. Synaptic dysfunction in Parkinson’s disease. Biochem Soc Trans (2010) 38:493–710.1042/BST0380493
    1. Shen W, Flajolet M, Greengard P, Surmeier DJ. Dichotomous dopaminergic control of striatal synaptic plasticity. Science (2008) 321:848–5110.1126/science.1160575
    1. Lovinger DM. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology (2010) 58:951–6110.1016/j.neuropharm.2010.01.008
    1. Calabresi P, Centonze D, Bernardi G. Electrophysiology of dopamine in normal and denervated striatal neurons. Trends Neurosci (2000) 23:S57–6310.1016/S1471-1931(00)00017-3
    1. Lovinger DM, Partridge JG, Tang KC. Plastic control of striatal glutamatergic transmission by ensemble actions of several neurotransmitters and targets for drugs of abuse. Ann N Y Acad Sci (2003) 1003:226–4010.1196/annals.1300.014
    1. Song S, Miller KD, Abbott LF. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci (2000) 3:919–2610.1038/78829
    1. Froemke RC, Poo MM, Dan Y. Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature (2005) 434:221–510.1038/nature03366
    1. Fino E, Glowinski J, Venance L. Bidirectional activity-dependent plasticity at corticostriatal synapses. J Neurosci (2005) 25:11279–8710.1523/JNEUROSCI.4476-05.2005
    1. Letzkus JJ, Kampa BM, Stuart GJ. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J Neurosci (2006) 26:10420–910.1523/JNEUROSCI.2650-06.2006
    1. Calabresi P, Saiardi A, Pisani A, Baik JH, Centonze D, Mercuri NB, et al. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci (1997) 17:4536–44
    1. Picconi B, Ghiglieri V, Bagetta V, Barone I, Sgobio C, Calabresi P. Striatal synaptic changes in experimental Parkinsonism: role of NMDA receptor trafficking in PSD. Parkinsonism Relat Disord (2008) 14(Suppl 2):S145–910.1016/j.parkreldis.2008.04.019
    1. Picconi B, Gardoni F, Centonze D, Mauceri D, Cenci MA, Bernardi G, et al. Abnormal Ca2+-calmodulin-dependent protein kinase II function mediates synaptic and motor deficits in experimental Parkinsonism. J Neurosci (2004) 24:5283–9110.1523/JNEUROSCI.1224-04.2004
    1. Picconi B, Centonze D, Hakansson K, Bernardi G, Greengard P, Fisone G, et al. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci (2003) 6:501–6
    1. Calabresi P, Galletti F, Saggese E, Ghiglieri V, Picconi B. Neuronal networks and synaptic plasticity in Parkinson’s disease: beyond motor deficits. Parkinsonism Relat Disord (2007) 13(Suppl 3):S259–6210.1016/S1353-8020(08)70013-0
    1. Calabresi P, Maj R, Mercuri NB, Bernardi G. Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett (1992) 142:95–910.1016/0304-3940(92)90628-K
    1. Paille 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) 30:14182–9310.1523/JNEUROSCI.2149-10.2010
    1. Chen R, Cros D, Curra A, DiLazzaro V, Lefaucheur JP, Magistris MR, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol (2008) 119:504–3210.1016/j.clinph.2007.10.014
    1. Chen R, Udupa K. Measurement and modulation of plasticity of the motor system in humans using transcranial magnetic stimulation. Motor Control (2009) 13:442–53
    1. Player MJ, Taylor JL, Alonzo A, Loo CK. Paired associative stimulation increases motor cortex excitability more effectively than theta-burst stimulation. Clin Neurophysiol (2012) 123:2220–610.1016/j.clinph.2012.03.081
    1. Chistiakova M, Volgushev M. Heterosynaptic plasticity in the neocortex. Exp Brain Res (2009) 199:377–9010.1007/s00221-009-1859-5
    1. Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord (2003) 18:231–4010.1002/mds.10327
    1. Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R. Short and long latency afferent inhibition in Parkinson’s disease. Brain (2003) 126:1883–9410.1093/brain/awg183
    1. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology (2001) 57:1899–90110.1212/WNL.57.10.1899
    1. Yashiro K, Philpot BD. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology (2008) 55:1081–9410.1016/j.neuropharm.2008.07.046
    1. Gardoni F, Ghiglieri V, Luca M, Calabresi P. Assemblies of glutamate receptor subunits with post-synaptic density proteins and their alterations in Parkinson’s disease. Prog Brain Res (2010) 183:169–8210.1016/S0079-6123(10)83009-2
