Neurophysiological measures in amyotrophic lateral sclerosis: Markers of progression in clinical trials

Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders

Volumn 6, Issue 1, 2005, Pages 17-28

  de Carvalho, Mamede ^a   Chio, Adriano ^b   Dengler, Reinhard ^c   Hecht, Martin ^d   Weber, Markus ^e   Swash, Michael ^f  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF TURIN   (Italy)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^f QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis; Cortical magnetic stimulation; Disease progression; Electromyography; Motor unit number estimation

Indexed keywords

ALCOHOL; BACLOFEN; BENZODIAZEPINE DERIVATIVE; CLOMIPRAMINE; RILUZOLE;

ACTION POTENTIAL; AMPLITUDE MODULATION; AMYOTROPHIC LATERAL SCLEROSIS; CLINICAL PRACTICE; CLINICAL STUDY; DIAGNOSTIC VALUE; DISEASE COURSE; DISEASE MARKER; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; EXCITATION CONTRACTION COUPLING; HUMAN; INTERMETHOD COMPARISON; METHODOLOGY; MOTONEURON; MOTOR CORTEX; MOTOR NERVE CONDUCTION; MOTOR UNIT; MUSCLE ACTION POTENTIAL; MUSCLE STRENGTH; NEUROPHYSIOLOGY; PRIORITY JOURNAL; RELIABILITY; REVIEW; SENSITIVITY ANALYSIS; TRANSCRANIAL MAGNETIC STIMULATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOLOGICAL MARKERS; CLINICAL TRIALS; DISEASE PROGRESSION; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, MOTOR; HUMANS; MAGNETICS; MOTOR NEURONS; NEUROPHYSIOLOGY;

EID: 18744416553     PISSN: 14660822     EISSN: None     Source Type: Journal    
DOI: 10.1080/14660820410020600     Document Type: Review

References (140)

1. Kelly JJ, Thibodeau L, Andres PL, Finison LJ. Use of electrophysiological tests to measure disease progression in ALS therapeutic trials. Muscle Nerve. 1990;13:471-9.
2. Kent-Braun JA, Walker CH, Winer MW, Miller RG. Functional significance of upper and lower motor neuron impairment in amyotrophic lateral sclerosis. Muscle Nerve. 1998;21:762-8.
3. De Carvalho M, Swash M. Nerve conduction studies in amyotrophic lateral sclerosis. Muscle Nerve. 2000;23:344-52.
4. Yuen E, Olney R. Longitudinal study of fibre density and motor unit estimates in patients with amyotrophic lateral sclerosis. Neurology. 1997;49:573-8.
5. Hansen S, Balantyne JP. A quantitative study of motor neurone disease. J Neurol Neurosurg Psychiatry. 1978;41:773-83.
6. Wang FC, Delwaide PJ. Number and relative size of thenar motor units in ALS patients: application of the adapted multiple point stimulation method. Electroencephalogr Clin Neurophysiol. 1998;109:36-43.
7. de Carvalho M. Compound muscle action potential. Amyotroph Lat Scler. 2002;3(Suppl 1):S103-S4.
8. de Carvalho M, Lopes A, Scotto M, Swash M. Reproducibility of neurophysiological and myometric measurement in the ulnar nerve-abductor digiti minimi system. Muscle Nerve. 2001;24:1391-5.
9. Bigland B, Lippold OCJ. The relationship between force, velocity and integrated electrical activity in human muscle. J Physiol (Lond), 1954;123:214-24.
10. Bromberg M, Fries T. Forshew D, Tandan R. Electrophysiological endpoint measures in a multicentre ALS drug trial. J Neurol Sci. 2001;184:51-4.
11. Daube JR. Electrophysiological studies in the diagnosis and prognosis of motor neuron diseases. Neurol Clin. 1985;3:473-93.
12. de Carvalho M, Scotto M, Lopes A, Swash M. Clinical and neurophysiological evaluation of progression in amyotrophic lateral sclerosis. Muscle Nerve. 2003;28:630-3.
