Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients

NeuroImage

Volumn 39, Issue 3, 2008, Pages 1370-1382

  Schaechter, Judith D ^a   Perdue, Katherine L ^a   Wang, Ruopeng ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; CADASIL; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; DIFFUSION TENSOR IMAGING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HANDEDNESS; HEMIPARESIS; HUMAN; IMAGE ANALYSIS; MALE; MORPHOMETRICS; MOTOR PERFORMANCE; PRIORITY JOURNAL; PYRAMIDAL TRACT; SENSORIMOTOR CORTEX; STATISTICAL ANALYSIS; STROKE;

ADULT; AGED; CHRONIC DISEASE; ECHO-PLANAR IMAGING; FEMALE; HAND; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PARESIS; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL TRACTS; SOMATOSENSORY CORTEX; STROKE;

EID: 38049052294     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2007.09.071     Document Type: Article

References (81)

1. Basser P.J. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8 (1995) 333-344
2. Basser P.J., Mattiello J., and LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson., B 103 (1994) 247-254
3. Basser P.J., Pajevic S., Pierpaoli C., Duda J., and Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 44 (2000) 625-632
4. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., and Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. NeuroImage 34 (2007) 144-155
5. Biernaskie J., Szymanska A., Windle V., and Corbett D. Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur. J. Neurosci. 21 (2005) 989-999
6. Butefisch C.M., Kleiser R., Korber B., Muller K., Wittsack H.J., Homberg V., and Seitz R.J. Recruitment of contralesional motor cortex in stroke patients with recovery of hand function. Neurology 64 (2005) 1067-1069
7. Carpenter M.B. Human Neuroanatomy (1976), Williams and Wilkins Co, Baltimore
8. Chollet F., DiPiero V., Wise R.J.S., Brooks D.J., Dolan R.J., and Frackowiak R.S.J. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann. Neurol. 29 (1991) 63-71
9. Chung M.K., Worsley K.J., Robbins S., Paus T., Taylor J., Giedd J.N., Rapoport J.L., and Evans A.C. Deformation-based surface morphometry applied to gray matter deformation. NeuroImage 18 (2003) 198-213
10. Conturo T.E., Lori N.F., Cull T.S., Akbudak E., Snyder A.Z., Shimony J.S., McKinstry R.C., Burton H., and Raichle M.E. Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10422-10427
11. Cramer S.C., and Crafton K.R. Somatotopy and movement representation sites following cortical stroke. Exp. Brain Res. 168 (2006) 25-32
12. Cramer S.C., Nelles G., Benson R.R., Kaplan J.D., Parker R.A., Kwong K.K., Kennedy D.N., Finklestein S.P., and Rosen B.R. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28 (1997) 2518-2527
13. Dale A., Fischl B., and Sereno M. Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage 9 (1999) 179-194
14. Dancause N., Barbay S., Frost S.B., Zoubina E.V., Plautz E.J., Mahnken J.D., and Nudo R.J. Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. J. Neurophysiol. 96 (2006) 3506-3511
15. Desrosiers J., Hebert R., Bravo G., and Dutil E. The Purdue Pegboard test: normative data for people aged 60 and over. Disabil. Rehabil. 17 (1995) 217-224
16. Feydy A., Carlier R., Roby-Brami A., Bussel B., Cazalis F., Pierol L., Burnod Y., and Maier M.A. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 33 (2002) 1610-1617
17. Fischl B., Sereno M.I., and Dale A.M. Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. NeuroImage 9 (1999) 195-207
18. Fischl B., Sereno M.I., Tootell R.B.H., and Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 8 (1999) 272-284
