An fMRI study of cerebral processing of brush-evoked allodynia in neuropathic pain patients

NeuroImage

Volumn 32, Issue 1, 2006, Pages 256-265

  Schweinhardt, Petra ^a   Glynn, Chris ^b   Brooks, Jonathan ^a   McQuay, Henry ^b   Jack, Tim ^b   Chessell, Iain ^c   Bountra, Chas ^c   Tracey, Irene ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CHURCHILL HOSPITAL   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Anterior insula; Dynamic mechanical allodynia; Fmri; Neuropathic pain; Pain encoding

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; EVOKED SOMATOSENSORY RESPONSE; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; MALE; MIDDLE AGED; NEURALGIA; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; REFERENCE VALUE; TOUCH;

ADULT; AGED; BRAIN MAPPING; CEREBRAL CORTEX; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURALGIA; PAIN; PAIN MEASUREMENT; REFERENCE VALUES; TOUCH;

EID: 33748651043     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2006.03.024     Document Type: Article

References (61)

1. Apkarian, A.V., Bushnell, M.C., Treede, R.D., Zubieta, J.K., 2005. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9 (4), 463- 484.
2. Augustine, J.R., 1996. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Brain Res. Rev. 22 (3), 229- 244.
3. Baron, R., Baron, Y., Disbrow, E., Roberts, T.P., 1999. Brain processing of capsaicin-induced secondary hyper algesia: a functional MRI study. Neurology 53 (3), 548- 557.
4. Beck, A.T., Ward, C.H., Mendelson, M., Mock, J., Erbaugh, J., 1961. An inventory for measuring depression. Arch. Gen. Psychiatry 4, 561-571.
5. Bornhovd, K., Quante, M., Glauche, V., Bromm, B.,Weiller, C., Buchel, C., 2002. Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain 125 (Pt 6), 1326-1336.
6. Bouhassira, D., Attal, N., Fermanian, J., Alchaar, H., Gautron, M., Masquelier, E., Rostaing, S., Lanter i-Minet, M., Collin, E., Grisart, J.,Boureau, F., 2004. Development and validation of the neuropathic pain symptom inventory. Pain 108 (3), 248- 257.
7. Brooks, J.C., Nurmikko, T.J., Bimson, W.E., Singh, K.D., Roberts, N., 2002. fMRI of thermal pain: effects of stimulus laterality and attention. NeuroImage 15 (2), 293- 301.
8. Brooks, J.C., Zambreanu, L., Godinez, A., Craig, A.D., Tracey, I., 2005. Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. NeuroImage 27 (1), 201-209.
9. Buchel, C., Bornhovd, K., Quante, M., Glau che, V., Bromm, B., Weiller, C., 2002. Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: aparametric single-trial laser functional magnetic resonance imaging study. J. Neurosci. 22 (3), 970- 976.
10. Burton, H., Abend, N.S., MacLeod, A.M., Sinclair, R.J., Snyder, A.Z., Raichle, M.E., 1999. Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. Cereb. Cortex 9 (7), 662-674.
11. Bushnell, M.C., Duncan, G.H., Hofbauer, R.K., Ha, B., Chen, J.I., Carrier, B., 1999. Pain perception: is there a role for primary somatosensory cortex. Proc. Natl. Acad. Sci. U. S. A. 96 (14), 7705-7709.
12. Coghill, R.C., Sang, C.N., Maisog, J.M., Iadarola, M.J., 1999. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J. Neurophysiol. 82 (4), 1934- 1943.
13. Craig, A.D., 1995. Supraspinal projections of lamina I neurons. In: Besson, J.-M., Ollat, H. (Eds.), For brain areas involved in pain processing. John Libbey, Eurotext, Montrouge, pp. 13- 26.
14. Craig, A.D., 2002. How do you feel Interoception: the sense of the physiological condition of the body. Nat. Rev., Neurosci. 3 (8), 655- 666.
15. Craig, A.D., 2003. Pain mechanisms: labeled lines versus convergence in central processing. Annu. Rev. Neurosci. 26, 1- 30.
16. Craig, A.D., Chen, K., Bandy, D., Reiman, E.M., 2000. Thermosensory activation of insular cortex. Nat. Neurosci. 3 (2), 184- 190.
17. Derbyshire, S.W., Jones, A.K., Gyulai, F., Clark, S., Townsend, D., Firestone, L.L., 1997. Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73 (3), 431- 445.
18. Devinsky, O., Morrell, M.J., Vogt, B.A., 1995. Contributions of anterior cingulate cortex to behaviour. Brain 1 (118), 279- 306.