13. Brooke MH, Florence JM, Heller SL. Controlled trial of thyrotropin releasing hormone in amyotrophic lateral sclerosis. Neurology. 1986;36:146-51.
14. Mitsumoto H, Salgado ED, Negroski D. Amyotrophic lateral sclerosis: effects of acute intravenous and chronic subcutaneous administration of thyrotropin releasing hormone in controlled trials, Neurology. 1986;36:152-9.
15. The ALS CNTF treatment study (ACTS) Phase II-III Group: longitudinal electrodiagnostic studies in amyotrophic lateral sclerosis patients treated with recombinant human ciliary neurotrophic factor. Neurology. 1995;45(Suppl 4):A448.
16. Kaji R, Kodama M, Imamura A, et al. Effect of ultra-high dose methylcobalamin on compound muscle action potential in amyotrophic lateral sclerosis: a double-blind controlled study. Muscle Nerve. 1998;21:1775-1178.
17. Askmark H, Aquilonius SM, Gillberg PG, Liedholm LJ, Stalberg E, Wuopio R. A pilot trial of dextromethorphan in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1993;56:197-200.
18. Dengler R. Quantitative compound muscle action potential: Con. Amyotroph Lat Scler. 2002;3(Suppl 1):S105-7.
19. de Carvalho M, Scotto M, Lopes A, Swash M. F-waves and the corticospinal lesion in amyotrophic lateral sclerosis. Amyotroph Lat Scler. 2002;3:131-6.
20. Drory VE, Kovach I, Groozman GB. Electrophysiological evaluation of upper motor involvement in amyotrophic lateral sclerosis. Amyotroph Lat Scler. 2001;2:147-52.
21. Sahrman SA, Norton BJ. The relationship of voluntary movement to spasticity in the upper motor neuron syndrome. Ann Neurol. 1977;2:460-5.
22. de Carvalho M, Scotto M, Lopes A, Swash M. Measurements of progression in ALS (abstract). Amyotroph Lat Scler. 2003;4(Suppl 1):44.
23. Stalberg E, Schwartz MS, Trontelj IV. Single fibre electromyography in various processes affecting the anterior horn cell. J Neurol Sci. 1974;24:403-15.
24. Stalberg E. Electromyographical studies of reinnervation in ALS. Adv Neurol. 1982;36:47-59.
25. Swash M, Schwartz MS. A longitudinal study of changes in motor units in motor neurone disease. J Neurol Sci. 1982;56:185-97.
26. Gooch CL, Harati Y. Longitudinal tracking of the same single motor unit in amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:511-3.
27. Chan KM, Stashuk DN, Brown WF. A longitudinal study of the pathophysiological changes in single human thenar motor units in amyotrophic lateral sclerosis. Muscle Nerve. 1998;21:1714-23.
28. McComas AJ, Fawcett PRW, Campbell MJ, Sica REP. Electrophysiological estimation of the number of motor units within a human muscle. J Neurol Neurosurg Psychiatry. 1971;34:121-31.
29. Daube JR. Electrodiagnostic studies in amyotrophic lateral sclerosis. Muscle Nerve. 2000;23:1488-502.
30. Dantes M, McComas A. The extent and time course of motor neuron involvement in amyotrophic lateral sclerosis. Muscle Nerve. 1991;14:416-21.
31. McComas AJ. Motor unit estimation: anxieties and achievements. Muscle Nerve. 1995; 18:369-79.
32. Kadrie HA, Yates SK, Milner-Brown HS, Brown WF. Multiple point electrical stimulation of ulnar and median nerves. J Neurol Neurosurg Psychiatry. 1976;39:973-85.
33. Wang FC, Delwaide PJ. Number and relative size of thenar motor units estimated by an adapted multiple point stimulation method. Muscle Nerve. 1995;18:969-79.
