Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis

Brain

Volumn 131, Issue 6, 2008, Pages 1540-1550

  Vucic, Steve ^a   Nicholson, Garth A ^b   Kiernan, Matthew C ^a,c  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

Author keywords

Cortical hyperexcitability; Familial ALS; SOD 1

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE COURSE; EVOKED MUSCLE RESPONSE; EXCITABILITY; FAMILIAL DISEASE; FEMALE; FOLLOW UP; HETEROZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; NERVE DEGENERATION; PERIPHERAL NERVE; PRIORITY JOURNAL; SYNAPTIC INHIBITION; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; CASE-CONTROL STUDIES; EVOKED POTENTIALS, MOTOR; FOLLOW-UP STUDIES; HUMANS; MEDIAN NERVE; MIDDLE AGED; MOTOR CORTEX; MOTOR NEURONS; MUTATION; SENSORY THRESHOLDS; SUPEROXIDE DISMUTASE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 44949243975     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn071     Document Type: Article

References (66)

1. Abbruzzese G, Buccolieri A, Marchese R, Trompetto C, Mandich P, Schieppati M. Intracortical inhibition and facilitation are abnormal in Huntington's disease: a paired magnetic stimulation study. Neurosci Lett 1997; 228: 87-90.
2. Aggarwal A, Nicholson G. Age dependent penetrance of three different superoxide dismutase 1 (sod 1) mutations. Int J Neurosci 2005; 115: 1119-30.
3. Alexianu ME, Ho BK, Mohamed AH, La Bella V, Smith RG, Appel SH. The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis. Ann Neurol 1994; 36: 846-58.
4. Andersen P. Amyotrophic lateral sclerosis genetics with Mendelian inheritance. In: Brown R Jr, Swash M, Pasinelli P, editors. Amyotrophic lateral sclerosis. London: Informa Healthcare; 2006a. pp. 187-207.
5. Andersen PM. Amyotrophic lateral sclerosis associated with mutations in the CuZn superoxide dismutase gene. Curr Neurol Neurosci Rep 2006b; 6: 37-46.
6. Baloh RH, Rakowicz W, Gardner R, Pestronk A. Frequent atrophic groups with mixed-type myofibers is distinctive to motor neuron syndromes. Muscle Nerve 2007; 36: 107-10.
7. Ben-Ari Y, Khalilov I, Represa A, Gozlan H. Interneurons set the tune of developing networks. Trends Neurosci 2004; 27: 422-7.
8. Borasio GD, Miller RG. Clinical characteristics and management of ALS. Semin Neurol 2001; 21: 155-66.
9. Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1: 293-9.
10. Browne SE, Yang L, DiMauro JP, Fuller SW, Licata SC, Beal MF. Bioenergetic abnormalities in discrete cerebral motor pathways presage spinal cord pathology in the G93A SOD1 mouse model of ALS. Neurobiol Dis 2006; 22: 599-610.
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. 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.
13. Chen R, Wassermann EM, Caños M, Hallett M. Impaired inhibition in writer's cramp during voluntary muscle activation. Neurology 1997; 49: 1054-9.
14. Choe CU, Ehrlich BE. The inositol 1,4,5-trisphosphate receptor (IP3R) and its regulators: sometimes good and sometimes bad teamwork. Sci STKE 2006; 2006: 15.
15. Cros D, Chiappa KH, Gominak S, Fang J, Santamaria J, King PJ, et al. Cervical magnetic stimulation. Neurology 1990; 40: 1751-6.
16. Cudkowicz M, Qureshi M, Shefner J. Measures and markers in amyotrophic lateral sclerosis. NeuroRx 2004; 1: 273-83.
17. Cudkowicz ME, McKenna-Yasek D, Sapp PE, Chin W, Geller B, Hayden DL, et al. Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann Neurol 1997; 41: 210-21.
18. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 2002; 543: 317-26.
19. Carvalho M, Swash M. Nerve conduction studies in amyotrophic lateral sclerosis. Muscle Nerve 2000; 23: 344-52.
20. Di Lazzaro V, Pilato F, Oliviero A, Dileone M, Saturno E, Mazzone P, et al. Origin of facilitation of motor-evoked potentials after paired magnetic stimulation: direct recording of epidural activity in conscious humans. J Neurophysiol 2006; 96: 1765-71.
21. Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, et al. Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 1998; 119: 265-8.
22. Eisen A, Pant B, Stewart H. Cortical excitability in amyotrophic lateral sclerosis: a clue to pathogenesis. Can J Neurol Sci 1993; 20: 11-6.
23. Eisen A, Weber M. Neurophysiological evaluation of cortical function in the early diagnosis of ALS. Amyotroph Lateral Scler 2000; 1 (Suppl 1): S47-51.
24. Fitzgerald PB, Brown TL, Daskalakis ZJ, Kulkarni J. A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia. Psychiatry Res 2002; 114: 11-22.
25. Gros-Louis F, Gaspar C, Rouleau GA. Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochim Biophys Acta 2006; 1762: 956-72.
26. Gutstein DE, Marks AR. Role of inositol 1,4,5-trisphosphate receptors in regulating apoptotic signaling and heart failure. Heart Vessels 1997; (Suppl 12): 53-7.
27. Hanajima R, Ugawa Y, Terao Y, Sakai K, Furubayashi T, Machii K, et al. Cortico-cortical inhibition of the motor cortical area projecting to sternocleidomastoid muscle in normals and patients with spasmodic torticollis or essential tremor. Electroencephalogr Clin Neurophysiol 1998; 109: 391-6.
28. Hand CK, Rouleau GA. Familial amyotrophic lateral sclerosis. Muscle Nerve 2002; 25: 135-59.
