Upper motor neuron involvement in amyotrophic lateral sclerosis evaluated by triple stimulation technique and diffusion tensor MRI

Journal of Neurology

Volumn 260, Issue 6, 2013, Pages 1535-1544

  Furtula, Jasna ^a   Johnsen, Birger ^a   Frandsen, Jesper ^a   Rodell, Anders ^a   Christensen, Peter Broegger ^a   Pugdahl, Kirsten ^a   Fuglsang Frederiksen, Anders ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Amyotrophic lateral sclerosis; Diffusion tensor imaging; Motor evoked potentials; Triple stimulation technique; Upper motor neuron

Indexed keywords

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CAPSULA INTERNA; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; INTERMETHOD COMPARISON; MALE; MOTOR NERVE CONDUCTION; NERVE CELL DEGENERATION; NERVE STIMULATION; NEUROIMAGING; PRIORITY JOURNAL; PYRAMIDAL TRACT; QUANTITATIVE DIAGNOSIS; SENSITIVITY ANALYSIS; TRIPLE STIMULATION TECHNIQUE; UPPER MOTOR NEURON DEGENERATION;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANISOTROPY; DIFFUSION TENSOR IMAGING; ELECTRODIAGNOSIS; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MALE; MIDDLE AGED; MOTOR NEURONS; NERVE DEGENERATION; SENSITIVITY AND SPECIFICITY;

EID: 84878832686     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-012-6824-8     Document Type: Article

References (56)