34. Daube JR. Estimating the number of motor units in a muscle. J Clin Neurophysiol. 1995;12:585-94.
35. Shefner JM, Jillapalli D, Bradshaw DY. Reducing intersubject variability in motor unit number estimation. Muscle Nerve. 1999;22:1457-80.
36. Brown WF, Strong MJ, Snow R. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with ageing. Muscle Nerve. 1988;11:423-32.
37. Stashuk DW, Doherty TJ, Kassam A, Brown WF. MUNE based on the automated analysis of F-responses. Muscle Nerve. 1994;17:881-90.
38. Felice KJ. A longitudinal study comparing thenar motor unit number estimate to other quantitative tests in patients with amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:179-85.
39. Gooch CT, Harati Y. Motor unit number estimation, ALS and clinical trials. ALS. 2000;1:71-82.
40. Gooch CT, Pleitez M, Ciabarra T, Kaufmann P, Haraty Y. Motor unit survival in a controlled trial of xaliproden, with and without riluzole, for the treatment of ALS. Ann Neurol. 2001;50:S23.
41. Smith BE, Clarke JC, Litchy WJ. Longitudinal electrodiagnosis studies in ALS patients treated with recombinant human ciliary neurotrophic factor. Neurology. 1995;45(Suppl 4):A448.
42. Doherty TJ, Brown WF. A method for the longitudinal study of human thenar motor units. Muscle Nerve. 1994;17:1029-36.
43. Felice KJ. Thenar motor unit number estimates using the multiple point stimulation technique: reproducibility studies in ALS patients and normal subjects. Muscle Nerve. 1995;18:1412-6.
44. Gooch CL, Wagner T. Longitudinal S-MUAP tracking and MUNE: validity of a combined method (abstract). Muscle Nerve. 1998;21:1601.
45. Bromberg MB, Larson WL. Relationship between motor unit estimates and isometric strength in distal muscles in ALS/MND. J Neurol Sci. 1996;139(suppl):38-42.
46. Olney RK, Yuen EC, Engstrom JW. Statistical motor unit number estimation: reproducibility and sources of error in patients with amyotrophic lateral sclerosis. Muscle Nerve. 2000;23:193-7.
47. Lomen-Hoerth C, Olney RK. Comparison of multiple point and statistical motor unit number estimation. Muscle Nerve. 2000;23:1525-33.
48. Simmons Z, Stashuk D, Brown WF. MUNE using an automated F-response technique: reproducibility of results. Muscle Nerve. 1994;17:1120.
49. Bromberg ME. Motor unit estimation: reproducibility of the spike triggered averaging technique in normal and ALS subjects. Muscle Nerve. 1993;16:466-71.
50. Lomen-Hoerth C, Olney RK. Effect of recording window and stimulation variables on the statistical technique of motor unit number estimation. Muscle Nerve. 2001;24:1659-64.
51. Henderson RD, McClelland R, Daube JR. Effect of changing data collection parameters on statistical motor unit number estimates. Muscle Nerve. 2003;27:320-31.
52. Brown WF, Jaatoul N. Amyotrophic lateral sclerosis. Electrophysiological study (number of motor units and rate of decay of motor units). Arch Neurol. 1978;30:242-8.
53. Wang FC, Bouquiaux O, De Pasqua V, Delwaide PJ. Changes in motor unit numbers in patients with ALS: a longitudinal study using the adapted multiple point stimulation method. Amyotroph Lat Scler. 2002;3:31-8.
54. Felice KJ. Nerve conduction velocities of single thenar motor axons based on the automated analysis of F-waves in amyotrophic lateral sclerosis. Muscle Nerve. 1998;21:756-61.
55. Shefner JM, Cudkowitz ME, Brown RH. Comparison of incremental with multipoint MUNE in transgenic ALS mice. Muscle Nerve. 2002;25:39-42.
56. Olney RK, Lomen-Hoerth C. Motor unit number estimation (MUNE): how may it contribute to the diagnosis of ALS? Amyotroph Lat Scler. 2000;1(Suppl 2):S41-S4.