    1. Julkunen P, Saisanen L, Danner N, Awiszus F, Kononen M. Within-subject effect of coil-to-cortex distance on cortical electric field threshold and motor evoked potentials in transcranial magnetic stimulation. J Neurosci Methods (2012) 206:158–6410.1016/j.jneumeth.2012.02.020
    1. Roy CK, Boyle L, Burke M, Lombard W, Ryan S, McNamara B. Intra subject variation and correlation of motor potentials evoked by transcranial magnetic stimulation. Ir J Med Sci (2011) 180:873–8010.1007/s11845-011-0722-4
    1. Shirota Y, Hanajima R, Hamada M, Terao Y, Matsumoto H, Tsutsumi R, et al. Inter-individual variation in the efficient stimulation site for magnetic brainstem stimulation. Clin Neurophysiol (2011) 122:2044–810.1016/j.clinph.2011.03.025
    1. Koski L, Schrader LM, Wu AD, Stern JM. Normative data on changes in transcranial magnetic stimulation measures over a ten hour period. Clin Neurophysiol (2005) 116:2099–10910.1016/j.clinph.2005.06.006
    1. Wassermann EM. Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol (2002) 113:1165–7110.1016/S1388-2457(02)00144-X
    1. Maeda F, Gangitano M, Thall M, Pascual-Leone A. Inter- and intra-individual variability of paired-pulse curves with transcranial magnetic stimulation (TMS). Clin Neurophysiol (2002) 113:376–8210.1016/S1388-2457(02)00008-1
    1. Boroojerdi B, Kopylev L, Battaglia F, Facchini S, Ziemann U, Muellbacher W, et al. Reproducibility of intracortical inhibition and facilitation using the paired-pulse paradigm. Muscle Nerve (2000) 23:1594–710.1002/1097-4598(200010)23:10<1594::AID-MUS19>;2-3
    1. Van der KW, Zwinderman AH, Ferrari MD, van Dijk JG. Cortical excitability and response variability of transcranial magnetic stimulation. J Clin Neurophysiol (1996) 13:164–7110.1097/00004691-199603000-00007
    1. Ridding MC, Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol (2010) 588:2291–30410.1113/jphysiol.2010.190314
    1. Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R. Motor cortex plasticity in Parkinson’s disease and levodopa-induced dyskinesias. Brain (2006) 129:1059–6910.1093/brain/awl031
    1. Ueki Y, Mima T, Kotb MA, Sawada H, Saiki H, Ikeda A, et al. Altered plasticity of the human motor cortex in Parkinson’s disease. Ann Neurol (2006) 59:60–7110.1002/ana.20692
    1. 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) 21:639–4510.1002/mds.20778
    1. Schwingenschuh P, Ruge D, Edwards MJ, 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) 25:560–910.1002/mds.23019
    1. 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) 78:1441–810.1212/WNL.0b013e318253d5dd
    1. Kacar A, Filipovic SR, Kresojevic N, Milanovic SD, Ljubisavljevic M, Kostic VS, et al. History of exposure to dopaminergic medication does not affect motor cortex plasticity and excitability in Parkinson’s disease. Clin Neurophysiol (2013) 124:697–70710.1016/j.clinph.2012.09.016
    1. 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 (2013). [Epub ahead of print].10.1093/cercor/bht058
    1. Eggers C, Fink GR, Nowak DA. Theta burst stimulation over the primary motor cortex does not induce cortical plasticity in Parkinson’s disease. J Neurol (2010) 257:1669–7410.1007/s00415-010-5597-1
    1. 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) 76:601–910.1212/WNL.0b013e31820ce6bb
    1. 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) 227:296–30110.1016/j.expneurol.2010.11.020
    1. Stephani C, Nitsche MA, Sommer M, Paulus W. Impairment of motor cortex plasticity in Parkinson’s disease, as revealed by theta-burst-transcranial magnetic stimulation and transcranial random noise stimulation. Parkinsonism Relat Disord (2011) 17:297–810.1016/j.parkreldis.2011.01.006
    1. 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) 123:815–2110.1016/j.clinph.2011.07.051
    1. 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) 123:822–810.1016/j.clinph.2011.06.034
    1. 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) 135:2074–8810.1093/brain/aws124
    1. Gilio F, Curra 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) 17:467–7310.1002/mds.1255