29. Ince P, Stout N, Shaw P, et al. Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol Appl Neurobiol 1993; 19: 291-9.
30. Jones CT, Swingler RJ, Simpson SA, Brock DJ. Superoxide dismutase mutations in an unselected cohort of Scottish amyotrophic lateral sclerosis patients. J Med Genet 1995; 32: 290-2.
31. Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, Kwak S. Glutamate receptors: RNA editing and death of motor neurons. Nature 2004; 427: 801.
32. Kiers L, Cros D, Chiappa KH, Fang J. Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 1993; 89: 415-23.
33. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol 1993; 471: 501-19.
34. Kwak S, Kawahara Y. Deficient RNA editing of GluR2 and neuronal death in amyotrophic lateral sclerosis. J Mol Med 2005; 83: 110-20.
35. Levanon D, Lieman-Hurwitz J, Dafni N, Wigderson M, Sherman L, Bernstein Y, et al. Architecture and anatomy of the chromosomal locus in human chromosome 21 encoding the Cu/Zn superoxide dismutase. Embo J 1985; 4: 77-84.
36. MacKinnon CD, Gilley EA, Weis-McNulty A, Simuni T. Pathways mediating abnormal intracortical inhibition in Parkinson's disease. Ann Neurol 2005; 58: 516-24.
37. Maekawa S, Al-Sarraj S, Kibble M, Landau S, Parnavelas J, Cotter D, et al. Cortical selective vulnerability in motor neuron disease: a morphometric study. Brain 2004; 127: 1237-51.
38. Medical Research Council. Aid to the examination of the peripheral nervous system. Vol. 1. London: Her Majesty's Stationary Office; 1976.
39. Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve 1997; 20: 1137-41.
40. Nihei K, McKee AC, Kowall NW. Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathologica 1993; 86: 55-64.
41. Prout AJ, Eisen A. The cortical silent period and ALS. Muscle Nerve 1994; 17: 217-23.
42. Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 1995a; 37: 181-8.
43. Ridding MC, Sheean G, Rothwell JC, Inzelberg R, Kujirai T. Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry 1995b; 59: 493-8.
44. Robberecht W. Genetics of familial amyotrophic lateral sclerosis and ethical aspects. In: Kuncl R, editor. Motor neuron disease. London: W.B. Saunders; 2002. pp. 75-95.
45. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993; 362: 59-62.
46. Rosenkranz K, Williamon A, Butler K, Cordivari C, Lees AJ, Rothwell JC. Pathophysiological differences between musician's dystonia and writer's cramp. Brain 2005; 128: 918-31.
47. Rowland LP, Shneider NA. Amyotrophic lateral sclerosis. N Engl J Med 2001; 344: 1688-700.
48. Roy J, Minotti S, Dong L, Figlewicz DA, Durham HD. Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J Neurosci 1998; 18: 9673-84.
49. Simpson C, Al-Chalabi A. Modifying genes in amyotrophic lateral sclerosis. In: Brown R, Swash M, Pasinelli P, editors. Amyotrophic lateral sclerosis. London: Informa Helathcare; 2006. pp. 209-24.
50. 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.
51. Stewart HG, Andersen PM, Eisen A, Weber M. Corticomotoneuronal dysfunction in ALS patients with different SOD1 mutations. Clin Neurophysiol 2006; 117: 1850-61.
52. Stys PK. General mechanisms of axonal damage and its prevention. J Neurol Sci 2005; 233: 3-13.
53. Suthers G, Laing N, Wilton S, Dorosz S, Waddy H. "Sporadic" motoneuron disease due to familial SOD1 mutation with low penetrance. Lancet 1994; 344: 1773.
54. 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.
55. Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Distinct cerebral lesions in sporadic and 'D90A' SOD1 ALS: studies with [11C] flumazenil PET. Brain 2005a; 128: 1323-9.
56. Turner MR, Osei-Lah AD, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, et al. Abnormal cortical excitability in sporadic but not homozygous D90A SOD1 ALS. J Neurol Neurosurg Psychiatry 2005b; 76: 1279-85.
57. Van Damme P, Braeken D, Callewaert G, Robberecht W, Van Den Bosch L. GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 2005; 64: 605-12.
58. Van Damme P, Van Den Bosch L, Van Houtte E, Callewaert G, Robberecht W. GluR2-dependent properties of AMPA receptors determine the selective vulnerability of motor neurons to excitotoxicity. J Neurophysiol 2002; 88: 1279-87.
59. Van Den Bosch L, Van Damme P, Bogaert E, Robberecht W. The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 2006; 1762: 1068-82.
60. van Es MA, Van Vught PW, Blauw HM, Franke L, Saris CG, Andersen PM, et al. ITPR2 as a susceptibility gene in sporadic amyotrophic lateral sclerosis: a genome-wide association study. Lancet Neurol 2007; 6: 869-77.
61. Vucic S, Howells J, Trevillion L, Kiernan MC. Assessment of cortical excitability using threshold tracking techniques. Muscle Nerve 2006; 33: 477-86.
62. Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain 2006; 129: 2436-46.
63. Weber M, Eisen A, Stewart HG, Andersen PM. Preserved slow conducting corticomotoneuronal projections in amyotrophic lateral sclerosis with autosomal recessive D90A CuZn-superoxide dismutase mutation. Brain 2000; 123: 1505-15.
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, Paulus W, Rothenberger A. Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 1997a; 154: 1277-84.
66. 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 1997b; 49: 1292-8.