The current state-of-the-art of spinal cord imaging: Applications

NeuroImage

Volumn 84, Issue , 2014, Pages 1082-1093

  Wheeler Kingshott, C A ^a   Stroman, P W ^b   Schwab, J M ^c,d   Bacon, M ^e   Bosma, R ^b   Brooks, J ^r   Cadotte, D W ^g   Carlstedt, T ^a   Ciccarelli, O ^a,h   Cohen Adad, J ⁱ   Curt, A ^j   Evangelou, N ^k   Fehlings, M G ^g   Filippi, M ^l   Kelley, B J ^m   Kollias, S ⁿ   Mackay, A ^o   Porro, C A ^p   Smith, S ^q   Strittmatter, S M ^m   Summers, P ^p   Thompson, A J ^a,h   Tracey, I ^f   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN S UNIVERSITY   (Canada)

^c Wings for Life Spinal Cord Research Foundation   (Austria)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e International Spinal Research Trust   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g UNIVERSITY OF TORONTO   (Canada)

^h National Institute for Health Research University College London Hospitals Biomedical Research Centre ^*  (United Kingdom)

ⁱ ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^j BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

^k UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^l VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^m YALE UNIVERSITY   (United States)

ⁿ UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^o UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^p UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^q VANDERBILT UNIVERSITY   (United States)

^r UNIVERSITY OF BRISTOL   (United Kingdom)

more..

Author keywords

Diffusion; Functional MRI; Magnetic resonance; Pathology; Spinal cord; Spinal cord injury

Indexed keywords

ANALGESIC AGENT;

CERVICAL SPONDYLOTIC MYELOPATHY; CLINICAL PRACTICE; COMPUTER PROGRAM; DIAGNOSTIC ACCURACY; DIAGNOSTIC VALUE; DIFFUSION TENSOR IMAGING; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GOLD STANDARD; HUMAN; IMAGE DISPLAY; IMAGE PROCESSING; IMAGE QUALITY; MEDICAL RESEARCH; METAL IMPLANTATION; MULTIPLE SCLEROSIS; NERVE FIBER DEGENERATION; NEUROIMAGING; NEUROMODULATION; NEUROPATHIC PAIN; NEUROSCIENCE; NOCICEPTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PATIENT MONITORING; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS; RECEIVER OPERATING CHARACTERISTIC; REVIEW; SENSITIVITY AND SPECIFICITY; SPINAL CORD COMPRESSION; SPINAL CORD DISEASE; SPINAL CORD INJURY; VOXEL BASED MORPHOMETRY;

DIFFUSION; FUNCTIONAL MRI; MAGNETIC RESONANCE; PATHOLOGY; SPINAL CORD; SPINAL CORD INJURY;

ANIMALS; HUMANS; MAGNETIC RESONANCE IMAGING; SPINAL CORD; SPINAL CORD DISEASES; SPINAL CORD INJURIES;

EID: 84888848353     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.07.014     Document Type: Review

References (151)

