The pathophysiology of essential tremor and parkinson's tremor

Current Neurology and Neuroscience Reports

Volumn 13, Issue 9, 2013, Pages

  Helmich, Rick C ^a,c   Toni, Ivan ^a   Deuschl, Günther ^b   Bloem, Bastiaan R ^c  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UNIVERSITY OF KIEL   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Basal ganglia; Cerebellum; Essential tremor; Neuroimaging; Parkinson's disease; Resting tremor; Thalamus

Indexed keywords

4 AMINOBUTYRIC ACID;

ANIMAL; COMPLICATION; ELECTROSTIMULATION THERAPY; ESSENTIAL TREMOR; HUMAN; METABOLISM; MOTOR DYSFUNCTION; NERVE CELL NETWORK; PARKINSON DISEASE; PATHOPHYSIOLOGY; PROCEDURES; METHODOLOGY; REVIEW;

ANIMALS; ELECTRIC STIMULATION THERAPY; ESSENTIAL TREMOR; GAMMA-AMINOBUTYRIC ACID; HUMANS; MOVEMENT DISORDERS; NERVE NET; PARKINSON DISEASE;

EID: 84880411701     PISSN: 15284042     EISSN: 15346293     Source Type: Journal    
DOI: 10.1007/s11910-013-0378-8     Document Type: Article

References (102)

1. Abdo WF, de Warrenburg BPCV, Burn DJ, Quinn NP, Bloem BR. The clinical approach to movement disorders. Nat Rev Neurol. 2010;6(1):29-37.
2. Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson's disease. Arch Neurol. 1993;50(2):140-8. (Pubitemid 23054795)
3. Deuschl G, Bain P, Brin M. Consensus statement of the Movement Disorder Society on tremor. Ad Hoc Scientific Committee. Mov Disord. 1998;13 Suppl 3:2-23. (Pubitemid 28517753)
4. Hallett M, Deuschl G. Are we making progress in the understanding of tremor in Parkinson's disease? Ann Neurol. 2010;68(6):780-1.
5. Elble RJ, Deuschl G. An update on essential tremor. Curr Neurol Neurosci Rep. 2009;9(4):273-7.
6. Anderson ME, Turner RS. Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey. J Neurophysiol. 1991;66(3):879-93.
7. Horne MK, Butler EG. The role of the cerebello-thalamo-cortical pathway in skilled movement. Prog Neurobiol. 1995;46(2-3):199-213.
8. Shinoda Y, Kano M, Futami T. Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract neurons in areas 4 and 6. Neurosci Res. 1985;2(3):133-56. (Pubitemid 15106912)
9. Mink JW. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol. 1996;50(4):381-425. (Pubitemid 27028538)
10. •• Bostan AC, Dum RP, Strick PL. The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci U S A. 2010;107(18):8452-6. This study in primates shows that the STN has anatomical projections to the cerebellar cortex via the pons.
11. Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8(11):1491-3. (Pubitemid 41573660)
12. Jain S, Lo SE, Louis ED. Common misdiagnosis of a common neurological disorder: how are we misdiagnosing essential tremor? Arch Neurol. 2006;63(8):1100-4. (Pubitemid 44232315)
13. Coria F, Gimenez-Garcia M, Samaranch L, Mora FJ, Sampol-Bas C, Pastor P. Nigrostriatal dopaminergic function in subjects with isolated action tremor. Parkinsonism Relat Disord. 2012;18(1):49-53.
14. Louis ED. Essential tremors: a family of neurodegenerative disorders? Arch Neurol. 2009;66(10):1202-8.
15. Deuschl G, Elble R. Essential tremor - neurodegenerative or nondegenerative disease towards a working definition of ET. Mov Disord. 2009;24(14):2033-41.
16. Louis ED. Essential tremor: evolving clinicopathological concepts in an era of intensive post-mortem enquiry. Lancet Neurol. 2010;9(6):613-22.