19. Foltys H., Krings T., Meister I.G., Sparing R., Boroojerdi B., Thron A., and Topper R. Motor representation in patients rapidly recovering after stroke: a functional magnetic resonance imaging and transcranial magnetic stimulation study. Clin. Neurophysiol. 114 (2003) 2404-2415
20. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintum M.A., and Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33 (1995) 636-647
21. Fridman E.A., Hanakawa T., Chung M., Hummel F., Leiguarda R.C., and Cohen L.G. Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127 (2004) 747-758
22. Fries W., Danek A., Scheidtmann K., and Hamburger C. Motor recovery following capsular stroke: role of descending pathways from multiple motor areas. Brain 116 (1993) 369-382
23. Frost S.B., Barbay S., Friel K.M., Plautz E.J., and Nudo R.J. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. Neurophysiol. 89 (2003) 3205-3214
24. Gerloff C., Bushara K., Sailer A., Wassermann E.M., Chen R., Matsuoka T., Waldvogel D., Wittenberg G.F., Ishii K., Cohen L.G., and Hallett M. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 129 (2006) 791-808
25. Geyer S., Ledberg A., Schleicher A., Kinomura S., Schormann T., Burgel U., Klingberg T., Larsson J., Zilles K., and Roland P.E. Two different areas within the primary motor cortex of man. Nature 382 (1996) 805-807
26. Geyer S., Schleicher A., and Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex: 1. Microstructural organization and interindividual variability. NeuroImage 10 (1999) 63-83
27. Geyer S., Matelli M., Luppino G., and Zilles K. Functional neuroanatomy of the primate isocortical motor system. Anat. Embryol. (Berl) 202 (2000) 443-474
28. Grefkes C., Geyer S., Schormann T., Roland P., and Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage 14 (2001) 617-631
29. Hepp-Reymond M.C., and Wiesendanger M. Unilateral pyramidotomy in monkeys: effect on force and speed of a conditioned precision grip. Brain Res. 36 (1972) 117-131
30. Holodny A.I., Gor D.M., Watts R., Gutin P.H., and Ulug A.M. Diffusion-tensor MR tractography of somatotopic organization of corticospinal tracts in the internal capsule: initial anatomic results in contradistinction to prior reports. Radiology 234 (2005) 649-653
31. Inoue Y., Matsumura Y., Fukuda T., Nemoto Y., Shirahata N., Suzuki T., Shakudo M., Yawata S., Tanaka S., Takemoto K., et al. MR imaging of Wallerian degeneration in the brainstem: temporal relationships. AJNR Am. J. Neuroradiol. 11 (1990) 897-902
32. Jaillard A., Martin C.D., Garambois K., Lebas J.F., and Hommel M. Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. Brain 128 (2005) 1122-1138
33. Johansen-Berg H., and Behrens T.E. Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Curr. Opin. Neurol. 19 (2006) 379-385
34. Jones D.K., Lythgoe D., Horsfield M.A., Simmons A., Williams S.C., and Markus H.S. Characterization of white matter damage in ischemic leukoaraiosis with diffusion tensor MRI. Stroke 30 (1999) 393-397
35. Jones D.K., Simmons A., Williams S.C., and Horsfield M.A. Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn. Reson. Med. 42 (1999) 37-41
36. Kuhn M.J., Mikulis D.J., Ayoub D.M., Kosofsky B.E., Davis K.R., and Taveras J.M. Wallerian degeneration after cerebral infarction: evaluation with sequential MR imaging. Radiology 172 (1989) 179-182
37. Lotze M., Markert J., Sauseng P., Hoppe J., Plewnia C., and Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J. Neurosci. 26 (2006) 6096-6102
38. Loubinoux I., Carel C., Pariente J., Dechaumont S., Albucher J.F., Marque P., Manelfe C., and Chollet F. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. NeuroImage 20 (2003) 2166-2180
