Tracking changes following spinal cord injury: Insights from neuroimaging

Neuroscientist

Volumn 19, Issue 2, 2013, Pages 116-128

  Freund, Patrick ^a,b   Curt, Armin ^b   Friston, Karl ^a   Thompson, Alan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Atrophy; Cortical reorganization; Disability; Neuroimaging

Indexed keywords

ARTICLE; DISABILITY; FUNCTIONAL ANATOMY; HUMAN; NEUROIMAGING; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SPINAL CORD ATROPHY; SPINAL CORD INJURY;

HUMANS; NEUROIMAGING; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 84877796369     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858412449192     Document Type: Article

References (82)

1. Aguilar J, Humanes-Valera D, Alonso-Calvino E, Yague JG, Moxon KA, Oliviero A, and others. 2010. Spinal cord injury immediately changes the state of the brain. J Neurosci 30: 7528-37.
2. Andre JB, Bammer R. 2010. Advanced diffusion-weighted magnetic resonance imaging techniques of the human spinal cord. Top Magn Reson Imaging 21: 367-78.
3. Ashburner J, Friston KJ. 2000. Voxel-based morphometry-the methods. Neuroimage 11: 805-21.
4. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. 2004. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7: 269-77.
5. Barkhof F, Calabresi PA, Miller DH, Reingold SC. 2009. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nat Rev Neurol 5: 256-66.
6. Basser PJ, Pierpaoli C. 1996. Microstructural and physiological features of tissues elucidated by quantitative-diffusiontensor MRI. J Magn Reson B 111: 209-19.
7. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O. 2009. Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: an in vivo study with TBSS and VBM. Hum Brain Mapp 30: 2852-61.
8. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, and others. 2002. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-40.
9. Budde MD, Kim JH, Liang HF, Russell JH, Cross AH, Song SK. 2008. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed 21: 589-97.
10. Calancie B, Lutton S, Broton JG. 1996. Central nervous system plasticity after spinal cord injury in man: interlimb reflexes and the influence of cutaneous stimulation. Electroencephalogr Clin Neurophysiol 101: 304-15.
11. Casha S, Zygun D, McGowan MD, Bains I, Yong VW, John HR. 2012. Results of a phase II placebo-controlled randomized trial of minocycline in acute spinal cord injury. Brain 135: 1224-36.
12. Cheran S, Shanmuganathan K, Zhuo J, Mirvis SE, Aarabi B, Alexander MT, and others. 2011. Correlation of MR diffusion tensor imaging parameters with ASIA motor scores in hemorrhagic and nonhemorrhagic acute spinal cord injury. J Neurotrauma 28: 1881-92.
13. Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A. 2008. Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol 7: 715-27.
14. Cohen-Adad J, El Mendili MM, Lehericy S, Pradat PF, Blancho S, Rossignol S, and others. 2011. Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI. Neuroimage 55: 1024-33.
15. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, and others. 2008. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 14: 69-74.
16. Crawley AP, Jurkiewicz MT, Yim A, Heyn S, Verrier MC, Fehlings MG, and others. 2004. Absence of localized grey matter volume changes in the motor cortex following spinal cord injury. Brain Res 1028: 19-25.
17. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, and others. 2005. Human neural stem cells differentiate and promote locomotor recovery in spinal cordinjured mice. Proc Natl Acad Sci U S A 102: 14069-74.
18. Curt A. 2012. The translational dialogue in spinal cord injury research. Spinal Cord 50: 352-7.
19. Curt A, Alkadhi H, Crelier GR, Boendermaker SH, Hepp- Reymond MC, Kollias SS. 2002. Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain 125: 2567-78.
20. Curt A, van Hedel HJ, Klaus D, Dietz V. 2008. Recovery from a spinal cord injury: significance of compensation, neural plasticity, and repair. J Neurotrauma 25: 677-85.
21. Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RS, Helms G, and others. 2011. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 55: 1423-34.
22. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. 2004. Neuroplasticity: changes in grey matter induced by training. Nature 427: 311-2.
23. Dusart I, Schwab ME. 1994. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6: 712-24.
24. Elbert T, Flor H, Birbaumer N, Knecht S, Hampson S, Larbig W, and others. 1994. Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. Neuroreport 5: 2593-7.
25. Endo T, Tominaga T, Olson L. 2009. Cortical changes following spinal cord injury with emphasis on the Nogo signaling system. Neuroscientist 15: 291-9.
26. Fawcett JW, Curt A, Steeves JD, Coleman WP, Tuszynski MH, Lammertse D, and others. 2007. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 45: 190-205.