19. Dworkin, R.H., Backonja, M., Rowbotham, M.C., Allen, R.R., Argoff, C.R., Bennett, G.J., Bushnell, M.C., Farrar, J.T., Galer, B.S., Haythornthwaite, J.A., Hewitt, D.J., Loeser, J.D., Max, M.B., Saltarelli, M., Schmader, K.E., Stein, C., Thompson, D., Turk, D.C., Wallace, M.S., Watkins, L.R., Weinstein, S.M., 2003. Advances in neuropathic pain: diagnosis, mechanisms, and treatment recommendations. Arch. Neurol. 60 (11), 1524- 1534.
20. Evans, A.C., Marrett, S., Neelin, P., Collins, L., Worsley, K., Dai, W., Milot, S., Meyer, E., Bub, D., 1992. Anatomical mapping of functional activation in stereotactic coordinate space. NeuroImage 1 (1), 43- 53.
21. Evans, K.C., Banzett, R.B., Adams, L., McKay, L., Frackowiak, R.S., Corfield, D.R., 2002. BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. J. Neurophysiol. 88 (3), 1500- 1511.
22. Hsieh, J.C., Belfrage, M., Stone-Elander, S., Hansson, P., Ingvar, M., 1995. Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. Pain 63 (2), 225- 236.
23. Hsieh, J.C., Hannerz, J., Ingvar, M., 1996. Right-lateralised central processing for pain of nitroglycerin-induced cluster headache. Pain 67 (1), 59- 68.
24. Iadarola, M.J., Berman, K.F., Zeffiro, T.A., Byas-Smith, M.G., Gracely, R.H., Max, M.B., Bennett, G.J., 1998. Neural activation during acute capsaicin-evoked pain and allodynia assessed with PET. Brain 121 (5), 931- 947.
25. Iannetti, G.D., Zambreanu, L., Cruccu, G., Tracey, I., 2005. Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131 (1), 199-208.
26. Jenkinson, M., Smith, S., 2001. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5 (2), 143- 156.
27. Johansen-Berg, H., Christensen, V., Woolrich, M., Matthews, P.M., 2000. Attention to touch modulates activity in both primary and secondary somatosensory areas. NeuroReport 11 (6), 1237- 1241.
28. LaBar, K.S., Gitelman, D.R., Parrish, T.B., Kim, Y.H., Nobre, A.C., Mesulam, M.M., 2001. Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav. Neurol. Sci. 115 (2), 493- 500.
29. Lorenz, J., Kohlhoff, H., Hansen, H.C., Kunze, K., Bromm, B., 1998. Abeta-fiber mediated activation of cingulate cortex as correlate of central post-stroke pain. NeuroReport 9 (4), 659-663.
30. Lorenz, J., Cross, D., Minoshima, S., Morrow, T., Paulson, P., Casey, K., 2002. A unique representation of heat allodynia in the human brain. Neuron 35 (2), 383- 393.
31. Maihofner, C., Handwerker, H.O., 2005. Differential coding of hyperalgesia in the human brain: a functional MRI study. NeuroImage 28 (4), 996- 1006.
32. Maihofner, C., Neundorfer, B., Stefan, H., Handwerker, H.O., 2003. Cortical processing of brush-evoked allodynia. NeuroReport 14 (6), 785-789.
33. Maihofner, C., Schmelz, M., Forster, C., Neundorfer, B., Handwerker, H.O., 2004. Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur. J. Neurosci. 19 (12), 3211- 3218.
34. Maihofner, C., Forster, C., Birklein, F., Neundorfer, B., Handwerker, H.O., 2005. Brain processing during mechanical hyper algesia in complex regional pain syndrome: a functional MRI study. Pain 114 (1-2), 93- 103.
35. Mauguiere, F., Frot, M., Peyron, R., Garcia-Larrea, L., Laurent, B., Michel, D., 1999. The role of parietal opercular and insular cortex in pain sensation in humans: data from PET activation studies and intracortical recordings of CO2 laser evoked potentials (LEPs). Electroencephalogr. Clin. Neurophysiol., Suppl. 49, 255- 260.
36. May, A., Bahra, A., Buchel, C., Frackowiak, R.S., Goadsby, P.J., 1998. Hypothalamic activation in cluster headache attacks. Lancet 352, 275-278.
37. May, A., Bahra, A., Buchel, C., Frackowiak, R.S., Goadsby, P.J., 2000. PET and MRA findings in cluster headache and MRA in experimental pain. Neurology 55 (9), 1328- 1335.
38. Mesulam, M.M., Mufson, E.J., 1982. Insula of the old world monkey: III. Efferent cortical output and comments on function. J. Comp. Neurol. 212 (1), 38-52.
39. Ostrowsky, K., Magnin, M., Ryvlin, P., Isnard, J., Guenot, M., Mauguiere, F., 2002. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb. Cortex 12 (4), 376-385.
40. Petrovic, P., Ingvar, M., Stone-Elander, S., Petersson, K.M., Hansson, P., 1999. A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy. Pain 83 (3), 459- 470.