57. Armon C, Brandstater ME. Motor unit number estimate-based rates of progression of ALS predict patient survival. Muscle Nerve. 1999;22:1571-5.
58. Rothwell JC, Hallet M, Berardelli A, Eisen A, Rossini P, Paulus W. Magnetic stimulation: motor evoked potentials. In: Deuschl G, Eisen A, editors. Recommendations for the practice of clinical neurophysiology: guidelines of the International Federation of Clinical Neurophysiology. 1999: 99.
59. Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:1137-41.
60. de Carvalho M, Miranda PC, Jardim L, Gabriel F, Falcão F. Reproducibility of corticomotor threshold: some observations. Muscle Nerve. 1999;22:538-9.
61. Eisen A, Pant B, Stewart H. Cortical excitability in amyotrophic lateral sclerosis: a clue to pathogenesis. Can J Neurol Sci. 1993;20:11-6.
62. Schwenkreis P, Liepert J, Witscher K, et al. Riluzole suppresses motor cortex facilitation in correlation to its plasma level. A study using transcranial magnetic stimulation. Exp Brain Res. 2000;135:293-9.
63. de Carvalho M, Evangelista T, Sales-Luis ML. The corticomotor threshold is not dependent on disease duration in amyotrophic lateral sclerosis (ALS). Amyotroph Lat Scler. 2002;3:39-42.
64. Zanette G, Tamburin S, Manganotti P, Refatti N, Forgione A, Rizzuto N. Different mechanisms contribute to motor cortex hyperexcitability in amyotrophic lateral sclerosis. Clin Neurophysiol. 2002;113:1688-97.
65. Ziemann U, Winter M, Reimers CD, Reimers K, Tergau F, Paulus W. Impaired motor cortex inhibition in patients with amyotrophic lateral sclerosis. Evidence from paired transcranial magnetic stimulation. Neurology. 1997;49:1292-8.
66. Caramia MD, Cicinelli P, Paradiso C, et al. Excitability changes of muscular responses to magnetic brain stimulation in patients with central motor disorders. Electroencephalogr Clin Neurophysiol. 1991;81:243-50.
67. Desiato MT, Bernardi G, Hagi HA, Boffa L, Caramia MD. Transcranial magnetic stimulation of motor pathways directed to muscles supplied by cranial nerves in amyotrophic lateral sclerosis. Clin Neurophysiol. 2002;113:132-40.
68. Salerno A, Carlander B, Camu W, Georgesco M. Motor evoked potentials (MEPs): evaluation of the different types of responses in amyotrophic lateral sclerosis and primary lateral sclerosis. Electromyogr Clin Neurophysiol. 1996;36:361-8.
69. Eisen A, Shytbel W, Murphy K, Hoirch M. Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve. 1990;13:146-51.
70. de Carvalho M, Miranda PC, Luis ML, Ducla-Soares E. Cortical muscle representation in amyotrophic lateral sclerosis patients: changes with disease evolution. Muscle Nerve. 1999;22:1684-92.
71. Weber M, Eisen A, Nakajima M. Corticomotoneuronal activity in ALS: changes in the peristimulus time histogram over time. Clin Neurophysiol. 2000a;111:169-77,
72. Zanette G, Tamburin S, Manganotti P, Refatti N, Forgione A, Rizzuto N. Changes in motor cortex inhibition over time in patients with amyotrophic lateral sclerosis. J Neurol. 2002;249:1723-8.
73. Brouwer B, Ashby P. Corticospinal projections to upper and lower limb spinal motor neurons in man. Electroencephalogr Clin Neurophysiol. 1990;76:509-19.
74. Chen R, Tam A, Butefisch C, et al. Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol. 1998;80:2870-81.
75. Kiers L, Cros D, Chiappa KH, Fang J. Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1993;89:415-23.
76. Uozumi T, Tsuji S, Murai Y. Motor potentials evoked by magnetic stimulation of the motor cortex in normal subjects and patients with motor disorders. Electroencephalogr Clin Neurophysiol. 1991;81:251-6.