27. Fehlings MG, Cadotte DW, Fehlings LN. 2011. A series of systematic reviews on the treatment of acute spinal cord injury: a foundation for best medical practice. J Neurotrauma 28: 1329-33.
28. Felix MS, Popa N, Djelloul M, Boucraut J, Gauthier P, Bauer S, and others. 2012. Alteration of forebrain neurogenesis after cervical spinal cord injury in the adult rat. Front Neurosci 6: 45.
29. Fields RD. 2008. White matter in learning, cognition and psychiatric disorders. Trends Neurosci 31: 361-70.
30. Freund P, Rothwell J, Craggs M, Thompson AJ, Bestmann S. 2011a. Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury. Eur J Neurosci 34: 1839-46.
31. Freund P, Schmidlin E, Wannier T, Bloch J, Mir A, Schwab ME, and others. 2006. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat Med 12: 790-2.
32. Freund P, Weiskopf N, Ward NS, Hutton C, Gall A, Ciccarelli O, and others. 2011b. Disability, atrophy and cortical reorganization following spinal cord injury. Brain 134: 1610-22.
33. Freund P, Wheeler-Kingshott C, Jackson J, Miller D, Thompson A, Ciccarelli O. 2010a. Recovery after spinal cord relapse in multiple sclerosis is predicted by radial diffusivity. Mult Scler 16: 1193-202.
34. Freund P, Wheeler-Kingshott CA, Nagy Z, Gorgoraptis N, Weiskopf N, Friston K, and others. 2012. Axonal integrity predicts cortical reorganisation following cervical injury. J Neurol Neurosurg Psychiatry 83: 629-37.
35. Freund PA, Dalton C, Wheeler-Kingshott CA, Glensman J, Bradbury D, Thompson AJ, and others. 2010b. Method for simultaneous voxel-based morphometry of the brain and cervical spinal cord area measurements using 3D-MDEFT. J Magn Reson Imaging 32: 1242-7.
36. Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD. 1996. Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4: 223-35.
37. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ. 1995. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2: 189-210.
38. Ghosh A, Haiss F, Sydekum E, Schneider R, Gullo M, Wyss MT, and others. 2010. Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat Neurosci 13: 97-104.
39. Ghosh A, Peduzzi S, Snyder M, Schneider R, Starkey M, Schwab ME. 2011. Heterogeneous spine loss in layer 5 cortical neurons after spinal cord injury. Cereb Cortex. doi: 10.1093/cercor/bhr191.
40. Guleria S, Gupta RK, Saksena S, Chandra A, Srivastava RN, Husain M, and others. 2008. Retrograde Wallerian degeneration of cranial corticospinal tracts in cervical spinal cord injury patients using diffusion tensor imaging. J Neurosci Res 86: 2271-80.
41. Hains BC, Black JA, Waxman SG. 2003. Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury. J Comp Neurol 462: 328-41.
42. Henderson LA, Gustin SM, Macey PM, Wrigley PJ, Siddall PJ. 2011. Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy. J Neurosci 31: 2630-7.
43. Horsfield MA, Sala S, Neema M, Absinta M, Bakshi A, Sormani MP, and others. 2010. Rapid semi-automatic segmentation of the spinal cord from magnetic resonance images: application in multiple sclerosis. Neuroimage 50: 446-55.
44. Hubli M, Dietz V, Bolliger M. 2012. Spinal reflex activity: a marker for neuronal functionality after spinal cord injury. Neurorehabil Neural Repair 26: 188-96.
45. Hutton C, De Vita E, Ashburner J, Deichmann R, Turner R. 2008. Voxel-based cortical thickness measurements in MRI. Neuroimage 40: 1701-10.
46. 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: 371-80.
47. Jacobs KM, Donoghue JP. 1991. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251: 944-7.
48. Jones EG. 2000. Cortical and subcortical contributions to activity- dependent plasticity in primate somatosensory cortex. Annu Rev Neurosci 23: 1-37.
49. Jurkiewicz MT, Crawley AP, Verrier MC, Fehlings MG, Mikulis DJ. 2006. Somatosensory cortical atrophy after spinal cord injury: a voxel-based morphometry study. Neurology 66: 762-4.
50. Jurkiewicz MT, Mikulis DJ, Fehlings MG, Verrier MC. 2010. Sensorimotor cortical activation in patients with cervical spinal cord injury with persisting paralysis. Neurorehabil Neural Repair 24: 136-40.
51. Jurkiewicz MT, Mikulis DJ, McIlroy WE, Fehlings MG, Verrier MC. 2007. Sensorimotor cortical plasticity during recovery following spinal cord injury: a longitudinal fMRI study. Neurorehabil Neural Repair 21: 527-38.
52. Kim BG, Dai HN, McAtee M, Vicini S, Bregman BS. 2006. Remodeling of synaptic structures in the motor cortex following spinal cord injury. Exp Neurol 198: 401-15.
53. Kim JH, Loy DN, Wang Q, Budde MD, Schmidt RE, Trinkaus K, and others. 2010. Diffusion tensor imaging at 3 hours after traumatic spinal cord injury predicts long-term locomotor recovery. J Neurotrauma 27: 587-98.
54. Kokotilo KJ, Eng JJ, Curt A. 2009. Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J Neurotrauma 26: 2113-26.