17. Rajput AH, Adler CH, Shill HA, Rajput A. Essential tremor is not a neurodegenerative disease. Neurodegener Dis Manag. 2012;2(3):259-68.
18. Rajput AH, Robinson CA, Rajput ML, Robinson SL, Rajput A. Essential tremor is not dependent upon cerebellar Purkinje cell loss. Parkinsonism Relat Disord. 2012;18(5):626-8.
19. •• Louis ED, Faust PL, Vonsattel JPG, Honig LS, Rajput A, Robinson CA, et al. Neuropathological changes in essential tremor: 33 cases compared with 21 controls. Brain. 2007;130(12):3297-307. This is the largest postmortem study in ET to date, demonstrating cerebellum and locus ceruleus disease in different subsets of patients. (Pubitemid 350209079)
20. Axelrad JE, Louis ED, Honig LS, Flores I, Ross GW, Pahwa R, et al. Reduced Purkinje cell number in essential tremor: a postmortem study. Arch Neurol. 2008;65(1):101-7.
21. Yu M, Ma K, Faust PL, Honig LS, Cortés E, Vonsattel JPG, et al. Increased number of Purkinje cell dendritic swellings in essential tremor. Eur J Neurol. 2011;19(4):625-30.
22. Louis ED, Faust PL, Ma KJ, Yu M, Cortés E, Vonsattel J-PG. Torpedoes in the cerebellar vermis in essential tremor cases vs. controls. Cerebellum. 2011;10(4):812-9.
23. Shill HA, Adler CH, Sabbagh MN, Connor DJ, Caviness JN, Hentz JG, et al. Pathologic findings in prospectively ascertained essential tremor subjects. Neurology. 2008;70(16 Pt 2):1452-5. (Pubitemid 351521939)
24. Louis ED, Faust PL, Vonsattel J-PG. Purkinje cell loss is a characteristic of essential tremor: towards a more mature understanding of pathogenesis. Parkinsonism Relat Disord. 2012;18(8):1003-4.
25. Louis ED, Babij R, Cortés E, Vonsattel J-PG, Faust PL. The inferior olivary nucleus: a postmortem study of essential tremor cases versus controls. Mov Disord. 2013;28(6):779-86.
26. Buijink AWG, Caan MWA, Tijssen MAJ, Hoogduin JM, Maurits NM, Rootselaar A-F. Decreased cerebellar fiber density in cortical myoclonic tremor but not in essential tremor. Cerebellum. 2013;12(2):199-204.
27. Klein JC, Lorenz B, Kang J-S, Baudrexel S, Seifried C, van de Loo S, et al. Diffusion tensor imaging of white matter involvement in essential tremor. Hum Brain Mapp. 2011;32(6):896-904.
28. Nicoletti G, Manners D, Novellino F, Condino F, Malucelli E, Barbiroli B, et al. Diffusion tensor MRI changes in cerebellar structures of patients with familial essential tremor. Neurology. 2010;74(12):988-94.
29. Bagepally BS, Bhatt MD, Chandran V, Saini J, Bharath RD, Vasudev MK, et al. Decrease in cerebral and cerebellar gray matter in essential tremor: a voxel-based morphometric analysis under 3T MRI. J Neuroimaging. 2011;22(3):275-8.
30. Benito-León J, Alvarez-Linera J, Hernández-Tamames JA, Alonso-Navarro H, Jiménez-Jiménez FJ, Louis ED. Brain structural changes in essential tremor: voxel-based morphometry at 3-tesla. J Neurol Sci. 2009;287(1-2):138-42.
31. Daniels C, Peller M, Wolff S, Alfke K, Witt K, Gaser C, et al. Voxel-based morphometry shows no decreases in cerebellar gray matter volume in essential tremor. Neurology. 2006;67(8):1452-6. (Pubitemid 44632071)
32. Deuschl G, Raethjen J, Hellriegel H, Elble RJ. Treatment of patients with essential tremor. Lancet Neurol. 2011;10(2):148-61.
