Changes in Pain Processing in the Spinal Cord and Brainstem after Spinal Cord Injury Characterized by Functional Magnetic Resonance Imaging

Journal of Neurotrauma

Volumn 33, Issue 15, 2016, Pages 1450-1460

  Stroman, Patrick W ^a   Khan, Hamza S ^a   Bosma, Rachel L ^a   Cotoi, Andrea I ^a   Leung, Roxanne ^a   Cadotte, David W ^b   Fehlings, Michael G ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

brainstem; fMRI; injury; pain; spinal cord

Indexed keywords

ADULT; AGED; ARTICLE; BLOOD OXYGENATION; BOLD SIGNAL; BRAIN REGION; BRAIN STEM; CERVICAL SPINAL CORD INJURY; CLINICAL ARTICLE; DERMATOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPOTHALAMUS; IMAGE QUALITY; INJURY SEVERITY; MALE; NERVE CELL NETWORK; NERVE FUNCTION; NOCICEPTION; NOCICEPTIVE STIMULATION; NUCLEAR MAGNETIC RESONANCE SCANNER; PAIN ASSESSMENT; PERIAQUEDUCTAL GRAY MATTER; ROSTRAL VENTROMEDIAL MEDULLA; SIGNAL NOISE RATIO; SPINAL CORD; SPINAL CORD INJURY; STRUCTURAL EQUATION MODELING; THERMAL STIMULATION; THORACIC SPINE; COMPLICATION; COMPUTER ASSISTED DIAGNOSIS; DIAGNOSTIC IMAGING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; YOUNG ADULT;

ADULT; AGED; BRAIN STEM; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PAIN; SPINAL CORD INJURIES; YOUNG ADULT;

EID: 84980025178     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.4257     Document Type: Article

References (63)