39. Mansur C.G., Fregni F., Boggio P.S., Riberto M., Gallucci-Neto J., Santos C.M., Wagner T., Rigonatti S.P., Marcolin M.A., and Pascual-Leone A. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64 (2005) 1802-1804
40. Medical Research Council (Great Britain). Aids to the Examination of the Peripheral Nervous System (1976), H.M. Stationery Office, London
41. Moller M., Frandsen J., Andersen G., Gjedde A., Vestergaard-Poulsen P., and Ostergaard L. Dynamic changes of corticospinal tracts after stroke detected by fibertracking. J. Neurol. Neurosurg. Psychiatry 78 (2007) 587-592
42. Morecraft R.J., Herrick J.L., Stilwell-Morecraft K.S., Louie J.L., Schroeder C.M., Ottenbacher J.G., and Schoolfield M.W. Localization of arm representation in the corona radiata and internal capsule in the non-human primate. Brain 125 (2002) 176-198
43. Mori S., Crain B.J., Chacko V.P., and van Zijl P.C. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45 (1999) 265-269
44. Nair D.G., Hutchinson S., Fregni F., Alexander M., Pascual-Leone A., and Schlaug G. Imaging correlates of motor recovery from cerebral infarction and their physiological significance in well-recovered patients. NeuroImage 34 (2007) 253-263
45. Newton J.M., Ward N.S., Parker G.J., Deichmann R., Alexander D.C., Friston K.J., and Frackowiak R.S. Non-invasive mapping of corticofugal fibres from multiple motor areas-relevance to stroke recovery. Brain 129 (2006) 1844-1858
46. Nudo R.J., and Milliken G. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J. Neurophysiol. 75 (1996) 2144-2149
47. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9 (1971) 97-113
48. Orita T., Tsurutani T., Izumihara A., and Kajiwara K. Early, evolving Wallerian degeneration of the pyramidal tract in cerebrovascular diseases: MR study. J. Comput. Assist. Tomogr. 18 (1994) 943-946
49. Pantano P., Mainero C., Iannetti G.D., Caramia F., Di Legge S., Piattella M.C., Pozzilli C., Bozzao L., and Lenzi G.L. Contribution of corticospinal tract damage to cortical motor reorganization after a single clinical attack of multiple sclerosis. NeuroImage 17 (2002) 1837-1843
50. Pierpaoli C., Jezzard P., Basser P.J., Barnett A., and Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 201 (1996) 637-648
51. Pierpaoli C., Barnett A., Pajevic S., Chen R., Penix L., Virta A., and Basser P. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage 13 (2001) 1174-1185
52. Reddy H., De Stefano N., Mortilla M., Federico A., and Matthews P.M. Functional reorganization of motor cortex increases with greater axonal injury from CADASIL. Stroke 33 (2002) 502-508
53. Reese T.G., Heid O., Weisskoff R.M., and Wedeen V.J. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn. Reson. Med. 49 (2003) 177-182
54. Sage C.A., Peeters R.R., Gorner A., Robberecht W., and Sunaert S. Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. NeuroImage 34 (2007) 486-499
55. Schaechter J.D., and Perdue K.L. Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb. Cortex (2007) (Advance Access published June 29, 2007)
56. Schambra H.M., Sawaki L., and Cohen L.G. Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin. Neurophysiol. 114 (2003) 130-133
57. Schaechter J.D., Stokes C., Connell B.D., Perdue K., and Bonmassar G. Finger motion sensors for fMRI motor studies. Neuroimage 31 (2006) 1549-1559
58. Shimoyama I., Ninchoji T., and Uemura K. The finger-tapping test. A quantitative analysis. Arch. Neurol. 47 (1990) 681-684
59. Stinear C.M., Barber P.A., Smale P.R., Coxon J.P., Fleming M.K., and Byblow W.D. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130 (2007) 170-180
60. Stovring J., and Fernando L.T. Wallerian degeneration of the corticospinal tract region of the brain stem: demonstration by computed tomography. Radiology 149 (1983) 717-720