41. Peyron, R., Garcia-Larrea, L., Gregoire, M.C., Convers, P., Lavenne, F., Veyre, L., Froment, J.C., Mauguiere, F., Michel, D., Laurent, B., 1998. Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. Brain 121 (Pt 2), 345- 356.
42. Peyron, R., Garcia-Larrea, L., Gregoire, M.C., Convers, P., Richard, A., Lavenne, F., Barral, F.G., Mauguiere, F., Michel, D., Laurent, B., 2000a. Parietal and cingulate processes in central pain. A combined positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) study of an unusual case. Pain 84 (1), 77- 87.
43. Peyron, R., Laurent, B., Garcia-Larrea, L., 2000b. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol. Clin. 30 (5), 263-288.
44. Peyron, R., Frot, M., Schneider, F., Garcia-Larrea, L., Mertens, P., Barral, F.G., Sindou, M., Laurent, B., Mauguiere, F., 2002. Role of operculoinsular cortices in human pain processing: converging evidence from PET, fMRI, dipole modeling, and intracerebral recordings of evoked potentials. NeuroImage 17 (3), 1336- 1346.
45. Peyron, R., Schneider, F., Faillenot, I., Convers, P., Barral, F.G., Garcia-Larrea, L., Laurent, B., 2004. An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain. Neurology 63 (10), 1838- 1846.
46. Porro, C.A., 2003. Functional imaging and pain: behavior, perception, and modulation. Neuroscientist 9 (5), 354- 369.
47. Rosen, S.D., Paulesu, E., Frith, C.D., Frackowiak, R.S., Davies, G.J., Jones, T., Camici, P.G., 1994. Central nervous pathways mediating angina pectoris. Lancet 344 (6), 147- 150.
48. Rosen, S.D., Paulesu, E., Wise, R.J., Camici, P.G., 2002. Central neural contribution to the perception of chest pain in cardiac syndrome X. Heart 87, 513- 519.
49. Small, D.M., Prescott, J., 2005. Odor/taste integration and the perception of flavour. Exp. Brain Res. 166 (3- 4), 345- 357.
50. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Bannister, P.R., DeLuca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., DeStefano, N., Brady, J.M., Matthews, P.M., 2004. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 (Suppl. 1), S208- S219.
51. Spielberger, C.D., Gorsuch, R.L., Luschene, R.E., 1970. Manual for the State-Trait Inventory. Consulting Psychologists Press, Palo Alto, CA.
52. Tataranni, P.A., Gautier, J.F., Chen, K., Uecker, A., Bandy, D., Salbe, A.D., Pratley, R.E., Lawson, M., Reiman, E.M., Ravussin, E., 1999. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc. Natl. Acad. Sci. U. S. A. 96 (8), 4569- 4574.
53. Tolle, T.R., Kaufmann, T., Siessmeier, T., Lautenbacher, S., Berthele, A., Munz, F., Zieglgansberger, W., Willoch, F., Schwaiger, M., Conrad, B., Bartenstein, P., 1999. Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann. Neurol. 45 (1), 40- 47.
54. Willoch, F., Gamringer, U., Medele, R., Steude, U., Tolle, T.R., 2003. An algesia by electrostimulation of the trigeminal ganglion in patients with trigeminopathic pain: a PET activation study. Pain 103 (1-2), 119-130.
55. Witting, N., Kupers, R.C., Svensson, P., Arendt-Nielsen, L., Gjedde, A., Jensen, T.S., 2001. Experimental brush-evoked allodynia activates posterior parietal cortex. Neurology 57 (10), 1817-1824.
56. Woolrich, M.W., Ripley, B.D., Brady, M., Smith, S.M., 2001. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuro-Image 14 (6), 1370-1386.
57. Woolrich, M.W., Behrens, T.E., Beckmann, C.F., Jenkinson, M., Smith, S.M., 2004. Multilevel linear modelling for FMRI group analysis using bayesian inference. NeuroImage 21 (4), 1732-1747.
58. Worsley, K.J., Friston, K.J., 1995. Analysis of fMRI time-series revisitedagain. NeuroImage 2 (3), 173-181.
59. Worsley, K.J., Evans, A.C., Marrett, S., Neelin, P., 1992. A threedimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 12 (6), 900-918.
60. Zald, D.H., Lee, J.T., Fluegel, K.W., Pardo, J.V., 1998. Aversive gustatory stimulation activates limbic circuits in humans. Brain 121 (Pt. 6), 1143-1154.
61. Zambreanu, L., Wise, R.G., Brooks, J.C., Iannetti, G.D., Tracey, I., 2005. A role for the brain stem in central sensitisation in humans. Evidence from functional magnetic resonance imaging. Pain 114 (3), 397- 407