1. Agosta F., Filippi M. MRI of spinal cord in multiple sclerosis. J. Neuroimaging 2007, 17(Suppl. 1):46S-49S.
2. Agosta F., Benedetti B., Rocca M.A., Valsasina P., Rovaris M., Comi G., Filippi M. Quantification of cervical cord pathology in primary progressive MS using diffusion tensor MRI. Neurology 2005, 64:631-635.
3. Agosta F., Absinta M., Sormani M.P., Ghezzi A., Bertolotto A., Montanari E., Comi G., Filippi M. In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain 2007, 130:2211-2219.
4. Agosta F., Pagani E., Caputo D., Filippi M. Associations between cervical cord gray matter damage and disability in patients with multiple sclerosis. Arch. Neurol. 2007, 64:1302-1305.
5. Agosta F., Valsasina P., Caputo D., Stroman P.W., Filippi M. Tactile-associated recruitment of the cervical cord is altered in patients with multiple sclerosis. NeuroImage 2008, 39:1542-1548.
6. Agosta F., Valsasina P., Rocca M.A., Caputo D., Sala S., Judica E., Stroman P.W., Filippi M. Evidence for enhanced functional activity of cervical cord in relapsing multiple sclerosis. Magn. Reson. Med. 2008, 59:1035-1042.
7. Agosta F., Rocca M.A., Valsasina P., Sala S., Caputo D., Perini M., Salvi F., Prelle A., Filippi M. A longitudinal diffusion tensor MRI study of the cervical cord and brain in amyotrophic lateral sclerosis patients. J. Neurol. Neurosurg. Psychiatry. 2009, 80:53-55.
8. Agosta F., Valsasina P., Absinta M., Sala S., Caputo D., Filippi M. Primary progressive multiple sclerosis: tactile-associated functional MR activity in the cervical spinal cord. Radiology 2009, 253:209-215.
9. Agosta F., Valsasina P., Caputo D., Rocca M.A., Filippi M. Tactile-associated fMRI recruitment of the cervical cord in healthy subjects. Hum. Brain Mapp. 2009, 30:340-345.
10. Aloisi A.M., Porro C.A., Cavazzuti M., Baraldi P., Carli G. 'Mirror pain' in the formalin test: behavioral and 2-deoxyglucose studies. Pain 1993, 55:267-273.
11. Apkarian A.V., Bushnell M.C., Treede R.D., Zubieta J.K. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain. 2005, 9(4):463-484.
12. Arvin B., Kalsi-Ryan S., Mercier D., Furlan J.C., Massicotte E.M., Fehlings M.G. Preoperative magnetic resonance imaging is associated with baseline neurological status and can predict postoperative recovery in patients with cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2013, 38:1170-1176.
13. Backes W.H., Mess W.H., Wilmink J.T. Functional MR imaging of the cervical spinal cord by use of median nerve stimulation and fist clenching. AJNR Am. J. Neuroradiol. 2001, 22:1854-1859.
14. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
15. Benedetti B., Rocca M.A., Rovaris M., Caputo D., Zaffaroni M., Capra R., Bertolotto A., Martinelli V., Comi G., Filippi M. A diffusion tensor MRI study of cervical cord damage in benign and secondary progressive multiple sclerosis patients. J. Neurol. Neurosurg. Psychiatry. 2010, 81:26-30.
16. Brex P.A., Leary S.M., O'Riordan J.I., Miszkiel K.A., Plant G.T., Thompson A.J., Miller D.H. Measurement of spinal cord area in clinically isolated syndromes suggestive of multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2001, 70:544-547.
17. Brooks J.C., Beckmann C.F., Miller K.L., Wise R.G., Porro C.A., Tracey I., Jenkinson M. Physiological noise modelling for spinal functional magnetic resonance imaging studies. NeuroImage 2008, 39:680-692.
18. Brooks J.C.W., Kong Y., Lee M.C., Warnaby C.E., Wanigasekera V., Jenkinson M., Tracey I. Stimulus site and modality dependence of functional activity within the human spinal cord. J. Neurosci. 2012, 32:6231-6239.
19. Budde M.D., Kim J.H., Liang H.F., Schmidt R.E., Russell J.H., Cross A.H., Song S.K. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn. Reson. Med. 2007, 57:688-695.
20. Budde M.D., Kim J.H., Liang H.-F., Russell J.H., Cross A.H., Song S.-K. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed. 2008, 21:589-597.
21. Budde M.D., Xie M., Cross A.H., Song S.-K. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J. Neurosci. 2009, 29:2805-2813.
22. Budzik J.F., Balbi V., Le Thuc V., Duhamel A., Assaker R., Cotten A. Diffusion tensor imaging and fibre tracking in cervical spondylotic myelopathy. Eur. Radiol. 2011, 21:426-433.
23. Bullitt E. Somatotopy of spinal nociceptive processing. J. Comp. Neurol. 1991, 312:279-290.
24. Cahill C.M., Stroman P.W. Mapping of neural activity produced by thermal pain in the healthy human spinal cord and brain stem: a functional magnetic resonance imaging study. Magn. Reson. Imaging 2011, 29:342-352.