61. Takeuchi N., Chuma T., Matsuo Y., Watanabe I., and Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36 (2005) 2681-2686
62. Thesen A., Heid O., Mueller E., and Schad L.R. Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magn. Reson. Med. 44 (2000) 457-465
63. Thomalla G., Glauche V., Koch M.A., Beaulieu C., Weiller C., and Rother J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. NeuroImage 22 (2004) 1767-1774
64. Thomalla G., Glauche V., Weiller C., and Rother J. Time course of wallerian degeneration after ischaemic stroke revealed by diffusion tensor imaging. J. Neurol. Neurosurg. Psychiatry 76 (2005) 266-268
65. Thomas B., Eyssen M., Peeters R., Molenaers G., Van Hecke P., De Cock P., and Sunaert S. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 128 (2005) 2562-2577
66. Tiffin J., and Asher E.J. The Purdue Pegboard: norms and studies of reliability and validity. J. Appl. Psychol. 32 (1948) 234-247
67. Tombari D., Loubinoux I., Pariente J., Gerdelat A., Albucher J.F., Tardy J., Cassol E., and Chollet F. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. NeuroImage 23 (2004) 827-839
68. van der Kouwe A.J., Benner T., Fischl B., Schmitt F., Salat D.H., Harder M., Sorensen A.G., and Dale A.M. On-line automatic slice positioning for brain MR imaging. NeuroImage 27 (2005) 222-230
69. Warabi T., Miyasaka K., Inoue K., and Nakamura N. Computed tomographic studies of the basis pedunculi in chronic hemiplegic patients: topographic correlation between cerebral lesion and midbrain shrinkage. Neuroradiology 29 (1987) 409-415
70. Warabi T., Inoue K., Noda H., and Murakami S. Recovery of voluntary movement in hemiplegic patients. Correlation with degenerative shrinkage of the cerebral peduncles in CT images. Brain 113 (1990) 177-189
71. Ward N.S., Newton J.M., Swayne O.B., Lee L., Thompson A.J., Greenwood R.J., Rothwell J.C., and Frackowiak R.S. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 129 (2006) 809-819
72. Wedeen V.J., Hagmann P., Tseng W.Y., Reese T.G., and Weisskoff R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 54 (2005) 1377-1386
73. Weiller C., Ramsay S.C., Wise R.J.S., Friston K.J., and Frackowiak R.S.J. Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann. Neurol. 33 (1993) 181-189
74. Wenzelburger R., Kopper F., Frenzel A., Stolze H., Klebe S., Brossmann A., Kuhtz-Buschbeck J., Golge M., Illert M., and Deuschl G. Hand coordination following capsular stroke. Brain 128 (2005) 64-74
75. Werhahn K.J., Conforto A.B., Kadom N., Hallett M., and Cohen L.G. Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann. Neurol. 54 (2003) 464-472
76. Werring D.J., Toosy A.T., Clark C.A., Parker G.J., Barker G.J., Miller D.H., and Thompson A.J. Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. J. Neurol. Neurosurg. Psychiatry 69 (2000) 269-272
77. Wiesendanger M. Pyramidal tract function and the clinical "pyramidal syndrome". Hum. Neurobiol. 2 (1984) 227-234
78. Wieshmann U.C., Clark C.A., Symms M.R., Franconi F., Barker G.J., and Shorvon S.D. Anisotropy of water diffusion in corona radiata and cerebral peduncle in patients with hemiparesis. NeuroImage 10 (1999) 225-230
79. Yang Q., Tress B.M., Barber P.A., Desmond P.M., Darby D.G., Gerraty R.P., Li T., and Davis S.M. Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 30 (1999) 2382-2390
80. Yousry T.A., Schmid U.D., Alkadhi H., Schmidt D., Peraud A., Buettner A., and Winkler P. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120 (1997) 141-157
81. Zemke A.C., Heagerty P.J., Lee C., and Cramer S.C. Motor cortex organization after stroke is related to side of stroke and level of recovery. Stroke 34 (2003) e23-e28