1. Felix, E.R. (2014). Chronic neuropathic pain in SCI: evaluation and treatment. Physical medicine and rehabilitation clinics of North America 25, 545-571, viii.
2. Finnerup, N.B., Norrbrink, C., Trok, K., Piehl, F., Johannesen, I.L., Sorensen, J.C., Jensen, T.S., and Werhagen, L. (2014). Phenotypes and predictors of pain following traumatic spinal cord injury: a prospective study. J. Pain 15, 40-48.
3. Wrigley, P.J. and Siddall, P.J. (2013). Pain following spinal cord injury. In: Wall and Melzack's Textbook of Pain, 6th Edition. S.B. McMahon, M. Koltzenburg, I. Tracey, and D.C. Turk, (eds). Elsevier: Philadelphia, pps. 978-989.
4. Masri, R. and Keller, A. (2012). Chronic pain following spinal cord injury. Adv. Exp. Med. Biol. 760, 74-88.
5. Jensen, T.S. and Finnerup, N.B. (2014). Allodynia and hyperalgesia in neuropathic pain: clinical manifestations and mechanisms. Lancet Neurol. 13, 924-935.
6. Szczudlik, A., Dobrogowski, J., Wordliczek, J., Stepien, A., Krajnik, M., Leppert, W., Woron, J., Przeklasa-Muszynska, A., Kocot-Kepska, M., Zajaczkowska, R., Janecki, M., Adamczyk, A., and Malec-Milewska, M. (2014). Diagnosis and management of neuropathic pain: review of literature and recommendations of the Polish Association for the Study of Pain and the Polish Neurological Society - Part Two. Neurol. Neurochir. Pol. 48, 423-435.
7. Gwak, Y.S. and Hulsebosch, C.E. (2011). Neuronal hyperexcitability: a substrate for central neuropathic pain after spinal cord injury. Current pain and headache reports 15, 215-222.
8. Bedi, S.S., Yang, Q., Crook, R.J., Du, J., Wu, Z., Fishman, H.M., Grill, R.J., Carlton, S.M., and Walters, E.T. (2010). Chronic spontaneous activity generated in the somata of primary nociceptors is associated with pain-related behavior after spinal cord injury. J. Neurosci. 30, 14870-14882.
9. Carlton, S.M., Du, J., Tan, H.Y., Nesic, O., Hargett, G.L., Bopp, A.C., Yamani, A., Lin, Q., Willis, W.D., and Hulsebosch, C.E. (2009). Peripheral and central sensitization in remote spinal cord regions contribute to central neuropathic pain after spinal cord injury. Pain 147, 265-276.
10. Hains, B.C. and Waxman, S.G. (2006). Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. 26, 4308-4317.
11. Gwak, Y.S., Crown, E.D., Unabia, G.C., and Hulsebosch, C.E. (2008). Propentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat. Pain 138, 410-422.
12. Bryce, T.N., Biering-Sorensen, F., Finnerup, N.B., Cardenas, D.D., Defrin, R., Lundeberg, T., Norrbrink, C., Richards, J.S., Siddall, P., Stripling, T., Treede, R.D., Waxman, S.G., Widerstrom-Noga, E., Yezierski, R.P., and Dijkers, M. (2012). International spinal cord injury pain classification: part I. Background and description. March 6-7, 2009. Spinal Cord 50, 413-417.
13. Finnerup, N.B., Gyldensted, C., Nielsen, E., Kristensen, A.D., Bach, F.W., and Jensen, T.S. (2003). MRI in chronic spinal cord injury patients with and without central pain. Neurology 61, 1569-1575.
14. Baron, R., Forster, M., and Binder, A. (2012). Subgrouping of patients with neuropathic pain according to pain-related sensory abnormalities: a first step to a stratified treatment approach. Lancet Neurol. 11, 999-1005.
15. Attal, N., Fermanian, C., Fermanian, J., Lanteri-Minet, M., Alchaar, H., and Bouhassira, D. (2008). Neuropathic pain: are there distinct subtypes depending on the aetiology or anatomical lesion? Pain 138, 343-353.
16. Moulin, D., Boulanger, A., Clark, A.J., Clarke, H., Dao, T., Finley, G.A., Furlan, A., Gilron, I., Gordon, A., Morley-Forster, P.K., Sessle, B.J., Squire, P., Stinson, J., Taenzer, P., Velly, A., Ware, M.A., Weinberg, E.L., and Williamson, O.D. (2014). Pharmacological management of chronic neuropathic pain: Revised consensus statement from the Canadian Pain Society. Pain Res. Manag. 19, 328-335.
17. The Canadian Pain Coalition. (2010). The status of pain in Canada - Moving toward a Canadian Pain Strategy. In: Brief for the Parliamentary Committee on Palliative and Compassionate Care. The Canadian Pain Coalition: Ottawa.
18. Coghill, R.C., McHaffie, J.G., and Yen, Y.F. (2003). Neural correlates of interindividual differences in the subjective experience of pain. Proc. Natl. Acad. Sci. U. S. A. 100, 8538-8542.