25. Charil A., Caputo D., Cavarretta R., Sormani M.P., Ferrante P., Filippi M. Cervical cord magnetization transfer ratio and clinical changes over 18months in patients with relapsing-remitting multiple sclerosis: a preliminary study. Mult. Scler. 2006, 12:662-665.
26. Ciccarelli O., Wheeler-Kingshott C.A., McLean M.A., Cercignani M., Wimpey K., Miller D.H., Thompson A.J. Spinal cord spectroscopy and diffusion-based tractography to assess acute disability in multiple sclerosis. Brain 2007, 130:2220-2231.
27. Ciccarelli O., Altmann D.R., McLean M.A., Wheeler-Kingshott C.A., Wimpey K., Miller D.H., Thompson A.J. Spinal cord repair in MS: does mitochondrial metabolism play a role?. Neurology 2010, 74:721-727.
28. Ciccarelli O., Toosy A.T., De Stefano N., Wheeler-Kingshott C.A., Miller D.H., Thompson A.J. Assessing neuronal metabolism in vivo by modeling imaging measures. J. Neurosci. 2010, 30:15030-15033.
29. Ciccarelli O., Thomas D., De Vita E., Wheeler-Kingshott C., Kachramanoglou C., Kapoor R., Leary S., Matthews L., Palace J., Chard D., Miller D., Toosy A., Thompson A. Low myo-inositol indicating astrocytic damage in a case series of NMO. Ann. Neurol. 2013, (in press, Electronic publication ahead of print).
30. Coggeshall R.E. Fos, nociception and the dorsal horn. Prog. Neurobiol. 2005, 77:299-352.
31. Coghill R.C., Price D.D., Hayes R.L., Mayer D.J. Spatial distribution of nociceptive processing in the rat spinal cord. J. Neurophysiol. 1991, 65:133-140.
32. Cohen-Adad J., Descoteaux M., Rossignol S., Hoge R.D., Deriche R., Benali H. Detection of multiple pathways in the spinal cord using q-ball imaging. NeuroImage 2008, 42:739-749.
33. Cohen-Adad J., El Mendili M.-M., Lehéricy S., Pradat P.-F., Blancho S., Rossignol S., Benali H. Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI. NeuroImage 2011, 55:1024-1033.
34. Cohen-Adad J., Buchbinder B., Oaklander A.L. Cervical spinal cord injection of epidural corticosteroids; comprehensive longitudinal study including multiparametric MRI. Pain 2012, 153:2292-2299.
35. Cohen-Adad J., El Mendili M.M., Morizot-Koutlidis R., Lehericy S., Meininger V., Blancho S., Rossignol S., Benali H., Pradat P.-F. Involvement of spinal sensory pathway in ALS and specificity of cord atrophy to lower motor neuron degeneration. Amyotroph. Lateral Scler. Frontotemporal Degener. 2013, 14(1):30-38.
36. Cui J.L., Wen C.Y., Hu Y., Mak K.C., Mak K.H., Luk K.D. Orientation entropy analysis of diffusion tensor in healthy and myelopathic spinal cord. NeuroImage 2011, 58:1028-1033.
37. DeBoy C.A., Zhang J., Dike S., Shats I., Jones M., Reich D.S., Mori S., Nguyen T., Rothstein B., Miller R.H., Griffin J.T., Kerr D.A., Calabresi P.A. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 2007, 130:2199-2210.
38. Eippert F., Bingel U., Schoell E.D., Yacubian J., Klinger R., Lorenz J., Buchel C. Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 2009, 63:533-543.
39. Eippert F., Finsterbusch J., Bingel U., Buchel C. Direct evidence for spinal cord involvement in placebo analgesia. Science 2009, 326:404.
40. Ellingson B.M., Ulmer J.L., Kurpad S.N., Schmit B.D. Diffusion tensor MR imaging in chronic spinal cord injury. AJNR Am. J. Neuroradiol. 2008, 29:1976-1982.
41. Elliott J.M., Pedler A.R., Cowin G., Sterling M., McMahon K. Spinal cord metabolism and muscle water diffusion in whiplash. Spinal Cord 2012, 50:474-476.
42. Facon D., Ozanne A., Fillard P., Lepeintre J.F., Tournoux-Facon C., Ducreux D. MR diffusion tensor imaging and fiber tracking in spinal cord compression. AJNR Am. J. Neuroradiol. 2005, 26(6):1587-1594.
43. Farrell J.A., Smith S.A., Gordon-Lipkin E.M., Reich D.S., Calabresi P.A., van Zijl P.C. High b-value q-space diffusion-weighted MRI of the human cervical spinal cord in vivo: feasibility and application to multiple sclerosis. Magn. Reson. Med. 2008, 59:1079-1089.
44. Fawcett J.W., Curt A., Steeves J.D., Coleman W.P., Tuszynski M.H., Lammertse D., Bartlett P.F., Blight A.R., Dietz V., Ditunno J., Dobkin B.H., Havton L.A., Ellaway P.H., Fehlings M.G., Privat A., Grossman R., Guest J.D., Kleitman N., Nakamura M., Gaviria M., Short D. 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 2007, 45:190-205.
45. Figley C.R., Stroman P.W. Measurement and characterization of the human spinal cord SEEP response using event-related spinal fMRI. Magn. Reson. Imaging 2012, 30(4):471-484.