77. Trompetto C, Caponnetto C, Buccolieri A, Marchese R, Abbruzzese G, Responses of masseter muscles to transcranial magnetic stimulation in patients with amyotrophic lateral sclerosis. Electroencephalogr Clin Neurophysiol. 1998;109:309-14.
78. Urban PP, Vogt T, Hopf HC. Corticobulbar tract involvement in amyotrophic lateral sclerosis: a transcranial magnetic stimulation study. Brain. 1998;121:1099-108.
79. Urban PP, Wicht S, Hopf HC. Sensitivity of transcranial magnetic stimulation of cortico-bulbar vs. cortico-spinal tract involvement in amyotrophic lateral sclerosis. J Neurol. 2001;248:850-5.
80. Weber M, Eisen A, Stewart H, Hirota N. The split hand in ALS has a cortical basis. J Neurol Sci. 2000;180:66-70.
81. Weber M, Eisen A. Magnetic stimulation of the central and peripheral nervous system. Muscle Nerve. 2002;25:160-75.
82. Ingram DA, Swash M. Central motor conduction time is abnormal in motor neurone disease. J Neurol Neurosurg Psychiatry. 1987;50:59-66.
83. Triggs WJ, Menkes D, Onorato J, et al. Transcranial magnetic stimulation identifies upper motor neuron involvement in motor neurone disease. Neurology. 1999;53:605-11.
84. Schriefer TN, Hess CW, Mills KR, Murray NM. Central motor conduction studies in motor neurone disease using magnetic brain stimulation. J Neurol Sci. 1989;74:431-7.
85. Claus D, Brunholzl C, Kerling FP, Henschel S. Transcranial magnetic stimulation as a diagnostic and prognostic test in amyotrophic lateral sclerosis. J Neurol Sci. 1995;1 29(suppl):30-4.
86. Mills KR, Nithi KA. Peripheral and central motor conduction in amyotrophic lateral sclerosis. J Neurol Sci. 1998;159:82-7.
87. Cruz-Martinez A, Trejo JM. Transcranial magnetic stimulation in amyotrophic and primary lateral sclerosis. Electromyogr Clin Neurophysiol. 1999;39:285-8.
88. Pohl C, Block W, Traber F, et al. Proton magnetic resonance spectroscopy and transcranial magnetic stimulation for the detection of upper motor neuron degeneration in ALS patients. J Neurol Sci. 2001;190:21-7.
89. Schulte-Mattler WJ, Muller T, Zierz S. Transcranial magnetic stimulation compared with upper motor neuron signs in patients with amyotrophic lateral sclerosis. J Neurol Sci. 1999;170:51-6.
90. de Carvalho M, Turkman A, Swash M. Motor responses evoked by transcranial magnetic stimulation and peripheral nerve stimulation in the ulnar innervation in amyotrophic lateral sclerosis: the effect of upper and lower motor neuron lesion. J Neurol Sci. 2003;210:83-90.
91. Eisen A, Swash M. Clinical neurophysiology in ALS. Clin Neurophysiol. 2001;112:2190-201.
92. Prout AJ, Eisen AA. The cortical silent period and amyotrophic lateral sclerosis. Muscle Nerve. 1994;17:217-23.
93. Desiato MT, Caramia MD. Towards a neurophysiological marker of amyotrophic lateral sclerosis as revealed by changes in cortical excitability. Electroencephalogr Clin Neurophysiol. 1997;105:1-7.
94. Siciliano G, Manca ML, Sagliocco L, et al. Cortical silent period in patients with amyotrophic lateral sclerosis. J Neurol Sci. 1999;169:93-7.
95. Kujirai T, Caramia JC, Day BL, et al. Cortical-cortical inhibition in human motor cortex. J Physiol (London). 1992;471:501-19.
96. Ziemann U, Rothwell JC, Riding MC. Interaction between intracortical inhibition and facilitation in the human cortex. J Physiol (London). 1996;496:873-81.