1. Schriefer TN, Hess CW, Mills KR, Murray NM (1989) Central motor conduction studies in motor neurone disease using magnetic brain stimulation. Electroencephalogr Clin Neurophysiol 74:431-437 (Pubitemid 20000338)
2. Eisen A, Shytbel W, Murphy K, Hoirch M (1990) Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve 13:146-151 (Pubitemid 20049330)
3. de Carvalho M, Turkman A, Swash M (2003) 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 210:83-90 (Pubitemid 36539410)
4. Attarian S, Azulay JP, Lardillier D, Verschueren A, Pouget J (2005) Transcranial magnetic stimulation in lower motor neuron diseases. Clin Neurophysiol 116:35-42 (Pubitemid 40267638)
5. Attarian S, Verschueren A, Pouget J (2007) Magnetic stimulation including the triple-stimulation technique in amyotrophic lateral sclerosis. Muscle Nerve 36:55-61 (Pubitemid 47016161)
6. Mills KR (2003) The natural history of central motor abnormalities in amyotrophic lateral sclerosis. Brain 126:2558-2566 (Pubitemid 37314443)
7. Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Motor Neuron Disord 1:293-299
8. Komissarow L, Rollnik JD, Bogdanova D, Krampfl K, Khabirov FA, Kossev A, Dengler R, Bufler J (2004) Triple stimulation technique (TST) in amyotrophic lateral sclerosis. Clin Neurophysiol 115:356-360 (Pubitemid 38117256)
9. Magistris MR, Rosler KM, Truffert A, Myers JP (1998) Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 121:437-450 (Pubitemid 28116341)
10. Magistris MR, Rosler KM, Truffert A, Landis T, Hess CW (1999) A clinical study of motor evoked potentials using a triple stimulation technique. Brain 122:265-279 (Pubitemid 29067209)
11. Rosler KM, Truffert A, Hess CW, Magistris MR (2000) Quantification of upper motor neuron loss in amyotrophic lateral sclerosis. Clin Neurophysiol 111:2208-2218
12. Kleine BU, Schelhaas HJ, van Elswijk G, de Rijk MC, Stegeman DF, Zwarts MJ (2010) Prospective, blind study of the triple stimulation technique in the diagnosis of ALS. Amyotroph Lateral Scler 11:67-75
13. Agosta F, Pagani E, Petrolini M, Caputo D, Perini M, Prelle A, Salvi F, Filippi M (2010) Assessment of white matter tract damage in patients with amyotrophic lateral sclerosis: a diffusion tensor MR imaging tractography study. AJNR Am J Neuroradiol 31:1457-1461
14. Cosottini M, Giannelli M, Vannozzi F, Pesaresi I, Piazza S, Belmonte G, Siciliano G (2010) Evaluation of corticospinal tract impairment in the brain of patients with amyotrophic lateral sclerosis by using diffusion tensor imaging acquisition schemes with different numbers of diffusion-weighting directions. J Comput Assist Tomogr 34:746-750
15. Ellis CM, Simmons A, Jones DK, Bland J, Dawson JM, Horsfield MA, Williams SC, Leigh PN (1999) Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology 53:1051-1058 (Pubitemid 29442122)
16. Iwata NK, Aoki S, Okabe S, Arai N, Terao Y, Kwak S, Abe O, Kanazawa I, Tsuji S, Ugawa Y (2008) Evaluation of corticospinal tracts in ALS with diffusion tensor MRI and brainstem stimulation. Neurology 70:528-532 (Pubitemid 351653377)
17. Sage CA, Peeters RR, Gorner A, Robberecht W, Sunaert S (2007) Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage 34:486-499 (Pubitemid 44830171)
18. Senda J, Ito M, Watanabe H, Atsuta N, Kawai Y, Katsuno M, Tanaka F, Naganawa S, Fukatsu H, Sobue G (2009) Correlation between pyramidal tract degeneration and widespread white matter involvement in amyotrophic lateral sclerosis: a study with tractography and diffusion-tensor imaging. Amyotroph Lateral Scler 10:288-294
19. Iwata NK, Aoki S, Masutani Y, Yoshida J, Okabe S, Arai N, Terao Y, Kwak S, Tsuji S, Ugawa Y (2005) Corticospinal tract and corticobulbar tract dysfunction in ALS: combined study using transcranial magnetic stimulation and diffusion tensor tractography. Int Congr Ser 1278:181-184 (Pubitemid 43693387)
20. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, Buchel C, Weiller C (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127:340-350 (Pubitemid 38160319)
21. Brooks BR (1994) El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial "Clinical limits of amyotrophic lateral sclerosis" workshop contributors. J Neurol Sci 124(96-107):96-107
22. Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, Moher D, Rennie D, de Vet HC, Lijmer JG (2003) The STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. Clin Chem 49:7-18 (Pubitemid 36078547)
23. Mioshi E, Lillo P, Kiernan M, Hodges J (2012) Activities of daily living in motor neuron disease: role of behavioural and motor changes. J Clin Neurosci 19:552-556
24. Roth G, Magistris MR (1987) Detection of conduction block by monopolar percutaneous stimulation of the brachial plexus. Electromyogr Clin Neurophysiol 27:45-53 (Pubitemid 18009348)
25. Moller M, Frandsen J, Andersen G, Gjedde A, Vestergaard-Poulsen P, Ostergaard L (2007) Dynamic changes in corticospinal tracts after stroke detected by fibretracking. J Neurol Neurosurg Psychiatry 78:587-592 (Pubitemid 46853892)
26. Dalby RB, Frandsen J, Chakravarty MM, Ahdidan J, Sorensen L, Rosenberg R, Videbech P, Ostergaard L (2010) Depression severity is correlated to the integrity of white matter fiber tracts in late-onset major depression. Psychiatry Res 184:38-48