46. Finsterbusch J. Functional neuroimaging of inner fields-of-view with 2D-selective RF excitations. Magn. Reson. Imaging 2013, (in press, Electronic publication ahead of print).
47. Finsterbusch J., Eippert F., Buchel C. Single, slice-specific z-shim gradient pulses improve T2*-weighted imaging of the spinal cord. NeuroImage 2012, 59:2307-2315.
48. Finsterbusch J., Sprenger C., Buchel C. Combined T2*-weighted measurements of the human brain and cervical spinal cord with a dynamic shim update. NeuroImage 2013, 79:153-161.
49. Freund P., Weiskopf N., Ward N.S., Hutton C., Gall A., Ciccarelli O., Craggs M., Friston K., Thompson A.J. Disability, atrophy and cortical reorganization following spinal cord injury. Brain 2011, 134:1610-1622.
50. Freund P., Schneider T., Nagy Z., Hutton C., Weiskopf N., Friston K., Wheeler-Kingshott C.A., Thompson A.J. Degeneration of the injured cervical cord is associated with remote changes in corticospinal tract integrity and upper limb impairment. PLoS One 2012, 7:e51729.
51. Freund P., Wheeler-Kingshott C.A., Nagy Z., Gorgoraptis N., Weiskopf N., Friston K., Thompson A.J., Hutton C. Axonal integrity predicts cortical reorganisation following cervical injury. J. Neurol. Neurosurg. Psychiatry 2012, 83:629-637.
52. Freund P., Weiskopf N., Ashburner J., Wolf K., Sutter R., Altmann D.R., Friston K., Thompson A., Curt A. Investigation of the sensorimotor cortex and corticospinal tract after acute spinal cord injury: a prospective longitudinal MRI study. Lancet Neurol. 2013, (in press, Electronic publication ahead of print).
53. Ghazni N.F., Cahill C.M., Stroman P.W. Tactile sensory and pain networks in the human spinal cord and brain stem mapped by means of functional MR imaging. AJNR Am. J. Neuroradiol. 2010, 31:661-667.
54. Goldfarb J.W., McLaughlin J., Gray C.A., Han J. Cyclic CINE-balanced steady-state free precession image intensity variations: implications for the detection of myocardial edema. J. Magn. Reson. Imaging 2011, 33:573-581.
55. Gwak Y.S., Hulsebosch C.E. GABA and central neuropathic pain following spinal cord injury. Neuropharmacology 2011, 60:799-808.
56. Herrera J.J., Chacko T., Narayana P.A. Histological correlation of diffusion tensor imaging metrics in experimental spinal cord injury. J. Neurosci. Res. 2008, 86:443-447.
57. Hesseltine S.M., Law M., Babb J., Rad M., Lopez S., Ge Y., Johnson G., Grossman R.I. Diffusion tensor imaging in multiple sclerosis: assessment of regional differences in the axial plane within normal-appearing cervical spinal cord. AJNR Am. J. Neuroradiol. 2006, 27:1189-1193.
58. Hochman S. Spinal cord. Curr. Biol. 2007, 17:R950-R955.
59. Hofling A.A., Kim J.H., Fantz C.R., Sands M.S., Song S.-K. Diffusion tensor imaging detects axonal injury and demyelination in the spinal cord and cranial nerves of a murine model of globoid cell leukodystrophy. NMR Biomed. 2009, 22:1100-1106.
60. Holly L.T., Freitas B., McArthur D.L., Salamon N. Proton magnetic resonance spectroscopy to evaluate spinal cord axonal injury in cervical spondylotic myelopathy. J. Neurosurg. Spine 2009, 10:194-200.
61. Hori M., Fukunaga I., Masutani Y., Nakanishi A., Shimoji K., Kamagata K., Asahi K., Hamasaki N., Suzuki Y., Aoki S. New diffusion metrics for spondylotic myelopathy at an early clinical stage. Eur. Radiol. 2012, 22:1797-1802.
62. Horsfield M.A., Sala S., Neema M., Absinta M., Bakshi A., Sormani M.P., Rocca M.A., Bakshi R., Filippi M. Rapid semi-automatic segmentation of the spinal cord from magnetic resonance images: application in multiple sclerosis. NeuroImage 2010, 50:446-455.
63. Hunt S.P., Pini A., Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 1987, 328:632-634.
64. Jones A.K., Brown W.D., Friston K.J., Qi L.Y., Frackowiak R.S. Cortical and subcortical localization of response to pain in man using positron emission tomography. Proc. Biol. Sci. 1991, 244:39-44.
65. Kachramanoglou C., De Vita E., Thomas D.L., Wheeler-Kingshott C.A., Balteau E., Carlstedt T., Choi D., Thompson A.J., Ciccarelli O. Metabolic changes in the spinal cord after brachial plexus root re-implantation. Neurorehabil. Neural Repair 2013, 27:118-124.
66. Kara B., Celik A., Karadereler S., Ulusoy L., Ganiyusufoglu K., Onat L., Mutlu A., Ornek I., Sirvanci M., Hamzaoglu A. The role of DTI in early detection of cervical spondylotic myelopathy: a preliminary study with 3-T MRI. Neuroradiology 2011, 53:609-616.