19. Nielsen, C.S., Staud, R., and Price, D.D. (2009). Individual differences in pain sensitivity: measurement, causation, and consequences. J. Pain 10, 231-237.
20. Porro, C.A., Cettolo, V., Francescato, M.P., and Baraldi, P. (1998). Temporal and intensity coding of pain in human cortex. J. Neurophysiol. 80, 3312-3320.
21. Kucyi, A., Salomons, T.V., and Davis, K.D. (2013). Mind wandering away from pain dynamically engages antinociceptive and default mode brain networks. Proc. Natl. Acad. Sci. U. S. A. 110, 18692-18697.
22. Cahill, C.M. and Stroman, P.W. (2011). 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 29, 342-352.
23. Kucyi, A. and Davis, K.D. (2014). The dynamic pain connectome. Trends in neurosciences.
24. Bosma, R.L., Ameli Mojarad, E., Leung, L., Pukall, C., Staud, R., and Stroman, P.W. (2015). Neural correlates of temporal summation of second pain in the human brainstem and spinal cord. Hum. Brain Mapp. 36, 5038-5050.
25. Cadotte, D.W., Bosma, R., Mikulis, D., Nugaeva, N., Smith, K., Pokrupa, R., Islam, O., Stroman, P.W., and Fehlings, M.G. (2012). Plasticity of the injured human spinal cord: insights revealed by spinal cord functional MRI. PLoS One 7, e45560.
26. Dobek, C.E., Beynon, M.E., Bosma, R.L., and Stroman, P.W. (2014). Music modulation of pain perception and pain-related activity in the brain, brainstem, and spinal cord: an fMRI study. J. Pain 15, 1057-1068.
27. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T., and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150-157.
28. Davis, K.D. and Moayedi, M. (2013). Central mechanisms of pain revealed through functional and structural MRI. J. Neuroimmune Pharmacol. 8, 518-534.
29. Schweinhardt, P., Glynn, C., Brooks, J., McQuay, H., Jack, T., Chessell, I., Bountra, C., and Tracey, I. (2006). An fMRI study of cerebral processing of brush-evoked allodynia in neuropathic pain patients. Neuroimage 32, 256-265.
30. Becerra, L., Morris, S., Bazes, S., Gostic, R., Sherman, S., Gostic, J., Pendse, G., Moulton, E., Scrivani, S., Keith, D., Chizh, B., and Borsook, D. (2006). Trigeminal neuropathic pain alters responses in CNS circuits to mechanical (brush) and thermal (cold and heat) stimuli. J. Neurosci. 26, 10646-10657.
31. Staud, R. (2011). Brain imaging in fibromyalgia syndrome. Clin. Exp. Rheumatol. 29, S109-S117.
32. Bosma, R.L. and Stroman, P.W. (2015). Spinal cord response to stepwise and block presentation of thermal stimuli: a functional MRI study. J. Magn. Reson. Imaging 41, 1318-1325.
33. Staud, R., Craggs, J.G., Robinson, M.E., Perlstein, W.M., and Price, D.D. (2007). Brain activity related to temporal summation of C-fiber evoked pain. Pain 129, 130-142.
34. Khan, H.S. and Stroman, P.W. (2015). Inter-individual differences in pain processing investigated by functional magnetic resonance imaging of the brainstem and spinal cord. Neuroscience 307, 231-241.
35. American Spinal Injury Association Neurological Standards, C. (2000). International Standards for Neurological Classification of Spinal Cord Injury. Available at www.ncbi.nlm.nih.gov/pubmed/ 9160449
36. Vierck, C.J., Jr., Cannon, R.L., Fry, G., Maixner, W., and Whitsel, B.L. (1997). Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J. Neurophysiol. 78, 992-1002.
37. Staud, R. and Domingo, M. (2001). Evidence for abnormal pain processing in fibromyalgia syndrome. Pain Med. 2, 208-215.
38. Staud, R., Craggs, J.G., Perlstein, W.M., Robinson, M.E., and Price, D.D. (2008). Brain activity associated with slow temporal summation of C-fiber evoked pain in fibromyalgia patients and healthy controls. Eur. J. Pain 12, 1078-1089.
39. Bosma, R.L. and Stroman, P.W. (2014). Assessment of data acquisition parameters, and analysis techniques for noise reduction in spinal cord fMRI data. Magn. Reson. Imaging 32, 473-481.
40. Figley, C.R. and Stroman, P.W. (2009). Development and validation of retrospective spinal cord motion time-course estimates (RESPITE) for spin-echo spinal fMRI: Improved sensitivity and specificity by means of a motion-compensating general linear model analysis. Neuroimage 44, 421-427.
41. 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., Kelley, B.J., Kollias, S., Mackay, A., Porro, C.A., Smith, S., Strittmatter, S.M., Summers, P., and Tracey, I. (2014). The current state-of-the-art of spinal cord imaging: methods. Neuroimage 84, 1070-1081.