27. Grabner G, Janke AL, Budge MM, Smith D, Pruessner J, Collins DL (2006) Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med Image Comput Comput Assist Interv 9:58-66 (Pubitemid 44609204)
28. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le GG, Boomsma D, Cannon T, Kawashima R, Mazoyer B (2001) A probabilistic atlas and reference system for the human brain: international consortium for brain mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293-1322 (Pubitemid 32876067)
29. Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192-205 (Pubitemid 24100002)
30. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265-269 (Pubitemid 29072377)
31. Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies - a technical review. NMR Biomed 15:468-480 (Pubitemid 36054510)
32. Galantucci S, Tartaglia MC, Wilson SM, Henry ML, Filippi M, Agosta F, Dronkers NF, Henry RG, Ogar JM, Miller BL, Gorno-Tempini ML (2011) White matter damage in primary progressive aphasias: a diffusion tensor tractography study. Brain 134:3011-3029
33. Wong JC, Concha L, Beaulieu C, Johnston W, Allen PS, Kalra S (2007) Spatial profiling of the corticospinal tract in amyotrophic lateral sclerosis using diffusion tensor imaging. J Neuroimaging 17:234-240 (Pubitemid 47019896)
34. Cook C, Roman M, Stewart KM, Leithe LG, Isaacs R (2009) Reliability and diagnostic accuracy of clinical special tests for myelopathy in patients seen for cervical dysfunction. J Orthop Sports Phys Ther 39:172-178
35. Miller TM, Johnston SC (2005) Should the Babinski sign be part of the routine neurologic examination? Neurology 65:1165-1168 (Pubitemid 41508204)
36. Mills KR, Nithi KA (1998) Peripheral and central motor conduction in amyotrophic lateral sclerosis. J Neurol Sci 159:82-87 (Pubitemid 28365888)
37. Buhler R, Magistris MR, Truffert A, Hess CW, Rosler KM (2001) The triple stimulation technique to study central motor conduction to the lower limbs. Clin Neurophysiol 112:938-949 (Pubitemid 32406271)
38. Pyra T, Hui B, Hanstock C, Concha L, Wong JC, Beaulieu C, Johnston W, Kalra S (2010) Combined structural and neurochemical evaluation of the corticospinal tract in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 11:157-165
39. Foerster BR, Dwamena BA, Petrou M, Carlos RC, Callaghan BC, Pomper MG (2012) Diagnostic accuracy using diffusion tensor imaging in the diagnosis of ALS: a meta-analysis. Acad Radiol 19:1075-1086
40. Kloppel S, Baumer T, Kroeger J, Koch MA, Buchel C, Munchau A, Siebner HR (2008) The cortical motor threshold reflects microstructural properties of cerebral white matter. Neuroimage 40:1782-1791
41. Hubers A, Klein JC, Kang JS, Hilker R, Ziemann U (2011) The relationship between TMS measures of functional properties and DTI measures of microstructure of the corticospinal tract. Brain Stimul 5:297-304
42. Ziemann U, Rothwell JC (2000) I-waves in motor cortex. J Clin Neurophysiol 17:397-405
43. Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W (1998) Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 511(Pt 1):181-190 (Pubitemid 28421322)
44. Patton HD, Amassian VE (1954) Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J Neurophysiol 17:345-363
45. Hugon J, Lubeau M, Tabaraud F, Chazot F, Vallat JM, Dumas M (1987) Central motor conduction in motor neuron disease. Ann Neurol 22:544-546 (Pubitemid 17164781)
46. Ingram DA, Swash M (1987) Central motor conduction is abnormal in motor neuron disease. J Neurol Neurosurg Psychiatry 50:159-166 (Pubitemid 17016556)
47. Schulte-Mattler WJ, Muller T, Zierz S (1999) Transcranial magnetic stimulation compared with upper motor neuron signs in patients with amyotrophic lateral sclerosis. J Neurol Sci 170:51-56 (Pubitemid 29502535)
48. Kang X, Herron TJ, Woods DL (2011) Regional variation, hemispheric asymmetries and gender differences in pericortical white matter. Neuroimage 56:2011-2023
49. Hammond G (2002) Correlates of human handedness in primary motor cortex: a review and hypothesis. Neurosci Biobehav Rev 26:285-292 (Pubitemid 34553315)
50. Buchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14:945-951 (Pubitemid 39121356)
51. Peled S, Gudbjartsson H, Westin CF, Kikinis R, Jolesz FA (1998) Magnetic resonance imaging shows orientation and asymmetry of white matter fiber tracts. Brain Res 780:27-33 (Pubitemid 28068076)
52. Westerhausen R, Huster RJ, Kreuder F, Wittling W, Schweiger E (2007) Corticospinal tract asymmetries at the level of the internal capsule: is there an association with handedness? Neuroimage 37:379-386 (Pubitemid 47444273)
53. Wang S, Poptani H, Bilello M, Wu X, Woo JH, Elman LB, McCluskey LF, Krejza J, Melhem ER (2006) Diffusion tensor imaging in amyotrophic lateral sclerosis: volumetric analysis of the corticospinal tract. AJNR Am J Neuroradiol 27:1234-1238 (Pubitemid 44897632)
54. Furutani K, Harada M, Minato M, Morita N, Nishitani H (2005) Regional changes of fractional anisotropy with normal aging using statistical parametric mapping (SPM). J Med Invest 52:186-190 (Pubitemid 41602594)
55. Nusbaum AO, Tang CY, Buchsbaum MS, Wei TC, Atlas SW (2001) Regional and global changes in cerebral diffusion with normal aging. AJNR Am J Neuroradiol 22:136-142 (Pubitemid 32105366)
56. Pfefferbaum A, Adalsteinsson E, Sullivan EV (2005) Frontal circuitry degradation marks healthy adult aging: evidence from diffusion tensor imaging. Neuroimage 26:891-899 (Pubitemid 40825031)