67. Kidd D., Thorpe J.W., Thompson A.J., Kendall B.E., Moseley I.F., MacManus D.G., McDonald W.I., Miller D.H. Spinal cord MRI using multi-array coils and fast spin echo. II. Findings in multiple sclerosis. Neurology 1993, 43:2632-2637.
68. Kim J.H., Loy D.N., Liang H.F., Trinkaus K., Schmidt R.E., Song S.K. Noninvasive diffusion tensor imaging of evolving white matter pathology in a mouse model of acute spinal cord injury. Magn. Reson. Med. 2007, 58:253-260.
69. Kong Y., Jenkinson M., Andersson J., Tracey I., Brooks J.C. Assessment of physiological noise modelling methods for functional imaging of the spinal cord. NeuroImage 2012, 60:1538-1549.
70. Kornelsen J., Stroman P.W. fMRI of the lumbar spinal cord during a lower limb motor task. Magn. Reson. Med. 2004, 52:411-414.
71. Kornelsen J., Stroman P.W. Detection of the neuronal activity occurring caudal to the site of spinal cord injury that is elicited during lower limb movement tasks. Spinal Cord 2007, 45:485-490.
72. Kozlowski P., Raj D., Liu J., Lam C., Yung A.C., Tetzlaff W. Characterizing white matter damage in rat spinal cord with quantitative MRI and histology. J. Neurotrauma 2008, 25:653-676.
73. Lammertse D., Dungan D., Dreisbach J., Falci S., Flanders A., Marino R., Schwartz E. Neuroimaging in traumatic spinal cord injury: an evidence-based review for clinical practice and research. J Spinal Cord Med. 2007, 30:205-214.
74. Laule C., Vavasour I.M., Zhao Y., Traboulsee A.L., Oger J., Vavasour J.D., MacKay A.L., Li D.K.B. Two year study of cervical cord volume and myelin water in primary progressive multiple sclerosis. Mult. Scler. 2010, 16:670-677.
75. Lawrence J., Stroman P.W., Bascaramurty S., Jordan L.M., Malisza K.L. Correlation of functional activation in the rat spinal cord with neuronal activation detected by immunohistochemistry. NeuroImage 2004, 22:1802-1807.
76. Lawrence J., Stroman P.W., Malisza K.L. Comparison of functional activity in the rat cervical spinal cord during alpha-chloralose and halothane anesthesia. NeuroImage 2007, 34:1665-1672.
77. Lawrence J.M., Stroman P.W., Kollias S.S. Functional magnetic resonance imaging of the human spinal cord during vibration stimulation of different dermatomes. Neuroradiology 2008, 50:273-280.
78. Leitch J., Cahill C.M., Ghazni N., Figley C.R., Stroman P.W. Spinal cord and brainstem activation in carpal tunnel syndrome patients in response to noxious stimuli: a spinal fMRI study. International Society for Magnetic Resonance in Medicine 17th Annual meeting, Honolulu, Hawaii, U.S.A., May 18-25 2009.
79. Leitch J.K., Figley C.R., Stroman P.W. Applying functional MRI to the spinal cord and brainstem. Magn. Reson. Imaging 2010, 28:1225-1233.
80. Lin X., Tench C.R., Evangelou N., Jaspan T., Constantinescu C.S. Measurement of spinal cord atrophy in multiple sclerosis. J. Neuroimaging 2004, 14:20S-26S.
81. Losseff N.A., Kingsley D.P., McDonald W.I., Miller D.H., Thompson A.J. Clinical and magnetic resonance imaging predictors of disability in primary and secondary progressive multiple sclerosis. Mult. Scler. 1996, 1:218-222.
82. Lundell H., Dyrby T., Ptito M., Nielsen J.B. Crossing fibers in lateral white matter of the cervical spinal cord detected with diffusion MRI in monkey postmortem. Proceedings of the 17th Annual Meeting of ISMRM, Honolulu, USA 2009, 1497.
83. Lundell H., Barthelemy D., Skimminge A., Dyrby T.B., Biering-Sorensen F., Nielsen J.B. Independent spinal cord atrophy measures correlate to motor and sensory deficits in individuals with spinal cord injury. Spinal Cord 2011, 49:70-75.
84. Lycklama G., Thompson A., Filippi M., Miller D., Polman C., Fazekas F., Barkhof F. Spinal-cord MRI in multiple sclerosis. Lancet Neurol. 2003, 2:555-562.
85. Mac Donald C.L., Dikranian K., Bayly P., Holtzman D., Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 2007, 27:11869-11876.
86. Maieron M., Iannetti G.D., Bodurka J., Tracey I., Bandettini P.A., Porro C.A. Functional responses in the human spinal cord during willed motor actions: evidence for side- and rate-dependent activity. J. Neurosci. 2007, 27:4182-4190.
87. Majcher K., Tomanek B., Jasinski A., Foniok T., Stroman P.W., Tuor U.I., Kirk D., Hess G. Simultaneous functional magnetic resonance imaging in the rat spinal cord and brain. Exp. Neurol. 2006, 197:458-464.
88. Majcher K., Tomanek B., Tuor U.I., Jasinski A., Foniok T., Rushforth D., Hess G. Functional magnetic resonance imaging within the rat spinal cord following peripheral nerve injury. NeuroImage 2007, 38:669-676.
