PAIN
Volume 148, Issue 3 , Pages 375-386 , March 2010

Using perfusion MRI to measure the dynamic changes in neural activation associated with tonic muscular pain

  • Daron G. Owen

      Affiliations

    • Lawson Health Research Institute, St. Joseph’s Health Care London, 268 Grosvenor St., London, Ontario, Canada N6A 4V2
    • Department of Medical Biophysics, The University of Western Ontario, London, Ontario, Canada
    • Corresponding Author InformationCorresponding author. Address: Lawson Health Research Institute, St. Joseph’s Health Care London, 268 Grosvenor St., London, Ontario, Canada N6A 4V2. Tel.: +1 519 646 6100x65732; fax: +1 519 646 6399.
    • ,
  • Collin F. Clarke

      Affiliations

    • Department of Anesthesia and Perioperative Medicine, The University of Western Ontario, London, Ontario, Canada
    • ,
  • Sugantha Ganapathy

      Affiliations

    • Department of Anesthesia and Perioperative Medicine, The University of Western Ontario, London, Ontario, Canada
    • ,
  • Frank S. Prato

      Affiliations

    • Lawson Health Research Institute, St. Joseph’s Health Care London, 268 Grosvenor St., London, Ontario, Canada N6A 4V2
    • Department of Medical Biophysics, The University of Western Ontario, London, Ontario, Canada
    • ,
  • Keith S. St. Lawrence

      Affiliations

    • Lawson Health Research Institute, St. Joseph’s Health Care London, 268 Grosvenor St., London, Ontario, Canada N6A 4V2
    • Department of Medical Biophysics, The University of Western Ontario, London, Ontario, Canada
    • Robarts Research Institute, London, Ontario, Canada

Received 7 November 2008 ,Revised 12 August 2009 ,Accepted 5 October 2009.

