Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease

Brain

Volumn 129, Issue 9, 2006, Pages 2436-2446

  Vucic, Steve ^b   Kiernan, Matthew C ^a  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b NONE

Author keywords

Cortical hyperexcitability; MND; Threshold tracking

Indexed keywords

ADULT; AGED; AMPLITUDE MODULATION; ARTICLE; AXOPLASM FLOW; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SEVERITY; EARLY DIAGNOSIS; EVOKED MUSCLE RESPONSE; FEMALE; HUMAN; INHIBITION KINETICS; LIMB DISEASE; MALE; MOTOR NEURON DISEASE; MUSCLE ACTION POTENTIAL; NERVE EXCITABILITY; NEUROPHYSIOLOGY; PERIPHERAL NERVE; PRIORITY JOURNAL; SHORT INTERVAL INTRACORTICAL INHIBITION; STIMULUS RESPONSE; TECHNIQUE; THRESHOLD TRACKING; TRANSCRANIAL MAGNETIC STIMULATION; ACTION POTENTIAL; CELL DEATH; COMPARATIVE STUDY; ELECTROSTIMULATION; MEDIAN NERVE; METHODOLOGY; MIDDLE AGED; MOTONEURON; MOTOR CORTEX; MUSCLE CONTRACTION; NERVE CELL INHIBITION; NERVE FIBER; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

ACTION POTENTIALS; ADULT; AGED; AXONS; CELL DEATH; ELECTRIC STIMULATION; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MEDIAN NERVE; MIDDLE AGED; MOTOR CORTEX; MOTOR NEURON DISEASE; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NEURAL INHIBITION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 33749239968     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl172     Document Type: Article

References (72)