33. Málly J, Baranyi M, Vizi ES. Change in the concentrations of amino acids in CSF and serum of patients with essential tremor. J Neural Transm. 1996;103(5):555-60. (Pubitemid 26383642)
34. Stratton SE, Lorden JF. Effect of harmaline on cells of the inferior olive in the absence of tremor: differential response of genetically dystonic and harmaline-tolerant rats. Neuroscience. 1991;41(2-3):543-9.
35. Kralic JE, Criswell HE, Osterman JL, O'Buckley TK, Wilkie ME, Matthews DB, et al. Genetic essential tremor in γ-aminobutyric acid A receptor α1 subunit knockout mice. J Clin Invest. 2005;115(3):774-9. (Pubitemid 40322254)
36. • Boecker H, Weindl A, Brooks DJ, Ceballos-Baumann AO, Liedtke C, Miederer M, et al. GABAergic dysfunction in essential tremor: an 11C-flumazenil PET study. J Nucl Med. 2010;51(7):1030-5. This study provides convincing evidence for GABAergic dysfunction in the entire cerebellothalamocortical circuit of ET patients.
37. Gironell G, Figueiras FP, Pagonabarraga J, Herance JR, Pascual-Sedano B, Trampal C, et al. Gaba and serotonin molecular neuroimaging in essential tremor: a clinical correlation study. Parkinsonism Relat Disord. 18(7):876-80.
38. •• Paris-Robidas S, Brochu E, Sintes M, Emond V, Bousquet M, Vandal M, et al. Defective dentate nucleus GABA receptors in essential tremor. Brain. 2012;135(1):105-16. This postmortem study shows reduced levels of GABA receptors in the dentate nucleus of ET patients, the extent of which is correlated with ET duration.
39. Shill HA, Adler CH, Beach TG, Lue L-F, Caviness JN, Sabbagh MN, et al. Brain biochemistry in autopsied patients with essential tremor. Mov Disord. 2011;27(1):113-7.
40. Deuschl G. Locus coeruleus dysfunction: a feature of essential or senile tremor? Mov Disord. 2012;27(1):1-2.
41. Thier S, Kuhlenbäumer G, Lorenz D, Nothnagel M, Nebel A, Christensen K, et al. GABAA receptor- and GABA transporter polymorphisms and risk for essential tremor. Eur J Neurol. 2010;18(8):1098-100.
42. García-Martín E, Martínez C, Alonso-Navarro H, Benito-León J, Lorenzo-Betancor O, Pastor P, et al. Gamma-aminobutyric acid (GABA) receptor rho (GABRR) polymorphisms and risk for essential tremor. J Neurol. 2011;258(2):203-11.
43. García-Martín E, Martínez C, Alonso-Navarro H, Benito-León J, Lorenzo-Betancor O, Pastor P, et al. Gamma-aminobutyric acid GABRA4, GABRE, and GABRQ receptor polymorphisms and risk for essential tremor. Pharmacogenet Genomics. 2011;21(7):436-9.
44. Llinás RR. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science. 1988;242(4886):1654-64. (Pubitemid 19022170)
45. Jahnsen H. Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol (Lond). 1986;372:129-47. (Pubitemid 16048146)
46. Nieuwenhuys R, Voogd J, Van Huijzen C, van Huijzen C, Voogd J. The human central nervous system. New York: Springer; 2008.
47. Raethjen J, Govindan RB, Kopper F, Muthuraman M, Deuschl G. Cortical involvement in the generation of essential tremor. J Neurophysiol. 2007;97(5):3219-28. (Pubitemid 47084739)
48. Hurtado JM, Gray CM, Tamas LB, Sigvardt KA. Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. Proc Natl Acad Sci U S A. 1999;96(4):1674-9. (Pubitemid 29098510)
49. Hurtado JM. Temporal evolution of oscillations and synchrony in GPi/muscle pairs in Parkinson's disease. J Neurophysiol. 2005;93(3):1569-84. (Pubitemid 40283741)
50. • Pedrosa DJ, Reck C, Florin E, Pauls K, et al. Essential tremor and tremor in Parkinson's disease are associated with distinct 'tremor clusters' in the ventral thalamus. Exp Neurol. 2012;237(2). This study shows multiple distinct tremor clusters in the thalamus of ET and PD patients, suggesting that different tremor loops may be involved.
