Involvement of spinal sensory pathway in ALS and specificity of cord atrophy to lower motor neuron degeneration

Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration

Volumn 14, Issue 1, 2013, Pages 30-38

  Cohen Adad, Julien ^a,b,h   Mendili, Mohamed Mounir El ^a   Morizot Koutlidis, Régine ^a   Lehéricy, Stéphane ^c,d,e   Meininger, Vincent ^a,d   Blancho, Sophie ^f   Rossignol, Serge ^g   Benali, Habib ^a   Pradat, Pierre François ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Centre de NeuroImagerie de Recherche CENIR   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^f Institut Pour La Recherche Sur La Moelle Epinière Et L Encéphale IRME   (France)

^g UNIVERSITÉ DE MONTRÉAL   (Canada)

^h ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

Author keywords

ALS; Atrophy; Diffusion tensor imaging; Magnetization transfer; Spinal cord

Indexed keywords

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CERVICAL SPINAL CORD; CONTROLLED STUDY; DELTOID MUSCLE; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; FEMALE; FRACTIONAL ANISOTROPY; HAND MUSCLE; HUMAN; LINEAR REGRESSION ANALYSIS; LOWER MOTOR NEURON DEGENERATION; MAJOR CLINICAL STUDY; MALE; MOTOR NEURON DISEASE; MUSCLE WEAKNESS; PRIORITY JOURNAL; PYRAMIDAL TRACT; SENSORY SYSTEM; SPINAL CORD ATROPHY; TRANSCRANIAL MAGNETIC STIMULATION;

AFFERENT PATHWAYS; AMYOTROPHIC LATERAL SCLEROSIS; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; SENSORY RECEPTOR CELLS; SPINAL CORD;

EID: 84875453121     PISSN: 21678421     EISSN: 21679223     Source Type: Journal    
DOI: 10.3109/17482968.2012.701308     Document Type: Article

References (53)