1. Abbruzzese G, Assini A, Buccolieri A, Schieppati M, Trompetto C. Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans. J Physiol (Lond) 1999; 514: 895-903.
2. Avoli M, Hwa G, Louvel J, Kurcewicz I, Pumain R, Lacaille JC. Functional and pharmacological properties of GABA-mediated inhibition in the human neocortex. Can J Physiol Pharmacol 1997; 75: 526-34.
3. Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med 1994; 330: 585-91.
4. Bostock H. The strength-duration relationship for excitation of myelinated nerve: computed dependence on membrane parameters. J Physiol (Lond) 1983; 341: 59-74.
5. Bostock H, Rothwell JC. Latent addition in motor and sensory fibres of human peripheral nerve. J Physiol (Lond) 1997; 498: 277-94.
6. Bostock H, Sharief MK, Reid G, Murray NM. Axonal ion channel dysfunction in amyotrophic lateral sclerosis. Brain 1995; 118: 217-25.
7. Bostock H, Cikurel K, Burke D. Threshold tracking techniques in the study of human peripheral nerve. Muscle Nerve 1998; 21: 137-58.
8. Brooks BR, Miller RG, Swash M, Munsat TL. World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1: 293-9.
9. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997; 18: 327-38.
10. Burke D, Kiernan MC, Bostock H. Excitability of human axons. Clin Neurophysiol 2001; 112: 1575-85.
11. Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 1992; 42: 1951-9.
12. Caramia MD, Cicinelli P, Paradiso C, Mariorenzi R, Zarola F, Bernardi G, et al. Excitability changes of muscular responses to magnetic brain stimulation in patients with central motor disorders. Electroencephalogr Clin Neurophysiol 1991; 81: 243-50.
13. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 1999; 169: 13-21.
14. Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res 1999; 128: 539-42.
15. Claus D. Central motor conduction: method and normal results. Muscle Nerve 1990; 13: 1125-32.
16. Connors BW, Malenka RC, Silva LR. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol (Lond) 1988; 406: 443-68.
17. Cros D, Chiappa KH, Gominak S, Fang J, Santamaria J, King PJ, et al. Cervical magnetic stimulation. Neurology 1990; 40: 1751-6.
18. De Carvalho M, Swash M. Nerve conduction studies in amyotrophic lateral sclerosis. Muscle Nerve 2000; 23: 344-52.
19. 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.
20. Desai J, Swash M. Essentials of diagnosis. In: Kuncl WR, editor. Motor neuron disease. London: W.B. Saunders; 2002. p. 1-21.
21. 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.
22. Drory VE, Kovach I, Groozman GB. Electrophysiologic evaluation of upper motor neuron involvement in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2001; 2: 147-52.
23. Eisen A, Kim S, Pant B. Amyotrophic lateral sclerosis (ALS): a phylogenetic disease of the corticomotoneuron? Muscle Nerve 1992; 15: 219-24.
24. Eisen A, Pant B, Stewart H. Cortical excitability in amyotrophic lateral sclerosis: a clue to pathogenesis. Can J Neurol Sci 1993; 20: 11-16.
25. Eisen A, Weber M. The motor cortex and amyotrophic lateral sclerosis. Muscle Nerve 2001; 24: 564-73.
26. Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 2002; 143: 240-8.
27. Hanajima R, Ugawa Y, Terao Y, Ogata K, Kanazawa I. Ipsilateral corticocortical inhibition of the motor cortex in various neurological disorders. J Neurol Sci 1996; 140: 109-16.
28. Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol (Lond) 1993; 466: 521-34.
29. Kanai K, Kuwabara S, Arai K, Sung JY, Ogawara K, Hattori T. Muscle cramp in Machado-Joseph disease: altered motor axonal excitability properties and mexiletine treatment. Brain 2003; 126: 965-73.
30. Kiernan JA, Hudson AJ. Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain 1991; 114: 843-53.
31. Kiernan MC. Riluzole: a glimmer of hope in the treatment of motor neurone disease. Med J Aust 2005; 182: 319-20.
32. Kiernan MC, Burke D, Andersen KV, Bostock H. Multiple measures of axonal excitability: a new approach in clinical testing. Muscle Nerve 2000; 23: 399-409.
33. Kiernan MC, Cikurel K, Bostock H. Effects of temperature on the excitability properties of human motor axons. Brain 2001a; 124: 816-25.
34. Kiernan MC, Lin CS, Andersen KV, Murray NM, Bostock H. Clinical evaluation of excitability measures in sensory nerve. Muscle Nerve 2001b; 24: 883-92.
35. Kohara N, Kaji R, Kojima Y, Mills KR, Fujii H, Hamano T, 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.
36. Komissarow L, Rollnik JD, Bogdanova D, Krampfl K, Khabirov FA, Kossev A, et al. Triple stimulation technique (TST) in amyotrophic lateral sclerosis. Clin Neurophysiol 2004; 115: 356-60.
37. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol (Lond) 1993; 471: 501-19.
38. Kuo JJ, Siddique T, Fu R, Heckman CJ. Increased persistent Na(+) current and its effect on excitability in motoneurones cultured from mutant SOD1 mice. J Physiol (Lond) 2005; 563: 843-54.