97. Pierantozzi M, Palmieri MG, Marciani MG, et al. Effect of apomorphine on cortical inhibition in Parkinson's disease patients: a transcranial magnetic stimulation study. Exp Brain Res. 2001;141:52-62.
98. Liepert J, Bar KJ, Maske U, et al. Motor cortex inhibition in Alzheimer's disease. Clin Neurophysiol. 2001;112: 1436-41.
99. Manganotti P, Tamburin S, Zanette G, et al. Hyperexcitable cortical responses in progressive myoclonic epilepsy: a transcortical magnetic stimulation study. Neurology. 2001;57:1793-9.
100. Sandbrink F, Syed NA, Fuji K, et al. Motor excitability in stiff person syndrome. Brain. 2000;133:2231-9.
101. Yokota T, Yoshino A, Inaba A, et al. Double cortical stimulation in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1996;61:596-600.
102. Sommer M, Tergau F, Wischer S, et al. Riluzole does not have an acute effect on motor thresholds and intracortical excitability in amyotrophic lateral sclerosis. J Neurol. 1999;246(Suppl 3):22-6.
103. 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.
104. Peinemann A, Lehner C, Conrad B, et al. Age-related decrease in paired pulse intracortical inhibition in the human primary motor cortex. Neurosci Letts. 2001;313:33-6.
105. Boroojerdi B, Kopylev L, Battaglia F, et al. Reproducibility of intracortical inhibition and facilitation using a paired pulse paradigm. Muscle Nerve. 2000;23:1594-7.
106. Ziemann U, Steinhoff BJ, Lonnecker S, et al. Inhibition of human motor cortex by ethanol. Brain. 1995;118:1437-46.
107. Ziemann U, Lonnecker S, Steinhoff BJ, et al. The effect of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996;40:367-78.
108. Ziemann U, Lonnecker S, Steinhoff BJ. The effect of lorazepam on motor cortex excitability in man. Exp Brain Res. 1996;109:127-35.
109. Manganotti P, Bortolomasi M, Zanette G, et al. Intravenous clomipramine decreases excitability of human motor cortex: a study with paired magnetic stimulation. J Neurol Sci. 2001;184:27-32.
110. Liepert J, Schardt S, Weiller C. Orally administered atropine enhances motor cortex excitability: a transcranial magnetic stimulation study in human subjects. Neurosci Letts. 2001;300:149-52.
111. Magistris MR, Rosler KM, Truffert A, Landis T, Hess CW. A clinical study of motor evoked potentials using a triple stimulation technique. Brain. 1999;122:265-79.
112. Rosler KM, Truffert A, Hess CW, Magistris MR. Quantification of upper motor neuron loss in amyotrophic lateral sclerosis. Clin Neurophysiol. 2000;111:2208-18.
113. Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res. 1997;114:329-38.
114. Hess CW, Mills KR, Murray NM. Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol (London). 1987;388:397-419.
115. de Noordhout AM, Rapisarda G, Bogacz D, et al. Corticomotoneuronal synaptic connections in normal man: an electrophysiological study. Brain. 1999;122:1327-40.
116. Mills KR. Corticomotoneuronal PSTH studies [editorial; comment]. Muscle Nerve. 1999;22:297-8.
117. Awiszus F, Feistner H. Abnormal EPSPs evoked by magnetic brain stimulation in hand muscle motor neurons of patients with amyotrophic lateral sclerosis. Electroencephalogr Clin Neurophysiol. 1993;89:408-14.
118. Eisen A, Entezari-Taher M, Stewart H. Cortical projections to spinal motor neurons: changes with ageing and amyotrophic lateral sclerosis. Neurology. 1996;46:1396-404.
119. Kohara N, Kaji R, Kojima Y, et al. Abnormal excitability of the corticospinal pathway in patients with amyotrophic lateral sclerosis: a single motor unit study using transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1996;101:32-41.