42. Myronenko, A. and Song, X.B. (2009). Image Registration by Minimization of Residual Complexity. Proc. Cvpr. IEEE, 49-56.
43. Myronenko, A. and Song, X.B. (2010). Intensity-based image registration by minimizing residual complexity. IEEE T Med. Imaging 29, 1882-1891.
44. Dobek, C.E., Beynon, M.E., Bosma, R.L., and Stroman, P.W. (2014). Music modulation of pain perception and pain-related activity in the brain, brain stem, and spinal cord: a functional magnetic resonance imaging study. J. Pain 15, 1057-1068.
45. Gray, H. (1995). Gray's Anatomy: the anatomical basis of medicine and surgery. In: Gray's Anatomy: The Anatomical Basis of Medicine and Surgery. P.L. Williams, M.M. Berry, P. Collins, M. Dyson, J.E. Dussek, and M.W.J. Ferguson (eds). Churchill Livingstone: London, pps. 975-1011.
46. Talairach, J. and Tournoux, P. (1988). Co-planar sterotaxic atlas of the human brain. Thieme Medical Publishers Inc: New York.
47. Naidich, T.P., Delman, B.N., Sorensen, A.G., Kollias, S.S., and Haacke, E.M. (2009). Internal architecture of the brain stem with key axial sections. In: Duvernoy's Atlas of the Human Brain Stem and Cerebellum. Springer-Verlag/Wien: New York, pps. 79-82.
48. McArdle, J.J. and McDonald, R.P. (1984). Some algebraic properties of the Reticular Action Model for moment structures. Br. J. Math. Stat. Psychol. 37 ( Pt 2), 234-251.
49. Craggs, J.G., Staud, R., Robinson, M.E., Perlstein, W.M., and Price, D.D. (2012). Effective connectivity among brain regions associated with slow temporal summation of C-fiber-evoked pain in fibromyalgia patients and healthy controls. J. Pain 13, 390-400.
50. Bollen, K.A. (1989). Structural Equations with Latent Variables. Wiley: New York.
51. Schlosser, R., Gesierich, T., Kaufmann, B., Vucurevic, G., Hunsche, S., Gawehn, J., and Stoeter, P. (2003). Altered effective connectivity during working memory performance in schizophrenia: a study with fMRI and structural equation modeling. Neuroimage 19, 751-763.
52. Millan, M.J. (2002). Descending control of pain. Prog. Neurobiol. 66, 355-474.
53. Mole, T.B., MacIver, K., Sluming, V., Ridgway, G.R., and Nurmikko, T.J. (2014). Specific brain morphometric changes in spinal cord injury with and without neuropathic pain. NeuroImage. Clin. 5, 28-35.
54. Freund, P., Weiskopf, N., Ward, N.S., Hutton, C., Gall, A., Ciccarelli, O., Craggs, M., Friston, K., and Thompson, A.J. (2011). Disability, atrophy and cortical reorganization following spinal cord injury. Brain 134, 1610-1622.
55. Wrigley, P.J., Gustin, S.M., Macey, P.M., Nash, P.G., Gandevia, S.C., Macefield, V.G., Siddall, P.J., and Henderson, L.A. (2009). Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb. Cortex 19, 224-232.
56. Jutzeler, C.R., Freund, P., Huber, E., Curt, A., and Kramer, J.L. (2015). Neuropathic pain and functional reorganization in the primary sensorimotor cortex after spinal cord injury. J. Pain 16, 1256-1267.
57. Wrigley, P.J., Press, S.R., Gustin, S.M., Macefield, V.G., Gandevia, S.C., Cousins, M.J., Middleton, J.W., Henderson, L.A., and Siddall, P.J. (2009). Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. Pain 141, 52-59.
58. Peyron, R., Schneider, F., Faillenot, I., Convers, P., Barral, F.G., Garcia-Larrea, L., and Laurent, B. (2004). An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain. Neurology 63, 1838-1846.
59. Jurkiewicz, M.T., Mikulis, D.J., Fehlings, M.G., and Verrier, M.C. (2010). Sensorimotor cortical activation in patients with cervical spinal cord injury with persisting paralysis. Neurorehabil. Neural Repair 24, 136-140.
60. Curt, A., Alkadhi, H., Crelier, G.R., Boendermaker, S.H., Hepp-Reymond, M.C., and Kollias, S.S. (2002). Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain 125, 2567-2578.
61. Gustin, S.M., Wrigley, P.J., Siddall, P.J., and Henderson, L.A. (2010). Brain anatomy changes associated with persistent neuropathic pain following spinal cord injury. Cereb. Cortex 20, 1409-1419.
62. Henderson, L.A., Gustin, S.M., Macey, P.M., Wrigley, P.J., and Siddall, P.J. (2011). Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy. J. Neurosci. 31, 2630-2637.
63. Flor, H., Nikolajsen, L., and Staehelin Jensen, T. (2006). Phantom limb pain: a case of maladaptive CNS plasticity? Nat. Rev. Neuroscience 7, 873-881.