51. Pollok B, Gross J, Dirks M, Timmermann L, Schnitzler A. The cerebral oscillatory network of voluntary tremor. J Physiol (Lond). 2004;554(Pt 3):871-8. (Pubitemid 38219898)
52. Schnitzler A, Münks C, Butz M, Timmermann L, Gross J. Synchronized brain network associated with essential tremor as revealed by magnetoencephalography. Mov Disord. 2009;24(11):1629-35.
53. Timmermann L, Gross J, Dirks M, Volkmann J, Freund H-J, Schnitzler A. The cerebral oscillatory network of parkinsonian resting tremor. Brain. 2003;126(Pt 1):199-212. (Pubitemid 36068570)
54. •• Muthuraman M, Heute U, Arning K, Anwar AR, Elble R, Deuschl G, et al. Oscillating central motor networks in pathological tremors and voluntary movements. What makes the difference? NeuroImage. 2012;60(2):1331-9. This study demonstrates how bidirectional thalamocortical interactions distinguish ET and PD resting tremor from voluntary tremor.
55. Raethjen J, Deuschl G. The oscillating central network of essential tremor. Clin Neurophysiol. 2012;123(1):61-4.
56. Dupuis MJ-M, Evrard FL, Jacquerye PG, Picard GR, Lermen OG. Disappearance of essential tremor after stroke. Mov Disord. 2010;25(16):2884-7.
57. Chahine LM, Ghosh D. Essential tremor after ipsilateral cerebellar hemispherectomy: support for the thalamus as the central oscillator. J Child Neurol. 2009;24(7):861-4.
58. Helmich RC, Hallett M, Deuschl G, Toni I, Bloem BR. Cerebral causes and consequences of parkinsonian resting tremor: a tale of two circuits? Brain. 2012;135(Pt 11):3206-26.
59. Zirh TA, Lenz FA, Reich SG, Dougherty PM. Patterns of bursting occurring in thalamic cells during parkinsonian tremor. Neuroscience. 1998;83(1):107-21. (Pubitemid 28068042)
60. Magnin M, Morel A, Jeanmonod D. Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience. 2000;96(3):549-64. (Pubitemid 30136320)
61. Llinás R, Urbano FJ, Leznik E, Ramírez RR, van Marle HJF. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 2005;28(6):325-33. (Pubitemid 40775778)
62. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989;12(10):366-75. (Pubitemid 19238787)
63. Atkinson JD, Collins DL, Bertrand G, Peters TM, Pike GB, Sadikot AF. Optimal location of thalamotomy lesions for tremor associated with Parkinson disease: a probabilistic analysis based on postoperative magnetic resonance imaging and an integrated digital atlas. J Neurosurg. 2002;96(5):854-66. (Pubitemid 34415399)
64. Plaha P, Khan S, Gill SS. Bilateral stimulation of the caudal zona incerta nucleus for tremor control. J Neurol Neurosurg Psychiatr. 2008;79(5):504-13. (Pubitemid 351571866)
65. Barthó P, Freund TF, Acsády L. Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci. 2002;16(6):999-1014. (Pubitemid 35463550)
66. Sánchez-González MA, García-Cabezas MA, Rico B, Cavada C. The primate thalamus is a key target for brain dopamine. J Neurosci. 2005;25(26):6076-83. (Pubitemid 40923474)
67. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, et al. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet. 1991;337(8738):403-6.