89. Malisza K.L., Stroman P.W. Functional imaging of the rat cervical spinal cord. J. Magn. Reson. Imaging 2002, 16:553-558.
90. Malisza K.L., Gregorash L., Turner A., Foniok T., Stroman P.W., Allman A.A., Summers R., Wright A. Functional MRI involving painful stimulation of the ankle and the effect of physiotherapy joint mobilization. Magn. Reson. Imaging 2003, 21:489-496.
91. McMahon S.B., Koltzenburg M., Wall P.D. Wall and Melzack's Textbook of Pain 2006, Elsevier Churchill Livingstone, Edinburgh. 5th ed.
92. Nair G., Carew J.D., Usher S., Lu D., Hu X.P., Benatar M. Diffusion tensor imaging reveals regional differences in the cervical spinal cord in amyotrophic lateral sclerosis. NeuroImage 2010, 53:576-583.
93. Oh J., Saidha S., Chen M., Smith S.A., Prince J., Jones C., Diener-West M., van Zijl P.C., Reich D.S., Calabresi P.A. Spinal cord quantitative MRI discriminates between disability levels in multiple sclerosis. Neurology 2013, 80(6):540-547.
94. Oh J., Zackowski K., Chen M., Newsome S., Saidha S., Smith S.A., Diener-West M., Prince J., Jones C.K., Van Zijl P.C., Calabresi P.A., Reich D.S. Multiparametric MRI correlates of sensorimotor function in the spinal cord in multiple sclerosis. Mult. Scler. 2013, 19(4):427-435.
95. Ohgiya Y., Oka M., Hiwatashi A., Liu X., Kakimoto N., Westesson P.L., Ekholm S.E. Diffusion tensor MR imaging of the cervical spinal cord in patients with multiple sclerosis. Eur. Radiol. 2007, 17:2499-2504.
96. Ozanne A., Krings T., Facon D., Fillard P., Dumas J.L., Alvarez H., Ducreux D., Lasjaunias P. MR diffusion tensor imaging and fiber tracking in spinal cord arteriovenous malformations: a preliminary study. AJNR Am. J. Neuroradiol. 2007, 28(7):1271-1279.
97. Petersen J.A., Wilm B.J., von Meyenburg J., Schubert M., Seifert B., Najafi Y., Dietz V., Kollias S. Chronic cervical spinal cord injury: DTI correlates with clinical and electrophysiological measures. J. Neurotrauma 2012, 29:1556-1566.
98. Plank C., Koller A., Mueller-Mang C., Bammer R., Thurnher M.M. Diffusion-weighted MR imaging (DWI) in the evaluation of epidural spinal lesions. Neuroradiology 2007, 49(12):977-985.
99. Porro C.A., Cavazzuti M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog. Neurobiol. 1993, 41:565-607.
100. Porro C.A., Cavazzuti M., Galetti A., Sassatelli L., Barbieri G.C. Functional activity mapping of the rat spinal cord during formalin-induced noxious stimulation. Neuroscience 1991, 41:655-665.
101. Pradat P.F., Cohen-Adad J., El-Mendili M.M., Lehericy S., Blancho S., Meininger V., Rossignol S., Benali H. Diffusion and magnetization transfer imaging detects spinal cord lesions in amyotrophic lateral sclerosis. Proceedings of the 19th Annual Meeting of ISMRM, Montreal, Canada 2011, 2465.
102. Renoux J., Facon D., Fillard P., Huynh I., Lasjaunias P., Ducreux D. MR diffusion tensor imaging and fiber tracking in inflammatory diseases of the spinal cord. AJNR Am. J. Neuroradiol. 2006, 27:1947-1951.
103. Rocca M.A., Horsfield M.A., Sala S., Copetti M., Valsasina P., Mesaros S., Martinelli V., Caputo D., Stosic-Opincal T., Drulovic J., Comi G., Filippi M. A multicenter assessment of cervical cord atrophy among MS clinical phenotypes. Neurology 2011, 76:2096-2102.
104. Rocca M.A., Valsasina P., Damjanovic D., Horsfield M.A., Mesaros S., Stosic-Opincal T., Drulovic J., Filippi M. Voxel-wise mapping of cervical cord damage in multiple sclerosis patients with different clinical phenotypes. J. Neurol. Neurosurg. Psychiatry 2013, 84:35-41.
105. Saranathan M., Bayram E., Worters P.W., Glockner J.F. A 3D balanced-SSFP Dixon technique with group-encoded k-space segmentation for breath-held non-contrast-enhanced MR angiography. Magn. Reson. Imaging 2012, 30:158-164.
106. Sato T., Horikoshi T., Watanabe A., Uchida M., Ishigame K., Araki T., Kinouchi H. Evaluation of cervical myelopathy using apparent diffusion coefficient measured by diffusion-weighted imaging. AJNR Am. J. Neuroradiol. 2012, 33:388-392.
107. Schmierer K., Tozer D.J., Scaravilli F., Altmann D.R., Barker G.J., Tofts P.S., Miller D.H. Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J. Magn. Reson. Imaging 2007, 26:41-51.
108. Sen P.N., Basser P.J. A model for diffusion in white matter in the brain. Biophys. J. 2005, 89:2927-2938.
109. Shen H., Tang Y., Huang L., Yang R., Wu Y., Wang P., Shi Y., He X., Liu H., Ye J. Applications of diffusion-weighted MRI in thoracic spinal cord injury without radiographic abnormality. Int. Orthop. 2007, 31(3):375-383.