1. Sasaki S, Tsutsumi Y, Yamane K, S akuma H, M aruyama S . Sporadic amyotrophic lateral sclerosis with extensive neurological involvement . Acta Neuropathol. 1992; 84: 211-5.
2. Hammad M, S ilva A, G lass J, S ladky JT, B enatar M . C linical, electrophysiologic, and pathologic evidence for sensory abnormalities in ALS . Neurology. 2007; 69: 2236-42.
3. Grosskreutz J, K aufmann J, F rä d rich J, D engler R, H einze H-J, Peschel T . Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis . BMC Neurology. 2006; 6: 17.
4. Lule D, D iekmann V, M uller HP, K assubek J, L udolph AC, Birbaumer N . Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis . J Neurol Neurosurg Psychiatr. 2010; 81: 899-906.
5. Sage CA, P eeters RR, G ör ner A, R obberecht W, S unaert S . Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis . Neuroimage. 2007; 34: 486-99.
6. Pugdahl K, F uglsang-Frederiksen A, d e Carvalho M, J ohnsen B, Fawcett PRW, Labarre-Vila A, et al . Generalized sensory system abnormalities in amyotrophic lateral sclerosis: a European multicentre study . J Neurol Neurosurg Psychiatr. 2007; 78: 746-9.
7. Ciccarelli O, B ehrens TE, J ohansen-Berg H, T albot K, O rrell RW, Howard RS, et al . Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics . Hum Brain Mapp. 2009; 30: 615-24.
8. Ciccarelli O, B ehrens TE, Altmann DR, O rrell RW, H oward RS, Johansen-Berg H, et al . Probabilistic diffusion tractography: a potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis . Brain. 2006; 129: 1859-71.
9. Ellis CM, S immons A, J ones DK, B land J, D awson JM, Horsfi eld MA, et al . Diffusion tensor MRI assesses corticospinal tract damage in ALS . Neurology. 1999; 53: 1051-8.
10. Iwata NK, Aoki S, Okabe S, Arai N, Terao Y, Kwak S, et al . Evaluation of corticospinal tracts in ALS with diffusion tensor MRI and brainstem stimulation . Neurology. 2008; 70: 528-32.
11. Abe O, Y amada H, M asutani Y, A oki S, K unimatsu A, Yamasue H, et al . Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis . NMR Biomed. 2004; 17: 411-6.
12. Agosta F, P agani E, P etrolini M, C aputo D, P erini M, P relle A, et al . Assessment of white matter tract damage in patients with amyotrophic lateral sclerosis: a diffusion tensor MR imaging tractography study . AJNR Am J Neuroradiol. 2010; 31: 1457-61.
13. Valsasina P, A gosta F, B enedetti B, C aputo D, P erini M, Salvi F, et al . Diffusion anisotropy of the cervical cord is strictly associated with disability in amyotrophic lateral sclerosis . J Neurol Neurosurg Psychiatry. 2007; 78: 480-4.
14. Nair G, C arew JD, U sher S, L u D, H u XP, B enatar M . D iffusion tensor imaging reveals regional differences in the cervical spinal cord in amyotrophic lateral sclerosis . Neuroimage. 2010; 53: 576-83.
15. Pike GB, D e Stefano N, N arayanan S, W orsley KJ, P elletier D, Francis GS, et al . Multiple sclerosis: magnetization transfer MR imaging of white matter before lesion appearance on T2-weighted images . Radiology. 2000; 215: 824-30.
16. Mottershead JP, S chmierer K, C lemence M, T hornton JS, Scaravilli F, Barker GJ, et al . High fi eld MRI correlates of myelin content and axonal density in multiple sclerosis: a post mortem study of the spinal cord . J Neurol. 2003; 250: 1293-301.
17. da Rocha AJ, O liveira AS, F onseca RB, M aia AC Jr, B uainain RP, Lederman HM . Detection of corticospinal tract compromise in amyotrophic lateral sclerosis with brain MR imaging: relevance of the T1-weighted spin-echo magnetization transfer contrast sequence . AJNR Am J Neuroradiol. 2004; 25: 1509-15.
18. Tanabe JL, V ermathen M, M iller R, G elinas D, W einer MW, Rooney WD . Reduced MTR in the corticospinal tract and normal T2 in amyotrophic lateral sclerosis . Magn Reson Imaging. 1998; 16: 1163-9.
19. Wheeler-Kingshott C, C ercignani M . A bout 'a xial ' and ' radial ' diffusivities . Magn Reson Med. 2009; 61: 1255-60.
20. McCreary CR, B jarnason TA, S kihar V, M itchell JR, Y ong VW, Dunn JF . Multiexponential T2 and magnetization transfer MRI of demyelination and remyelination in murine spinal cord . Neuroimage. 2009; 45: 1173-82.
21. Reich DS, S mith SA, Z ackowski KM, G ordon-Lipkin EM, Jones CK, Farrell JA, et al . Multiparametric magnetic resonance imaging analysis of the corticospinal tract in multiple sclerosis . Neuroimage. 2007; 38: 271-9.
22. Cohen-Adad J, E l Mendili M-M, L eh é ricy S, P radat P-F, Blancho S, Rossignol S, et al . Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI . Neuroimage. 2011; 55: 1024-33.
23. Brooks BR, M iller RG, S wash M, M unsat TL . E l Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis . Amyotroph Lateral Scler Other Motor Neuron Disord. 2000; 1: 293-9.
24. Cedarbaum JM, S tambler N, M alta E, F uller C, H ilt 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.