    1. Lomarev MP, Kanchana S, Bara-Jimenez W, Iyer M, Wassermann EM, Hallett M. Placebo-controlled study of rTMS for the treatment of Parkinson’s disease. Mov Disord (2006) 21:325–3110.1002/mds.20713
    1. Buhmann C, Gorsler A, Baumer T, Hidding U, Demiralay C, Hinkelmann K, et al. Abnormal excitability of premotor-motor connections in de novo Parkinson’s disease. Brain (2004) 127:2732–4610.1093/brain/awh321
    1. Lang N, Speck S, Harms J, Rothkegel H, Paulus W, Sommer M. Dopaminergic potentiation of rTMS-induced motor cortex inhibition. Biol Psychiatry (2008) 63:231–310.1016/j.biopsych.2007.04.033
    1. Kuo MF, Paulus W, Nitsche MA. Boosting focally-induced brain plasticity by dopamine. Cereb Cortex (2008) 18:648–5110.1093/cercor/bhm098
    1. Monte-Silva K, Liebetanz D, Grundey J, Paulus W, Nitsche MA. Dosage-dependent non-linear effect of L-dopa on human motor cortex plasticity. J Physiol (2010) 588:3415–2410.1113/jphysiol.2010.190181
    1. Monte-Silva K, Kuo MF, Thirugnanasambandam N, Liebetanz D, Paulus W, Nitsche MA. Dose-dependent inverted U-shaped effect of dopamine (D2-like) receptor activation on focal and nonfocal plasticity in humans. J Neurosci (2009) 29:6124–3110.1523/JNEUROSCI.0728-09.2009
    1. Thirugnanasambandam N, Grundey J, Paulus W, Nitsche MA. Dose-dependent nonlinear effect of L-DOPA on paired associative stimulation-induced neuroplasticity in humans. J Neurosci (2011) 31:5294–910.1523/JNEUROSCI.6258-10.2011
    1. Centonze D, Grande C, Saulle E, Martin AB, Gubellini P, Pavon N, et al. Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci (2003) 23:8506–12
    1. Otani S, Daniel H, Roisin MP, Crepel F. Dopaminergic modulation of long-term synaptic plasticity in rat prefrontal neurons. Cereb Cortex (2003) 13:1251–610.1093/cercor/bhg092
    1. Gaspar P, Stepniewska I, Kaas JH. Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys. J Comp Neurol (1992) 325:1–2110.1002/cne.903250102
    1. Alexander GE, Delong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci (1986) 9:357–8110.1146/annurev.ne.09.030186.002041
    1. Delong MR, Alexander GE, Mitchell SJ, Richardson RT. The contribution of basal ganglia to limb control. Prog Brain Res (1986) 64:161–7410.1016/S0079-6123(08)63411-1
    1. Nakano K, Kayahara T, Tsutsumi T, Ushiro H. Neural circuits and functional organization of the striatum. J Neurol (2000) 247(Suppl 5):V1–1510.1007/PL00007778
    1. Ahlskog JE, Muenter MD. Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord (2001) 16:448–5810.1002/mds.1090
    1. Schrag A, Quinn N. Dyskinesias and motor fluctuations in Parkinson’s disease. A community-based study. Brain (2000) 123(Pt 11):2297–30510.1093/brain/123.11.2297
    1. Picconi B, Bagetta V, Ghiglieri V, Paille V, Di Filippo M, Pendolino V, et al. Inhibition of phosphodiesterases rescues striatal long-term depression and reduces levodopa-induced dyskinesia. Brain (2011) 134:375–8710.1093/brain/awq342
    1. Huang YZ, Rothwell JC, Lu CS, Chuang WL, Chen RS. Abnormal bidirectional plasticity-like effects in Parkinson’s disease. Brain (2011) 134:2312–2010.1093/brain/awr158
    1. Oh JD, Chase TN. Glutamate-mediated striatal dysregulation and the pathogenesis of motor response complications in Parkinson’s disease. Amino Acids (2002) 23:133–910.1007/s00726-001-0118-2
    1. Dunah AW, Standaert DG. Subcellular segregation of distinct heteromeric NMDA glutamate receptors in the striatum. J Neurochem (2003) 85:935–4310.1046/j.1471-4159.2003.01744.x
    1. Hallett PJ, Dunah AW, Ravenscroft P, Zhou S, Bezard E, Crossman AR, et al. Alterations of striatal NMDA receptor subunits associated with the development of dyskinesia in the MPTP-lesioned primate model of Parkinson’s disease. Neuropharmacology (2005) 48:503–1610.1016/j.neuropharm.2004.11.008
    1. Kim SJ, Udupa K, Gunraj C, Mazzella F, Moro E, Lozano A, et al. Effect of subthalamic nucleus stimulation on paired associated plasticity in Parkinson’s disease. Abstract Book of 38th Annual Meeting of the Society for Neuroscience, 239.21/H14. Chicago: (2009).