68. Krack P, Pollak P, Limousin P, Benazzouz A, Benabid AL. Stimulation of subthalamic nucleus alleviates tremor in Parkinson's disease. Lancet. 1997;350(9092):1675. (Pubitemid 28036830)
69. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, et al. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 1998;21(1):32-8. (Pubitemid 128766376)
70. Bar-Gad I, Heimer G, Ritov Y, Bergman H. Functional correlations between neighboring neurons in the primate globus pallidus are weak or nonexistent. J Neurosci. 2003;23(10):4012-6. (Pubitemid 36958418)
71. Filion M, Tremblay L, Bédard PJ. Abnormal influences of passive limb movement on the activity of globus pallidus neurons in parkinsonian monkeys. Brain Res. 1988;444(1):165-76. (Pubitemid 18071205)
72. Pessiglione M. Thalamic neuronal activity in dopamine-depleted primates: evidence for a loss of functional segregation within basal ganglia circuits. J Neurosci. 2005;25(6):1523-31. (Pubitemid 40250728)
73. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J Neurosci. 2002;22(7):2855-61. (Pubitemid 37465834)
74. Plenz D, Kital ST. A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature. 1999;400(6745):677-82. (Pubitemid 29382573)
75. Dovzhenok A, Rubchinsky LL. On the origin of tremor in Parkinson's disease. PLoS One. 2012;7(7):e41598.
76. •• Helmich RC, Janssen MJR, Oyen WJG, Bloem BR, Toni I. Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson tremor. Ann Neurol. 2011;69(2):269-81. With use of combined single photon emission computed tomography and EMG-functional MRI, this study shows that altered interactions between the basal ganglia and cerebellothalamocortical circuit are associated with PD resting tremor.
77. Hirsch EC, Mouatt A, Faucheux B, Bonnet AM, Javoy-Agid F, Graybiel AM, et al. Dopamine, tremor, and Parkinson's disease. Lancet. 1992;340(8811):125-6.
78. Jan C, François C, Tandé D, Yelnik J, Tremblay L, Agid Y, et al. Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients. Eur J Neurosci. 2000;12(12):4525-35. (Pubitemid 32037860)
79. Isaias IU, Marzegan A, Pezzoli G, Marotta G, Canesi M, Biella GEM, et al. A role for locus coeruleus in Parkinson tremor. Front Hum Neurosci. 2011;5:179.
80. Prodoehl J, Planetta PJ, Kurani AS, Comella CL, Corcos DM, Vaillancourt DE. Differences in brain activation between tremor- and nontremor-dominant Parkinson disease. JAMA Neurol. 2013;70(1):100-6.
81. Deuschl G, Wilms H, Krack P, Würker M, Heiss WD. Function of the cerebellum in Parkinsonian rest tremor and Holmes' tremor. Ann Neurol. 1999;46(1):126-8. (Pubitemid 29314393)
82. Jankovic J, Schwartz KS, Ondo W. Re-emergent tremor of Parkinson's disease. J Neurol Neurosurg Psychiatr. 1999;67(5):646-50. (Pubitemid 29486214)
83. Louis ED, Levy G, Côte LJ, Mejia H, Fahn S, Marder K. Clinical correlates of action tremor in Parkinson disease. Arch Neurol. 2001;58(10):1630-4. (Pubitemid 32963227)
84. Raethjen J, Pohle S, Govindan R, Morsnowski A, Wenzelburger R, Deuschl G. Parkinsonian action tremor: interference with object manipulation and lacking levodopa response. Exp Neurol. 2005;194(1):151-60. (Pubitemid 40719751)
85. Papengut F, Raethjen J, Binder A, Deuschl G. Rest tremor suppression may separate essential from Parkinsonian rest tremor. Parkinsonism Relat Disord. 2013;19(7):693-7.