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. Bencherif B, Fuchs PN, Sheth R, Dannals RF, Campbell JN, Frost JJ. Pain activation of human supraspinal opioid pathways as demonstrated by [11C]-carfentanil and positron emission tomography (PET). Pain. 2002;99:589–598
  3. Berman S, Munakata J, Naliboff BD, Chang L, Mandelkern M, Silverman D, et al. Gender differences in regional brain response to visceral pressure in IBS patients. Eur J Pain. 2000;4:157–172
  4. Brett M, Johnsrude IS, Owen AM. The problem of functional localization in the human brain. Nat Rev Neurosci. 2002;3:243–249
  5. Brooks JC, Nurmikko TJ, Bimson WE, Singh KD, Roberts N. FMRI of thermal pain: effects of stimulus laterality and attention. NeuroImage. 2002;15:293–301
  6. Capra NF, Ro JY. Human and animal experimental models of acute and chronic muscle pain: intramuscular algesic injection. Pain. 2004;110:3–7
  7. Casanova R, Srikanth R, Baer A, Laurienti PJ, Burdette JH, Hayasaka S, et al. Biological parametric mapping: a statistical toolbox for multimodality brain image analysis. NeuroImage. 2007;34:137–143
  8. 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
  9. Craig AD. A new view of pain as a homeostatic emotion. Trends Neurosci. 2003;26:303–307
  10. Craig AD, Chen K, Bandy D, Reiman EM. Thermosensory activation of insular cortex. Nat Neurosci. 2000;3:184–190
  11. Craig KD. Emotions and psychobiology. In:  McMahon S,  Wall PD,  Koltzenburg M,  Melzack R editor. Melzack and Wall’s textbook of pain. Churchill Livingstone: Elsevier; 2005;
  12. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nat Neurosci. 2004;7:189–195
  13. de Leeuw R, Albuquerque R, Okeson J, Carlson C. The contribution of neuroimaging techniques to the understanding of supraspinal pain circuits: implications for orofacial pain. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100:308–314
  14. de Zwart JA, van Gelderen P, Kellman P, Duyn JH. Application of sensitivity-encoded echo-planar imaging for blood oxygen level-dependent functional brain imaging. Magn Reson Med. 2002;48:1011–1020
  15. Derbyshire SW, Jones AK. Cerebral responses to a continual tonic pain stimulus measured using positron emission tomography. Pain. 1998;76:127–135
  16. Detre JA, Floyd TF. Functional MRI and its applications to the clinical neurosciences. Neuroscientist. 2001;7:64–79
  17. Dunckley P, Wise RG, Aziz Q, Painter D, Brooks J, Tracey I, et al. Cortical processing of visceral and somatic stimulation: differentiating pain intensity from unpleasantness. Neuroscience. 2005;133:533–542
  18. Duyn JH, van Gelderen P, Talagala L, Koretsky A, de Zwart JA. Technological advances in MRI measurement of brain perfusion. J Magn Reson Imaging. 2005;22:751–753
  19. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage. 2005;25:1325–1335
  20. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995;33:636–647
  21. Garraux G, Hallett M, Talagala SL. CASL fMRI of subcortico-cortical perfusion changes during memory-guided finger sequences. NeuroImage. 2005;25:122–132
  22. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage. 2002;15:870–878
  23. Glantz SA, Slinker BK. Primer of applied regression and analysis of variance. New York: McGraw-Hill, Medical Pub. Division; 2001.
  24. Gracely RH, Geisser ME, Giesecke T, Grant MA, Petzke F, Williams DA, et al. Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain. 2004;127:835–843
  25. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, et al. Studying sex and gender differences in pain and analgesia: a consensus report. Pain. 2007;132:S26–S45
  26. Henderson LA, Bandler R, Gandevia SC, Macefield VG. Distinct forebrain activity patterns during deep versus superficial pain. Pain. 2006;120:286–296
  27. Henderson LA, Gandevia SC, Macefield VG. Somatotopic organization of the processing of muscle and cutaneous pain in the left and right insula cortex: a single-trial fMRI study. Pain. 2007;128:20–30
  28. Hernandez-Garcia L, Lee GR, Vazquez AL, Noll DC. Fast, pseudo-continuous arterial spin labeling for functional imaging using a two-coil system. Magn Reson Med. 2004;51:577–585
  29. Kastrup A, Baudewig J, Schnaudigel S, Huonker R, Becker L, Sohns JM, et al. Behavioral correlates of negative BOLD signal changes in the primary somatosensory cortex. NeuroImage. 2008;41:1364–1371
  30. Kong J, White NS, Kwong KK, Vangel MG, Rosman IS, Gracely RH, et al. Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum Brain Mapp. 2006;27:715–721
  31. Lui F, Duzzi D, Corradini M, Serafini M, Baraldi P, Porro CA. Touch or pain? Spatio-temporal patterns of cortical fMRI activity following brief mechanical stimuli. Pain. 2008;138:362–374