    1. Hamada M, Strigaro G, Murase N, Sadnicka A, Galea JM, Edwards MJ, et al. Cerebellar modulation of human associative plasticity. J Physiol (2012) 590:2365–7410.1113/jphysiol.2012.230540
    1. Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC. The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex (2012) 23:1593–60510.1093/cercor/bhs147
    1. Ghiglieri V, Pendolino V, Sgobio C, Bagetta V, Picconi B, Calabresi P. Theta-burst stimulation and striatal plasticity in experimental Parkinsonism. Exp Neurol (2012) 236:395–810.1016/j.expneurol.2012.04.020
    1. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, 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) 22:1046–5010.1002/mds.21460
    1. 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) 20:2224–3310.1093/cercor/bhp288
    1. Fregni F, Boggio PS, Santos MC, Lima M, Vieira AL, Rigonatti SP, et al. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord (2006) 21:1693–70210.1002/mds.21012
    1. Gruner U, Eggers C, Ameli M, Sarfeld AS, Fink GR, Nowak DA. 1 Hz rTMS preconditioned by tDCS over the primary motor cortex in Parkinson’s disease: effects on bradykinesia of arm and hand. J Neural Transm (2010) 117:207–1610.1007/s00702-009-0356-0
    1. Linazasoro G. New ideas on the origin of L-dopa-induced dyskinesias: age, genes and neural plasticity. Trends Pharmacol Sci (2005) 26:391–710.1016/j.tips.2005.06.007
    1. 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) 20:1926–3610.1093/cercor/bhp269
    1. Li S, Arbuthnott GW, Jutras MJ, Goldberg JA, Jaeger D. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J Neurophysiol (2007) 98:3525–3710.1152/jn.00808.2007
    1. Bahl NE, Udupa K, Gunraj C, Mazzella F, Moro E, Lozano A, et al. Induction of long-term potentiation and long-term depression-like changes in the motor cortex by pairing subthalamic deep brain stimulation and transcranial magnetic stimulation in Parkinson’s disease. Abstract Book of 40th Annual Meeting of the Society for Neuroscience, L6: 51.27. San Diego: (2010).
    1. Prescott IA, Dostrovsky JO, Moro E, Hodaie M, Lozano AM, Hutchison WD. Levodopa enhances synaptic plasticity in the substantia nigra pars reticulata of Parkinson’s disease patients. Brain (2009) 132:309–1810.1093/brain/awn322
    1. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of Parkinsonian neural circuitry. Science (2009) 324:354–910.1126/science.1167093
    1. Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, et al. Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain (2001) 124:558–7010.1093/brain/124.3.558
    1. Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, et al. Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain (2000) 123:394–40310.1093/brain/123.2.394
    1. Lefaucheur JP, Drouot X, Von Raison F, Menard-Lefaucheur I, Cesaro P, Nguyen JP. 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) 115:2530–4110.1016/j.clinph.2004.05.025
    1. Siebner HR, Rossmeier C, Mentschel C, Peinemann A, Conrad B. Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson’s disease. J Neurol Sci (2000) 178:91–410.1016/S0022-510X(00)00370-1
    1. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Hamdy A. Effect of daily repetitive transcranial magnetic stimulation on motor performance in Parkinson’s disease. Mov Disord (2006) 21:2201–510.1002/mds.21089
    1. Benninger DH, Lomarev M, Lopez G, Wassermann EM, Li X, Considine E, et al. Transcranial direct current stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry (2010) 81:1105–1110.1136/jnnp.2009.202556
    1. Pereira JB, Junque C, Bartres-Faz D, Marti MJ, Sala-Llonch R, Compta Y, et al. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson’s disease. Brain Stimul (2013) 6:16–2410.1016/j.brs.2012.01.006
    1. 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) 65:623–510.1212/01.wnl.0000172861.36430.95
    1. 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) 73:113–910.1212/WNL.0b013e3181ad5387
    1. 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) 24:246–5310.1002/mds.22348
    1. 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) 68:704–510.1212/01.wnl.0000256036.20927.a5
    1. Elahi B, Elahi B, Chen R. Effect of transcranial magnetic stimulation on Parkinson motor function – systematic review of controlled clinical trials. Mov Disord (2009) 24:357–6310.1002/mds.22364
    1. Fregni F, Simon DK, Wu A, Pascual-Leone A. Non-invasive brain stimulation for Parkinson’s disease: a systematic review and meta-analysis of the literature. J Neurol Neurosurg Psychiatry (2005) 76:1614–2310.1136/jnnp.2005.069849

Source: PubMed

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