39. Lacomblez L, Bensimon G, Leigh PN, Guillet P, Meininger V. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet 1996; 347: 1425-31.
40. Leigh PN, Swash M. Cytoskeletal pathology in motor neuron diseases. In: Rowland LP, editor. Amyotrophic lateral sclerosis and other motor neuron diseases. Advances in Neurology. New York: Raven Press; 1991: p. 115-24.
41. Liepert J, Schwenkreis P, Tegenthoff M, Malin JP. The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 1997; 104: 1207-14.
42. Magistris MR, Rosler KM, Truffert A, Myers JP. Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 1998; 121: 437-50.
43. Medical Research Council. Aids to the examination of the peripheral nervous system. London: Her Majesty's Stationery Office; 1976. p. 1-2.
44. Miller RG, Mitchell JD, Lyon M, Moore DH. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Amyotroph Lateral Scler Other Motor Neuron Disord 2003; 4: 191-206.
45. Mills KR. The natural history of central motor abnormalities in amyotrophic lateral sclerosis. Brain 2003; 126: 2558-66.
46. Mills KR, Murray NM. Electrical stimulation over the human vertebral column: which neural elements are excited? Electroencephalogr Clin Neurophysiol 1986; 63: 582-9.
47. Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve 1997; 20: 1137-41.
48. Mogyoros I, Kiernan MC, Burke D. Strength-duration properties of human peripheral nerve. Brain 1996; 119: 439-47.
49. Mogyoros I, Kiernan MC, Burke D, Bostock H. Strength-duration properties of sensory and motor axons in amyotrophic lateral sclerosis. Brain 1998; 121: 851-9.
50. Nihei K, McKee AC, Kowall NW. Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathol (Berl) 1993; 86: 55-64.
51. Pamphlett R, Kril J, Hng TM. Motor neuron disease: a primary disorder of corticomotoneurons? Muscle Nerve 1995; 18: 314-8.
52. Prout AJ, Eisen A. The cortical silent period and amyotrophic lateral sclerosis. Muscle Nerve 1994; 17: 217-23.
53. Raynor EM, Shefner JM. Recurrent inhibition is decreased in patients with amyotrophic lateral sclerosis. Neurology 1994; 44: 2148-53.
54. Roshan L, Paradiso GO, Chen R. Two phases of short-interval intracortical inhibition. Exp Brain Res 2003; 151: 330-7.
55. Rosler KM, Truffert A, Hess CW, Magistris MR. Quantification of upper motor neuron loss in amyotrophic lateral sclerosis. Clin Neurophysiol 2000; 111: 2208-18.
56. Rothstein JD, Jin L, Dykes-Hoberg M, Kuncl RW. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc Natl Acad Sci USA 1993; 90: 6591-5.
57. Sommer M, Tergau F, Wischer S, Reimers CD, Beuche W, Paulus W. Riluzole does not have an acute effect on motor thresholds and the intracortical excitability in amyotrophic lateral sclerosis. J Neurol 1999; 246 (Suppl 3): S22-6.
58. Stefan K, Kunesch E, Benecke R, Classen J. Effects of riluzole on cortical excitability in patients with amyotrophic lateral sclerosis. Ann Neurol 2001; 49: 537-40.
59. Triggs WJ, Menkes D, Onorato J, Yan RS, Young MS, Newell K, et al. Transcranial magnetic stimulation identifies upper motor neuron involvement in motor neuron disease. Neurology 1999; 53: 605-11.
60. Trotti D, Rolfs A, Danbolt NC, Brown RH Jr, Hediger MA. SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat Neurosci 1999; 2: 427-33.
61. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 2004; 15: 601-9.
62. Vucic S, Howells J, Trevillion L, Kiernan MC. Assessment of cortical excitability using threshold tracking techniques. Muscle Nerve 2006; 33: 477-86.
63. Weber M, Eisen A. Peristimulus time histograms (PSTHs)-a marker for upper motor neuron involvement in ALS? Amyotroph Lateral Scler Other Motor Neuron Disord 2000; Suppl 2: S51-6.
64. Weber M, Eisen A, Nakajima M. Corticomotoneuronal activity in ALS: changes in the peristimulus time histogram over time. Clin Neurophysiol 2000; 111: 169-77.
65. Weiss G. Sur la possibilité de rendre comparables entre eux les appareils servant l'excitation électrique. Arch Ital Biol 1901; 35: 413-46.
66. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol (Lond) 1999; 517: 591-7.
67. Yokota T, Yoshino A, Inaba A, Saito Y. Double cortical stimulation in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 1996; 61: 596-600.
68. 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.
69. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 1996; 109: 127-35.
70. 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.
71. Ziemann U. TMS and drugs. Clin Neurophysiol 2004a; 115: 1717-29.
72. Ziemann U. Cortical threshold and excitability measurements. In: Eisen A, editor. In: Clinical neurophysiology of motor neuron diseases. Handbook of clinical neurophysiology. Amsterdam: Elsevier; 2004b. p. 317-35.