55. Lang C, Guo X, Kerschensteiner M, Bareyre FM. 2012. Single collateral reconstructions reveal distinct phases of corticospinal remodeling after spinal cord injury. PLoS One 7: e30461.
56. Langer N, Hanggi J, Muller NA, Simmen HP, Jancke L. 2012. Effects of limb immobilization on brain plasticity. Neurology 78: 182-8.
57. Losseff NA, Webb SL, O'Riordan JI, Page R, Wang L, Barker GJ, and others. 1996. Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain 119: 701-8.
58. Lundell H, Barthelemy D, Skimminge A, Dyrby TB, Biering- Sorensen F, Nielsen JB. 2011a. Independent spinal cord atrophy measures correlate to motor and sensory deficits in individuals with spinal cord injury. Spinal Cord 49: 70-5.
59. Lundell H, Christensen MS, Barthelemy D, Willerslev-Olsen M, Biering-Sorensen F, Nielsen JB. 2011b. Cerebral activation is correlated to regional atrophy of the spinal cord and functional motor disability in spinal cord injured individuals. Neuroimage 54: 1254-61.
60. Miller DH, Barkhof F, Frank JA, Parker GJ, Thompson AJ. 2002. Measurement of atrophy in multiple sclerosis: pathological basis, methodological aspects and clinical relevance. Brain 125: 1676-95.
61. Mohammadi S, Nagy Z, Hutton C, Josephs O, Weiskopf N. 2011. Correction of vibration artifacts in DTI using phase-encoding reversal (COVIPER). Magn Reson Med. doi: 10.1002/mrm.23308.
62. Mohammadi S, Nagy Z, Moller HE, Symms MR, Carmichael DW, Josephs O, and others. 2012. The effect of local perturbation fields on human DTI: characterisation, measurement and correction. Neuroimage 60: 562-70.
63. Morelli JN, Runge VM, Feiweier T, Kirsch JE, Williams KW, Attenberger UI. 2010. Evaluation of a modified Stejskal- Tanner diffusion encoding scheme, permitting a marked reduction in TE, in diffusion-weighted imaging of stroke patients at 3 T. Invest Radiol 45: 29-35.
64. Nicotra A, Critchley HD, Mathias CJ, Dolan RJ. 2006. Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging. Brain 129: 718-28.
65. Nishimura Y, Onoe H, Morichika Y, Perfiliev S, Tsukada H, Isa T. 2007. Time-dependent central compensatory mechanisms of finger dexterity after spinal cord injury. Science 318: 1150-5.
66. Petersen JA, Wilm BJ, von Meyenburg J, Schubert M, Seifert B, Najafi Y, and others. 2012. Chronic cervical spinal cord injury: DTI correlates with clinical and electrophysiological measures. J Neurotrauma 29: 1556-66.
67. Ramer MS, Priestley JV, McMahon SB. 2000. Functional regeneration of sensory axons into the adult spinal cord. Nature 403: 312-6.
68. Schmid MR, Pfirrmann CW, Koch P, Zanetti M, Kuehn B, Hodler J. 2005. Imaging of patellar cartilage with a 2D multiple-echo data image combination sequence. AJR Am J Roentgenol 184: 1744-8.
69. Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH. 2004. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 56: 407-15.
70. Schmierer K, Wheeler-Kingshott CA, Boulby PA, Scaravilli F, Altmann DR, Barker GJ, and others. 2007. Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage 35: 467-77.
71. Schwab ME. 2002. Repairing the injured spinal cord. Science 295: 1029-31.
72. Thurnher MM, Law M. 2009. Diffusion-weighted imaging, diffusion-tensor imaging, and fiber tractography of the spinal cord. Magn Reson Imaging Clin N Am 17: 225-44.
73. Tseng GF, Prince DA. 1996. Structural and functional alterations in rat corticospinal neurons after axotomy. J Neurophysiol 75: 248-67.
74. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW. 2011. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31: 9332-44.
75. Wannier T, Schmidlin E, Bloch J, Rouiller EM. 2005. A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. J Neurotrauma 22: 703-17.
76. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. 2004. The influence of time after stroke on brain activations during a motor task. Ann Neurol 55: 829-34.
77. Weiskopf N, Lutti A, Helms G, Novak M, Ashburner J, Hutton C. 2011. Unified segmentation based correction of R1 brain maps for RF transmit field inhomogeneities (UNICORT). Neuroimage 54: 2116-24.
78. Wilm BJ, Gamper U, Henning A, Pruessmann KP, Kollias SS, Boesiger P. 2009. Diffusion-weighted imaging of the entire spinal cord. NMR Biomed 22: 174-81.
79. Woollett K, Maguire EA. 2011. Acquiring "the knowledge" of London's layout drives structural brain changes. Curr Biol 21: 2109-14.
80. Wrigley PJ, Gustin SM, Macey PM, Nash PG, Gandevia SC, Macefield VG, and others. 2009. Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb Cortex 19: 224-32.
81. Wyndaele M, Wyndaele JJ. 2006. Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord 44: 523-29.
82. Yague JG, Foffani G, Aguilar J. 2011. Cortical hyperexcitability in response to preserved spinothalamic inputs immediately after spinal cord hemisection. Exp Neurol 227: 252-63.