Motor network degeneration in amyotrophic lateral sclerosis: A structural and functional connectivity study

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Verstraete, Esther ^a   van den Heuvel, Martijn P ^a   Veldink, Jan H ^a   Blanken, Niels ^b   Mandl, René C ^a   Pol, Hilleke E Hulshoff ^a   van den Berg, Leonard H ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN CORTEX ATROPHY; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DISEASE EXACERBATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MOTOR CORTEX; MOTOR SYSTEM; NERVE CELL NETWORK; NERVE DEGENERATION; PYRAMIDAL TRACT; AGED; BRAIN; CASE CONTROL STUDY; DISEASE COURSE; MIDDLE AGED; MOTONEURON; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; CASE-CONTROL STUDIES; DISEASE PROGRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR NEURONS;

EID: 78149434140     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013664     Document Type: Article

References (68)

1. Kunst CB (2004) Complex genetics of amyotrophic lateral sclerosis. Am J Hum Genet 75: 933-947.
2. Rothstein JD (2009) Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 65(Suppl 1): S3-9.
3. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319: 1668-1672.
4. Ellis CM, Suckling J, Amaro E, Jr., Bullmore ET, Simmons A, et al. (2001) Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology 57: 1571-1578.
5. Chang JL, Lomen-Hoerth C, Murphy J, Henry RG, Kramer JH, et al. (2005) A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/ FTLD. Neurology 65: 75-80.
6. Turner MR, Hammers A, Allsop J, Al-Chalabi A, Shaw CE, et al. (2007) Volumetric cortical loss in sporadic and familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler 8: 343-347.
7. Thivard L, Pradat PF, Lehericy S, Lacomblez L, Dormont D, et al. (2007) Diffusion tensor imaging and voxel based morphometry study in amyotrophic lateral sclerosis: relationships with motor disability. J Neurol Neurosurg Psychiatry 78: 889-892.
8. Sage CA, Peeters RR, Gorner A, Robberecht W, Sunaert S (2007) Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. NeuroImage 34: 486-499.
9. Ciccarelli O, Behrens TE, Johansen-Berg H, Talbot K, Orrell RW, et al. (2009) Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp 30: 615-624.
10. Senda J, Ito M, Watanabe H, Atsuta N, Kawai Y, et al. (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.
11. Graham JM, Papadakis N, Evans J, Widjaja E, Romanowski CA, et al. (2004) Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 63: 2111-2119.
12. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, et al. (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127: 340-350.
13. Tessitore A, Esposito F, Monsurro MR, Graziano S, Panza D, et al. (2006) Subcortical motor plasticity in patients with sporadic ALS: An fMRI study. Brain Res Bull 69: 489-494.
14. Schoenfeld MA, Tempelmann C, Gaul C, Kuhnel GR, Duzel E, et al. (2005) Functional motor compensation in amyotrophic lateral sclerosis. J Neurol 252: 944-952.
15. Stanton BR, Williams VC, Leigh PN, Williams SC, Blain CR, et al. (2007) Altered cortical activation during a motor task in ALS. Evidence for involvement of central pathways. J Neurol 254: 1260-1267.
16. Mohammadi B, Kollewe K, Samii A, Krampfl K, Dengler R, et al. (2009) Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol 217: 147-153.
17. Kim JH, Loy DN, Liang HF, Trinkaus K, Schmidt RE, et al. (2007) Noninvasive diffusion tensor imaging of evolving white matter pathology in a mouse model of acute spinal cord injury. Magn Reson Med 58: 253-260.
18. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34: 537-541.
19. Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, et al. (2007) Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci 27: 12132-12138.
20. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, et al. (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106: 2035-2040.
21. van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE (2009) Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30: 3127-3141.
22. Van den Heuvel MP, Mandl RC, Luigjes J, Hulshoff Pol HE (2008) Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28: 10844-10851.
23. Agosta F, Chio A, Cosottini M, De Stefano N, Falini A, et al. (2010) The Present and the Future of Neuroimaging in Amyotrophic Lateral Sclerosis. AJNR Am J Neuroradiol Epub 2010 Apr 1.
24. Rivara CB, Sherwood CC, Bouras C, Hof PR (2003) Stereologic characterization and spatial distribution patterns of Betz cells in the human primary motor cortex. Anat Rec A Discov Mol Cell Evol Biol 270: 137-151.
25. Kiernan JA, Hudson AJ (1991) Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain (114(Pt 2): 843-853.
26. Agosta F, Pagani E, Rocca MA, Caputo D, Perini M, et al. (2007) Voxel-based morphometry study of brain volumetry and diffusivity in amyotrophic lateral sclerosis patients with mild disability. Hum Brain Mapp 28: 1430-1438.
27. Grossman M, Anderson C, Khan A, Avants B, Elman L, et al. (2008) Impaired action knowledge in amyotrophic lateral sclerosis. Neurology 71: 1396-1401.
28. Hutton C, Draganski B, Ashburner J, Weiskopf N (2009) A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. NeuroImage 48: 371-380.
29. Bakkour A, Morris JC, Dickerson BC (2009) The cortical signature of prodromal AD: regional thinning predicts mild AD dementia. Neurology 72: 1048-1055.
30. Rohrer JD, Warren JD, Modat M, Ridgway GR, Douiri A, et al. (2009) Patterns of cortical thinning in the language variants of frontotemporal lobar degeneration. Neurology 72: 1562-1569.