120. Nakajima M, Eisen A, Stewart H. Diverse abnormalities of corticomotoneuronal projections in individual patients with amyotrophic lateral sclerosis. Electroencephalogr Clin Neurophysiol. 1997;105:451-57.
121. Weber M, Eisen A. Assessment of upper and lower motor neurons in Kennedy's disease: implications for corticomotoneuronal PSTH studies [see comments]. Muscle Nerve. 1999;22:299-306.
122. Fetz EE, Gustafsson B. Relation between shapes of postsynaptic potentials and changes in firing probability of cat motor neurons. J Physiol (Lond). 1983;341:387-410.
123. Day BL, Rothwell JC, Thompson PD, et al. Motor cortex stimulation in intact man. 2. Multiple descending volleys. Brain. 1987;110:1191-209.
124. Ellaway PH. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978;45:302-04.
125. Weber M, Eisen A. Peristimulus time histograms (PSTHs):a marker for upper motor neuron involvement in ALS? Amyotroph Lat Scler. 2000;1(Suppl 2):S51-S6.
126. Kohara N, Kaji R, Kojima Y, Kimura J. An electrophysiological study of the corticospinal projections in amyotrophic lateral sclerosis. Clin Neurophysiol. 1999;110:1123-32.
127. Weber M, Eisen A, Stewart HG, Andersen PM. Preserved slow conducting corticomotoneuronal projections in amyotrophic lateral sclerosis with autosomal recessive D90A Cu/Zn-superoxide dismutase mutation [in process citation]. Brain. 2000;123:1505-15.
128. Mills KR. Motor neurone disease. Studies of the corticospinal excitation of single motor neurons by magnetic brain stimulation. Brain. 1995;118:971-82.
129. Nakajima M, Eisen A, McCarthy R, Olney RK, Aminoff MJ. Reduced corticomotoneuronal excitatory postsynaptic potentials (EPSPs) with normal Ia afferent EPSPs in amyotrophic lateral sclerosis. Neurology. 1996;47:1555-61.
130. Nakajima M, Eisen A, Stewart H. Comparison of corticomotoneuronal EPSPs and macro-MUPs in amyotrophic lateral sclerosis. Muscle Nerve. 1998;21:18-24.
131. Chan KM, Doherty TJ, Andres LP, et al. Longitudinal study of the contractile and electrical properties of single human thenar motor units. Muscle Nerve. 1998;21:839-49.
132. Brown WF, Doherty TJ, Chan M, Andres A, Provost SM. Human motor units in health and disease. Muscle Nerve. 2000;9:S7-S18.
133. Chan KM, Doherty TJ, Brown WF. Contractile properties of human motor units in health, ageing and disease. Muscle Nerve. 2001;24:1113-33.
134. Dengler R, Konstanzer A, Küther G, Wolf W, Hesse S, Struppler A. Amyotrophic lateral sclerosis: Macro-EMG and twitch forces of single motor units. Muscle Nerve. 1990;13:545-50.
135. Stalberg E, Fawcett PRW. Macro-EMG in healthy subjects of different ages. J Neurol Neurosurg Psychiatry. 1982;45:870-8.
136. Stein RB, French AS, Mannard A, Yemm R. New methods for analysing muscle function in man and animals. Brain Res. 1972;40:187-92.
137. Heinze HJ, Elger CE, Schubert W, Kunz WS. Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis. Brain. 2000;123:1339-48.
138. Swash M. What does the neurologist expect from clinical neurophysiology? Muscle And Nerve. 2002;25(suppl - Stalberg Festschrift):S13-S8.
139. Brooks BR. Amyotrophic Lateral Sclerosis Scale: guidelines for administration and scoring. In: Herndon RM, editor. Handbook of Neurologic Rating Scales. New York: Demos Vermande, 1997: 27-80.
140. Kalra S, Arnold D. Neuroimaging in amyotrophic lateral sclerosis. Amyotroph Lat Scler. 2003;4:243-8.