110. Smith S.A., Jones C.K., Gifford A., Belegu V., Chodkowski B., Farrell J.A., Landman B.A., Reich D.S., Calabresi P.A., McDonald J.W., van Zijl P.C. Reproducibility of tract-specific magnetization transfer and diffusion tensor imaging in the cervical spinal cord at 3 tesla. NMR Biomed. 2010, 23(2):207-217.
111. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 2002, 17:1429-1436.
112. Sprenger C., Eippert F., Finsterbusch J., Bingel U., Rose M., Buchel C. Attention modulates spinal cord responses to pain. Curr. Biol. 2012, 22:1019-1022.
113. Stroman P.W. Spinal fMRI investigation of human spinal cord function over a range of innocuous thermal sensory stimuli and study-related emotional influences. Magn. Reson. Imaging 2009, 27:1333-1346.
114. Stroman P.W., Cahill C.M. Functional magnetic resonance imaging of the human spinal cord and brainstem during heat stimulation. Proceedings of the International Society for Magnetic Resonance in Medicine 14th Annual Meeting, Seattle, USA, May 6-12, 2006 2006.
115. Stroman P.W., Ryner L.N. Functional MRI of motor and sensory activation in the human spinal cord. Magn. Reson. Imaging 2001, 19:27-32.
116. Stroman P.W., Nance P.W., Ryner L.N. BOLD MRI of the human cervical spinal cord at 3 tesla. Magn. Reson. Med. 1999, 42:571-576.
117. Stroman P.W., Krause V., Malisza K.L., Frankenstein U.N., Tomanek B. Characterization of contrast changes in functional MRI of the human spinal cord at 1.5T. Magn. Reson. Imaging 2001, 19:833-838.
118. Stroman P.W., Krause V., Malisza K.L., Frankenstein U.N., Tomanek B. Extravascular proton-density changes as a non-BOLD component of contrast in fMRI of the human spinal cord. Magn. Reson. Med. 2002, 48:122-127.
119. Stroman P.W., Krause V., Malisza K.L., Frankenstein U.N., Tomanek B. Functional magnetic resonance imaging of the human cervical spinal cord with stimulation of different sensory dermatomes. Magn. Reson. Imaging 2002, 20:1-6.
120. Stroman P.W., Tomanek B., Krause V., Frankenstein U.N., Malisza K.L. Mapping of neuronal function in the healthy and injured human spinal cord with spinal fMRI. NeuroImage 2002, 17:1854-1860.
121. Stroman P.W., Krause V., Malisza K.L., Kornelsen J., Bergman A., Lawrence J., Tomanek B. Spinal fMRI of Spinal Cord Injury in Human Subjects Proceedings of the International Society for Magnetic Resonance in Medicine 11th Annual Meeting, Toronto, Canada, July 10-16, 2005 2003, 13.
122. Stroman P.W., Kornelsen J., Bergman A., Krause V., Ethans K., Malisza K.L., Tomanek B. Noninvasive assessment of the injured human spinal cord by means of functional magnetic resonance imaging. Spinal Cord 2004, 42:59-66.
123. Stroman P.W., Kornelsen J., Lawrence J., Malisza K.L. A novel technique for spinal fMRI with large volume three-dimensional coverage of the spinal cord. Proceedings of the International Society for Magnetic Resonance in Medicine 12th Annual Meeting, Kyoto, Japan, May 15-21, 2004 2004, 2541.
124. Stroman P.W., Coe B.C., Munoz D.P. Influence of attention focus on neural activity in the human spinal cord during thermal sensory stimulation. Magn. Reson. Imaging 2011, 29:9-18.
125. Stroman P.W., Bosma R.L., Tsyben A. Somatotopic arrangement of thermal sensory regions in the healthy human spinal cord determined by means of spinal cord functional MRI. Magn. Reson. Med. 2012, 68(3):923-931.
126. Stroman P.W., Wheeler-Kingshott C., Bacon M., Schwab J.M., Bosma R., Brooks J., Cadotte D., Carlstedt T., Ciccarelli O., Cohen-Adad J., Curt A., Evangelou N., Fehlings M.G., Filippi M., Kelly B., Kollias S., Mackay A., Porro C.A., Smith S., Strittmatter S.M., Summers P., Tracey I. The current state-of-the-art of spinal cord imaging: methods. NeuroImage 2014, 84:1070-1081.
127. Summers P.E., Ferraro D., Duzzi D., Lui F., Iannetti G.D., Porro C.A. A quantitative comparison of BOLD fMRI responses to noxious and innocuous stimuli in the human spinal cord. NeuroImage 2010, 50:1408-1415.
128. Sun S.-W., Liang H.-F., Trinkaus K., Cross A.H., Armstrong R.C., Song S.-K. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 2006, 55:302-308.
129. Tator C.H., Fehlings M.G. Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J. Neurosurg. 1991, 75:15-26.
130. Thurnher M.M., Bammer R. Diffusion-weighted MR imaging (DWI) in spinal cord ischemia. Neuroradiology 2006, 48(11):795-801.
131. Tracey I., Ploghaus A., Gati J.S., Clare S., Smith S., Menon R.S., Matthews P.M. Imaging attentional modulation of pain in the periaqueductal gray in humans. J. Neurosci. Off. J. Soc. Neurosci. 2002, 22:2748-2752.