  32. Macefield VG, Gandevia SC, Henderson LA. Discrete changes in cortical activation during experimentally induced referred muscle pain: a single-trial fMRI study. Cereb Cortex. 2007;17:2050–2059
  33. Moulton EA, Keaser ML, Gullapalli RP, Greenspan JD. Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat. J Neurophysiol. 2005;93:2183–2193
  34. Owen DG, Bureau Y, Thomas AW, Prato FS, St Lawrence KS. Quantification of pain-induced changes in cerebral blood flow by perfusion MRI. Pain. 2008;136:85–96
  35. Penny WD, Holmes AP, Friston KJ. Random effects analysis. In:  Frackowiak RSJ,  Friston KJ,  Frith C,  Dolan R,  Price CJ,  Zeki S,  Ashburner J,  Penny WD editor. Human brain function. London: Academic Press; 2003;
  36. Petrovic P, Kalso E, Petersson KM, Ingvar M. Placebo and opioid analgesia – imaging a shared neuronal network. Science. 2002;295:1737–1740
  37. Petrovic P, Petersson KM, Hansson P, Ingvar M. Brainstem involvement in the initial response to pain. NeuroImage. 2004;22:995–1005
  38. 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
  39. Price DD. Psychological mechanisms of pain and analgesia. Seattle: IASP Press; 1999;
  40. Price DD. Psychological and neural mechanisms of the affective dimension of pain. Science. 2000;288:1769–1772
  41. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci USA. 2001;98:676–682
  42. Schreckenberger M, Siessmeier T, Viertmann A, Landvogt C, Buchholz HG, Rolke R, et al. The unpleasantness of tonic pain is encoded by the insular cortex. Neurology. 2005;64:1175–1183
  43. 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
  44. Seymour B, O’Doherty JP, Dayan P, Koltzenburg M, Jones AK, Dolan RJ, et al. Temporal difference models describe higher-order learning in humans. Nature. 2004;429:664–667
  45. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science. 2004;303:1157–1162
  46. Sprenger T, Valet M, Boecker H, Henriksen G, Spilker ME, Willoch F, et al. Opioidergic activation in the medial pain system after heat pain. Pain. 2006;122:63–67
  47. St Lawrence KS, Frank JA, Bandettini PA, Ye FQ. Noise reduction in multi-slice arterial spin tagging imaging. Magn Reson Med. 2005;53:735–738
  48. St Lawrence KS, Ye FQ, Lewis BK, Frank JA, McLaughlin AC. Measuring the effects of indomethacin on changes in cerebral oxidative metabolism and cerebral blood flow during sensorimotor activation. Magn Reson Med. 2003;50:99–106
  49. Stohler CS, Kowalski CJ. Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain. 1999;79:165–173
  50. Strigo IA, Duncan GH, Boivin M, Bushnell MC. Differentiation of visceral and cutaneous pain in the human brain. J Neurophysiol. 2003;89:3294–3303
  51. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL. Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol. 1997;78:450–460
  52. Thunberg J, Lyskov E, Korotkov A, Ljubisavljevic M, Pakhomov S, Katayeva G, et al. Brain processing of tonic muscle pain induced by infusion of hypertonic saline. Eur J Pain. 2005;9:185–194
  53. van Oudenhove L, Vandenberghe J, Dupont P, Geeraerts B, Vos R, Bormans G, et al. Cortical deactivations during gastric fundus distension in health: visceral pain-specific response or attenuation of ‘default mode’ brain function? A H2 15O-PET study. Neurogastroenterol Motil. 2009;21:259–271
  54. Vogt BA, Berger GR, Derbyshire SW. Structural and functional dichotomy of human midcingulate cortex. Eur J Neurosci. 2003;18:3134–3144
  55. Wang J, Aguirre GK, Kimberg DY, Roc AC, Li L, Detre JA. Arterial spin labeling perfusion fMRI with very low task frequency. Magn Reson Med. 2003;49:796–802
  56. Wong EC, Buxton RB, Frank LR. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn Reson Med. 1998;39:702–708
  57. Yang Y, Glover GH, van Gelderen P, Mattay VS, Santha AK, Sexton RH, et al. Fast 3D functional magnetic resonance imaging at 1. 5T with spiral acquisition. Magn Reson Med. 1996;36:620–626
  58. Ye FQ, Frank JA, Weinberger DR, McLaughlin AC. Noise reduction in 3D perfusion imaging by attenuating the static signal in arterial spin tagging (ASSIST). Magn Reson Med. 2000;44:92–100
  59. Ye FQ, Smith AM, Yang Y, Duyn J, Mattay VS, Ruttimann UE, et al. Quantitation of regional cerebral blood flow increases during motor activation: a steady-state arterial spin tagging study. NeuroImage. 1997;6:104–112
  60. Zubieta JK, Smith YR, Bueller JA, Xu Y, Kilbourn MR, Jewett DM, et al. Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science. 2001;293:311–315

PII: S0304-3959(09)00576-4

doi: 10.1016/j.pain.2009.10.003

PAIN
Volume 148, Issue 3 , Pages 375-386 , March 2010

Article Tools

* Image Usage & Resolution