PAIN
Volume 138, Issue 2 , Pages 292-300 , 31 August 2008

Functional MRI of the brain detects neuropathic pain in experimental spinal cord injury

  • Toshiki Endo

      Affiliations

    • Department of Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden
    • Department of Neurosurgery, School of Medicine, Tohoku University, Sendai 980-8574, Japan
    • Corresponding Author InformationCorresponding author. Address: Department of Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden. Tel.: +46 8 524 87062; fax: +46 8 323 742.
  • ,
  • Christian Spenger

      Affiliations

    • Department of Clinical Science, Intervention and Technology, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden
  • ,
  • Jingxia Hao

      Affiliations

    • Section of Clinical Neurophysiology, Department of Clinical Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden
  • ,
  • Teiji Tominaga

      Affiliations

    • Department of Neurosurgery, School of Medicine, Tohoku University, Sendai 980-8574, Japan
  • ,
  • Zsuzsanna Wiesenfeld-Hallin

      Affiliations

    • Section of Clinical Neurophysiology, Department of Clinical Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden
  • ,
  • Lars Olson

      Affiliations

    • Department of Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden
  • ,
  • Xiao-Jun Xu

      Affiliations

    • Section of Clinical Neurophysiology, Department of Clinical Neuroscience, Karolinska Institutet, Retzius vag 8, B2:4, Stockholm 171 77, Sweden

Received 30 June 2007 ,Revised 21 December 2007 ,Accepted 21 December 2007.