25. Rossini PM, B arker AT, B erardelli A, C aramia MD, C aruso G, Cracco RQ, et al . Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee . Electroencephalogr Clin Neurophysiol. 1994; 91: 79-92.
26. Mills KR, N ithi KA . C orticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis . Muscle Nerve. 1997; 20: 1137-41.
27. Losseff NA, W ebb SL, O 'Riordan JI, P age R, W ang L, B arker GJ, et al . Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression . Brain. 1996; 119: 701-8.
28. Lundell H, B arthelemy D, S kimminge A, D yrby TB, B iering-S ø rensen F, Nielsen JB . Independent spinal cord atrophy measures correlate to motor and sensory defi cits in individuals with spinal cord injury . Spinal Cord. 2011; 49: 70-5.
29. Jenkinson M, B annister P, B rady M, S mith S . I mproved optimization for the robust and accurate linear registration and motion correction of brain images . Neuroimage. 2002; 17: 825-41.
30. Turner MR, K iernan MC, L eigh PN, T albot K . B iomarkers in amyotrophic lateral sclerosis . Lancet Neurol. 2009; 8: 94-109.
31. Filippini N, D ouaud G, M ackay CE, K night S, T albot K, Turner MR . Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis . Neurology. 2010; 75: 1645-52.
32. Williams C, K ozlowski MA, H inton DR, M iller CA . D egeneration of spinocerebellar neurons in amyotrophic lateral sclerosis . Ann Neurol. 1990; 27: 215-25.
33. Guo YS, W u DX, W u HR, W u SY, Y ang C, L i B, et al. S ensory involvement in the SOD1-G93A mouse model of amyotrophic lateral sclerosis . Exp Mol Med. 2009; 41: 140-50.
34. Malaspina A, N goh SF, W ard RE, H all JC, T ai FW, Y ip PK, et al . Activation transcription factor-3 activation and the development of spinal cord degeneration in a rat model of amyotrophic lateral sclerosis . Neuroscience. 2010; 169: 812-27.
35. Ling KK, L in MY, Z ingg B, F eng Z, K o CP . S ynaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy . PLoS One. 2010; 5: e15457.
36. Mentis GZ, B livis D, L iu W, D robac E, C rowder ME, K ong L, et al . Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy . Neuron. 2011; 69: 453-67.
37. Anziska BJ, C racco RQ . S hort-latency somatosensory evoked potentials to median nerve stimulation in patients with diffuse neurologic disease . Neurology. 1983; 33: 989-93.
38. Bosch EP, Y amada T, K imura J . S omatosensory evoked potentials in motor neuron disease . Muscle Nerve. 1985; 8: 556-62.
39. Cosi V, P oloni M, M azzini L, C allieco R . S omatosensory evoked potentials in amyotrophic lateral sclerosis . J Neurol Neurosurg Psychiatry. 1984; 47: 857-61.
40. Radtke RA, E rwin A, E rwin CW . A bnormal sensory evoked potentials in amyotrophic lateral sclerosis . Neurology. 1986; 36: 796-801.
41. Matheson JK, H arrington HJ, H allett M . A bnormalities of multimodality evoked potentials in amyotrophic lateral sclerosis . Arch Neurol. 1986; 43: 338-40.
42. Blain CR, W illiams VC, J ohnston C, S tanton BR, G anesalingam J, Jarosz JM, et al . Alongitudinal study of diffusion tensor MRI in ALS . Amyotroph Lateral Scler. 2007; 8: 348-55.
43. Andersen PM, N ilsson P, K eranen ML, F orsgren L, H agglund J, Karlsborg M, et al . Phenotypic heterogeneity in motor neuron disease patients with Cu/Zn superoxide dismutase mutations in Scandinavia . Brain. 1997; 120: 1723-37.
44. Ince PG, S haw PJ, S lade JY, J ones C, H udgson P . F amilial amyotrophic lateral sclerosis with a mutation in exon 4 of the Cu/Zn superoxide dismutase gene: pathological and immunocytochemical changes . Acta Neuropathol. 1996; 92: 395-403
45. Vucic S, N icholson GA, K iernan MC . C ortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis . Brain. 2008; 131: 1540-50.
46. Verstraete E, v an den Heuvel MP, V eldink JH, B lanken N, Mandl RC, Hulshoff Pol HE, et al . Motor network degeneration in amyotrophic lateral sclerosis: a structural and functional connectivity study . PLoS One. 2010; 5: e13664.
47. Eisen A . A myotrophic lateral sclerosis: evolutionary and other perspectives . Muscle Nerve. 2009; 40: 297-304.
48. Eisen A, K im S, P ant B . A myotrophic lateral sclerosis (ALS): a phylogenetic disease of the corticomotoneuron? Muscle Nerve. 1992; 15: 219-24.
49. Fischer LR, C ulver DG, T ennant P, D avis AA, W ang M, Castellano-Sanchez A, et al . Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man . Exp Neurol. 2004; 185: 232-40.
50. Chou SM, N orris FH . A myotrophic lateral sclerosis: lower motor neuron disease spreading to upper motor neurons . Muscle Nerve. 1993; 16: 864-9.
51. Ellis CM, S uckling J, A maro E, B ullmore ET, S immons A, Williams SC, et al . Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS . Neurology. 2001; 57: 1571-8.
52. Iwata NK, K wan JY, D anielian LE, B utman JA, T ovar-Moll F, Bayat E, et al . White matter alterations differ in primary lateral sclerosis and amyotrophic lateral sclerosis . Brain. 2011; 134: 2642-55.
53. Ravits JM, L a Spada AR . ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration . Neurology. 2009; 73: 805-11.