31. Rosas HD, Salat DH, Lee SY, Zaleta AK, Pappu V, et al. (2008) Cerebral cortex and the clinical expression of Huntington's disease: complexity and heterogeneity. Brain 131: 1057-1068.
32. Vucic S, Nicholson GA, Kiernan MC (2008) Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 131: 1540-1550.
33. Eisen A (2009) Amyotrophic lateral sclerosis-Evolutionary and other perspectives. Muscle Nerve 40: 297-304.
34. Wittstock M, Wolters A, Benecke R (2007) Transcallosal inhibition in amyotrophic lateral sclerosis. Clin Neurophysiol 118: 301-307.
35. Bartels C, Mertens N, Hofer S, Merboldt KD, Dietrich J, et al. (2008) Callosal dysfunction in amyotrophic lateral sclerosis correlates with diffusion tensor imaging of the central motor system. Neuromuscul Disord 18: 398-407.
36. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain.l. Nat Cell Bio 11: 909-913.
37. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62: 42-52.
38. Kahkonen S, Ilmoniemi RJ (2004) Transcranial magnetic stimulation: applications for neuropsychopharmacology. J Psychopharmacol 18: 257-261.
39. Vucic S, Cheah BC, Kiernan MC (2009) Defining the mechanisms that underlie cortical hyperexcitability in amyotrophic lateral sclerosis. Exp Neurol 220: 177-182.
40. Lowe MJ, Beall EB, Sakaie KE, Koenig KA, Stone L, et al. (2008) Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum Brain Mapp 29: 818-827.
41. Morgan VL, Mishra A, Newton AT, Gore JC, Ding Z (2009) Integrating functional and diffusion magnetic resonance imaging for analysis of structure-function relationship in the human language network. PLoS One 4: e6660.
42. Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, et al. (2010) Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 133: 1352-1367.
43. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 1: 293-299.
44. Jones DK (2004) The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med 51: 807-815.
45. Jones DK, Horsfield MA, Simmons A (1999) Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 42: 515-25.
46. van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009) Efficiency of functional brain networks and intellectual performance. J Neurosci 29: 7619-7624.
47. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, et al. (2001) Frequencies contributing to functional connectivity in the cerebral cortex in ''resting-state'' data. AJNR Am J Neuroradiol 22: 1326-33.
48. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97: 11050-11055.
49. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, et al. (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31: 968-980.
50. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, et al. (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14: 11-22.
51. Rogers J, Kochunov P, Lancaster J, Shelledy W, Glahn D, et al. (2007) Heritability of brain volume, surface area and shape: an MRI study in an extended pedigree of baboons. Hum Brain Mapp 28: 576-583.
52. van der Schot AC, Vonk R, Brans RG, van Haren NE, Koolschijn PC, et al. (2009) Influence of genes and environment on brain volumes in twin pairs concordant and discordant for bipolar disorder. Arch Gen Psychiatry 66: 142-151.
53. Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, et al. (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47: 215-223.
54. Mandl RC, Schnack HG, Luigjes J, van den Heuvel MP, Cahn W, et al. (2008) Tract-based Analysis of Magnetization Transfer Ratio and Diffusion Tensor Imaging of the Frontal and Frontotemporal Connections in Schizophrenia. Schizophr Bull 36: 778-787.
55. Budde MD, Kim JH, Liang HF, Russell JH, Cross AH, et al. (2008) Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed 21: 589-597.
56. Lowe MJ, Dzemidzic M, Lurito JT, Mathews VP, Phillips MD (2000) Correlations in low-frequency BOLD fluctuations reflect cortico-cortical connections. NeuroImage 12: 582-587.
57. Aertsen AM, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: modulation of ''effective connectivity''. Journal of Neuro-physiology 61: 900-917.
58. Friston KJ, Frith CD, Liddle PF, Frackowiak RS (1993) Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 13: 5-14.
59. Cordes D, Haughton VM, Arfanakis K, Wendt GJ, Turski PA, et al. (2000) Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol 21: 1636-1344.
60. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360: 1001-1013.
61. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26: 63-72.
62. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, et al. (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848-13853.
63. van den Heuvel MP, Stam CJ, Boersma M, Hulshoff Pol HE (2008) Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. NeuroImage 43: 528-539.
64. Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, et al. (2008) Reduced resting-state brain activity in the ''default network'' in normal aging. Cereb Cortex 18: 1856-1864.
65. Salvador R, Martinez A, Pomarol-Clotet E, Sarro S, Suckling J, et al. (2007) Frequency based mutual information measures between clusters of brain regions in functional magnetic resonance imaging. NeuroImage 35: 83-88.
66. Stam CJ, Reijneveld JC (2007) Graph theoretical analysis of complex networks in the brain. Nonlinear Biomedical Physics 1: 3.
67. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews 10: 186-198.
68. Reijneveld JC, Ponten SC, Berendse HW, Stam CJ (2007) The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 118: 2317-2331.