References 

  1. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain. 2005;9:463–484
  2. Bushnell MC, Duncan GH, Hofbauer RK, Ha B, Chen JI, Carrier B. Pain perception: is there a role for primary somatosensory cortex?. Proc Natl Acad Sci USA. 1999;96:7705–7709
  3. Chang C, Shyu BC. A fMRI study of brain activations during non-noxious and noxious electrical stimulation of the sciatic nerve of rats. Brain Res. 2001;897:71–81
  4. Coghill RC, Sang CN, Maisog JM, Iadarola MJ. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol. 1999;82:1934–1943
  5. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. 2002;3:655–666
  6. Curt A, Alkadhi H, Crelier GR, Boendermaker SH, Hepp-Reymond MC, Kollias SS. Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain. 2002;125:2567–2578
  7. Drew GM, Siddall PJ, Duggan AW. Responses of spinal neurones to cutaneous and dorsal root stimuli in rats with mechanical allodynia after contusive spinal cord injury. Brain Res. 2001;893:59–69
  8. Gauriau C, Bernard JF. Posterior triangular thalamic neurons convey nociceptive messages to the secondary somatosensory and insular cortices in the rat. J Neurosci. 2004;24:752–761
  9. Hao JX, Yu W, Xu XJ, Wiesenfeld-Hallin Z. Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. Brain Res. 1996;722:177–180
  10. Hao JX, Yu W, Xu XJ. Evidence that spinal endogenous opioidergic systems control the expression of chronic pain-related behaviors in spinally injured rats. Exp Brain Res. 1998;118:259–268
  11. Hao JX, Kupers RC, Xu XJ. Response characteristics of spinal cord dorsal horn neurons in chronic allodynic rats after spinal cord injury. J Neurophysiol. 2004;92:1391–1399
  12. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32:77–88
  13. Hess A, Sergejeva M, Budinsky L, Zeilhofer HU, Brune K. Imaging of hyperalgesia in rats by functional MRI. Eur J Pain. 2007;11:109–119
  14. Hofstetter CP, Schweinhardt P, Klason T, Olson L, Spenger C. Numb rats walk – a behavioural and fMRI comparison of mild and moderate spinal cord injury. Eur J Neurosci. 2003;18:3061–3068
  15. Hoheisel U, Scheifer C, Trudrung P, Unger T, Mense S. Pathophysiological activity in rat dorsal horn neurones in segments rostral to a chronic spinal cord injury. Brain Res. 2003;974:134–145
  16. Johansen JP, Fields HL, Manning BH. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA. 2001;98:8077–8082
  17. Lilja J, Endo T, Hofstetter C, Westman E, Young J, Olson L, et al. Blood oxygenation level-dependent visualization of synaptic relay stations of sensory pathways along the neuroaxis in response to graded sensory stimulation of a limb. J Neurosci. 2006;26:6330–6336
  18. Lowe AS, Beech JS, Williams SC. Small animal, whole brain fMRI: innocuous and nociceptive forepaw stimulation. Neuroimage. 2007;35:719–728
  19. Luttinger D. Determination of antinociceptive efficacy of drugs in mice using different water temperatures in a tail-immersion test. J Pharmacol Methods. 1985;13:351–357
  20. Malisza KL, Docherty JC. Capsaicin as a source for painful stimulation in functional MRI. J Magn Reson Imaging. 2001;14:341–347
  21. Moylan Governo RJ, Morris PG, William Prior MJ, Marsden CA, Chapman V. Capsaicin-evoked brain activation and central sensitization in anaesthetised rats: a functional magnetic resonance imaging study. Pain. 2006;126:35–45
  22. Paxinos G, Watson C. The rat brain in stereotaxic coordinates, the new coronal set. New York: Academic Press; 2005;
  23. Petrovic P, Ingvar M, Stone-Elander S, Petersson KM, Hansson P. A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy. Pain. 1999;83:459–470
  24. Peyron R, Garcia-Larrea L, Gregoire MC, Convers P, Lavenne F, Veyre L, et al. Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. Brain. 1998;121:345–356
  25. Peyron R, Laurent B, Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol Clin. 2000;30:263–288
  26. Peyron R, Schneider F, Faillenot I, Convers P, Barral FG, Garcia-Larrea L, et al. An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain. Neurology. 2004;63:1838–1846
  27. Randall LO, Selitto JJ. A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodyn Ther. 1957;111:409–419
  28. Schweinhardt P, Fransson P, Olson L, Spenger C, Andersson JL. A template for spatial normalisation of MR images of the rat brain. J Neurosci Methods. 2003;129:105–113
  29. Schweinhardt P, Glynn C, Brooks J, McQuay H, Jack T, Chessell I, et al. An fMRI study of cerebral processing of brush-evoked allodynia in neuropathic pain patients. Neuroimage. 2006;32:256–265
  30. Siddall PJ, Yezierski RP, Loser DJ. Taxonomy and epidemiology of spinal cord injury pain. In:  Yezierski RP,  Burchiel K editor. Spinal cord injury pain: assessment, mechanisms, management. Seattle, WA: IASP Press; 2002;p. 9–24
  31. Spenger C, Josephson A, Klason T, Hoehn M, Schwindt W, Ingvar M, et al. Functional MRI at 4.7 tesla of the rat brain during electric stimulation of forepaw, hindpaw, or tail in single- and multislice experiments. Exp Neurol. 2000;166:246–253
  32. Takahashi Y, Nakajima Y. Dermatomes in the rat limbs as determined by antidromic stimulation of sensory C-fibers in spinal nerves. Pain. 1996;67:197–202
  33. Treede RD, Kenshalo DR, Gracely RH, Jones AK. The cortical representation of pain. Pain. 1999;79:105–111
  34. Tuor UI, Malisza K, Foniok T, Papadimitropoulos R, Jarmasz M, Somorjai R, et al. Functional magnetic resonance imaging in rats subjected to intense electrical and noxious chemical stimulation of the forepaw. Pain. 2000;87:315–324
  35. Vogt BA. Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci. 2005;6:533–544
  36. Waxman SG, Hains BC. Fire and phantoms after spinal cord injury: Na+ channels and central pain. Trends Neurosci. 2006;29:207–215
  37. Xu XJ, Hao JX, Aldskogius H, Seiger A, Wiesenfeld-Hallin Z. Chronic pain-related syndrome in rats after ischemic spinal cord lesion: a possible animal model for pain in patients with spinal cord injury. Pain. 1992;48:279–290
  38. Xu XJ, Hao JX, Seiger A, Hughes J, Hokfelt T, Wiesenfeld-Hallin Z. Chronic pain-related behaviors in spinally injured rats: evidence for functional alterations of the endogenous cholecystokinin and opioid systems. Pain. 1994;56:271–277
  39. Xu XJ, Hao JX, Wiesenfeld-Hallin Z. Physiological and pharmacological characterization of a rat model of spinal cord injury pain after spinal ischemia. In:  Yezierski RP,  Burchiel K editor. Spinal cord injury pain: assessment, mechanisms, management. Seattle, WA: IASP Press; 2002;p. 175–188

PII: S0304-3959(08)00002-X

doi: 10.1016/j.pain.2007.12.017

PAIN
Volume 138, Issue 2 , Pages 292-300 , 31 August 2008