132. Tuch D.S. Q-ball imaging. Magn. Reson. Med. 2004, 52:1358-1372.
133. Uda T., Takami T., Tsuyuguchi N., Sakamoto S., Yamagata T., Ikeda H., Nagata T., Ohata K. Assessment of cervical spondylotic myelopathy using diffusion tensor magnetic resonance imaging parameter at 3.0tesla. Spine (Phila Pa 1976) 2013, 38:407-414.
134. Valsasina P., Rocca M.A., Agosta F., Benedetti B., Horsfield M.A., Gallo A., Rovaris M., Comi G., Filippi M. Mean diffusivity and fractional anisotropy histogram analysis of the cervical cord in MS patients. NeuroImage 2005, 26:822-828.
135. Valsasina P., Agosta F., Benedetti B., Caputo D., Perini M., Salvi F., Prelle A., Filippi M. Diffusion anisotropy of the cervical cord is strictly associated with disability in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 2007, 78:480-484.
136. Valsasina P., Agosta F., Absinta M., Sala S., Caputo D., Filippi M. Cervical cord functional MRI changes in relapse-onset MS patients. J. Neurol. Neurosurg. Psychiatry 2010, 81:405-408.
137. Valsasina P., Rocca M.A., Horsfield M.A., Absinta M., Messina R., Caputo D., Comi G., Filippi M. Regional cervical cord and disability in multiple sclerosis: a voxel-based analysis. Radiology 2013, 266:853-861.
138. van Eijsden P., Hyder F., Rothman D.L., Shulman R.G. Neurophysiology of functional imaging. NeuroImage 2009, 45:1047-1054.
139. Van Hecke W., Nagels G., Emonds G., Leemans A., Sijbers J., Van Goethem J., Parizel P. A diffusion tensor imaging group study of the spinal cord in multiple sclerosis patients with and without T(2) spinal cord lesions. J. Magn. Reson. Imaging 2009, 30:25-34.
140. Vedantam A., Jirjis M.B., Schmit B.D., Wang M.C., Ulmer J.L., Kurpad S.N. Characterization and limitations of diffusion tensor imaging metrics in the cervical spinal cord in neurologically intact subjects. J. Magn. Reson. Imaging 2013, (in press, Electronic publication ahead of print).
141. Wall P.D. Presynaptic control of impulses at the first central synapse in the cutaneous pathway. Prog. Brain Res. 1964, 12:92-118.
142. Watson C. The Spinal Cord: A Christopher and Dana Reeve Foundation Text and Atlas 2009, Academic, London.
143. Wheeler-Kingshott C., Cercignani M. About "axial" and "radial" diffusivities. Magn. Reson. Med. 2009, 61:1255-1260.
144. Wheeler-Kingshott C.A., Hickman S.J., Parker G.J., Ciccarelli O., Symms M.R., Miller D.H., Barker G.J. Investigating cervical spinal cord structure using axial diffusion tensor imaging. NeuroImage 2002, 16:93-102.
145. Wheeler-Kingshott C.A., Ciccarelli O., Schneider T., Alexander D.C., Cercignani M. A new approach to structural integrity assessment based on axial and radial diffusivities. Funct. Neurol. 2012, 27:85-90.
146. Wrigley P.J., Gustin S.M., Macey P.M., Nash P.G., Gandevia S.C., Macefield V.G., Siddall P.J., Henderson L.A. Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb. Cortex 2009, 19:224-232.
147. Xiangshui M., Xiangjun C., Xiaoming Z., Qingshi Z., Yi C., Chuanqiang Q., Xiangxing M., Chuanfu L., Jinwen H. 3T magnetic resonance diffusion tensor imaging and fibre tracking in cervical myelopathy. Clin. Radiol. 2010, 65:465-473.
148. Xie M., Tobin J.E., Budde M.D., Chen C.-I., Trinkaus K., Cross A.H., Mcdaniel D.P., Song S.-K., Armstrong R.C. Rostrocaudal analysis of corpus callosum demyelination and axon damage across disease stages refines diffusion tensor imaging correlations with pathological features. J. Neuropathol. Exp. Neurol. 2010, 69:704-716.
149. Xie G., Piche M., Khoshnejad M., Perlbarg V., Chen J.I., Hoge R.D., Benali H., Rossignol S., Rainville P., Cohen-Adad J. Reduction of physiological noise with independent component analysis improves the detection of nociceptive responses with fMRI of the human spinal cord. NeuroImage 2012, 63:245-252.
150. Zackowski K.M., Smith S.A., Reich D.S., Gordon-Lipkin E., Chodkowski B.A., Sambandan D.R., Shteyman M., Bastian A.J., van Zijl P.C., Calabresi P.A. Sensorimotor dysfunction in multiple sclerosis and column-specific magnetization transfer-imaging abnormalities in the spinal cord. Brain 2009, 132:1200-1209.
151. Zhang J., Jones M., DeBoy C.A., Reich D.S., Farrell J.A., Hoffman P.N., Griffin J.W., Sheikh K.A., Miller M.I., Mori S., Calabresi P.A. Diffusion tensor magnetic resonance imaging of Wallerian degeneration in rat spinal cord after dorsal root axotomy. J. Neurosci. 2009, 29:3160-3171.