86. Sturman MM. Effects of subthalamic nucleus stimulation and medication on resting and postural tremor in Parkinson's disease. Brain. 2004;127(9):2131-43. (Pubitemid 39150270)
87. Ni Z, Pinto AD, Lang AE, Chen R. Involvement of the cerebellothalamocortical pathway in Parkinson disease. Ann Neurol. 2010;68(6):816-24.
88. Reck C, Himmel M, Florin E, Maarouf M, Sturm V, Wojtecki L, et al. Coherence analysis of local field potentials in the subthalamic nucleus: differences in parkinsonian rest and postural tremor. Eur J Neurosci. 2010;32(7):1202-14.
89. Loane C, Wu K, Bain P, Brooks DJ, Piccini P, Politis M. Serotonergic loss in motor circuitries correlates with severity of action-postural tremor in PD. Neurology. 2013;80(20):1850-5.
90. Doder M, Rabiner EA, Turjanski N, Lees AJ, Brooks DJ. Tremor in Parkinson's disease and serotonergic dysfunction: an 11C-WAY 100635 PET study. Neurology. 2003;60(4):601-5. (Pubitemid 36246076)
91. • Muthuraman M, Hossen A, Heute U, Deuschl G, Raethjen J. A new diagnostic test to distinguish tremulous Parkinson's disease from advanced essential tremor. Mov Disord. 2011;26(8):1548-52. With use of accelerometry, this study shows qualitative differences between ET and action tremor in PD.
92. •• Sandvik U, Koskinen L-O, Lundquist A, Blomstedt P. Thalamic and subthalamic deep brain stimulation for essential tremor. Neurosurgery. 2012;70(4):840-6. This study shows that DBS of the posterior subthalamic area is effective in treating ET.
93. Contarino MF, Speelman JD, de Bie RMA, Schuurman PR, van den Munckhof P. Bilateral cerebellorubrothalamic fibers stimulation for essential tremor? Mov Disord. 2011;26(7):1366-7.
94. Herzog J, Hamel W, Wenzelburger R, Pötter M, Pinsker MO, Bartussek J, et al. Kinematic analysis of thalamic versus subthalamic neurostimulation in postural and intention tremor. Brain. 2007;130(Pt 6):1608-25. (Pubitemid 47355924)
95. Wu T, Hallett M. The cerebellum in Parkinson's disease. Brain. 2013;136(3):696-709.
96. Zhou J, Gennatas ED, Kramer JH, Miller BL, Seeley WW. Predicting regional neurodegeneration from the healthy brain functional connectome. Neuron. 2012;73(6):1216-27.
97. Hacker C, Perlmutter J, Criswell S, Ances B, Snyder A. Resting state functional connectivity of the striatum in Parkinson's disease. Brain. 2012;135(Pt 12):3699-711.
98. Novellino F, Cherubini A, Chiriaco C, Morelli M, Salsone M, Arabia G, et al. Brain iron deposition in essential tremor: a quantitative 3-tesla magnetic resonance imaging study. Mov Disord. 2012;28(2):196-200.
99. Rossi M, Ruottinen H, Soimakallio S, Elovaara I, Dastidar P. Clinical MRI for iron detection in Parkinson's disease. Clin Imaging. 2013;37(4):631-6.
100. •• Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron. 2011;72(2):370-84. This study in primates shows that closed-loop DBS, where motor cortex activity is used to change GPi DBS parameters, is superior to standard DBS. It shows that network parameters can be used to substantially improve therapies.
101. •• Brittain J-S, Probert-Smith P, Aziz TZ, Brown P. Tremor suppression by rhythmic transcranial current stimulation. Curr Biol. 2013;5:436-40. This study demonstrates robust tremor reduction in PD by means of phase cancellation through transcranial alternating current stimulation over the motor cortex.
102. Wang S-Y, Aziz TZ, Stein JF, Liu X. Time-frequency analysis of transient neuromuscular events: dynamic changes in activity of the subthalamic nucleus and forearm muscles related to the intermittent resting tremor. J Neurosci Methods. 2005;145(1-2):151-8. (Pubitemid 40732441)