Dissociable neural activity to self- vs. externally administered thermal hyperalgesia: A parametric fMRI study

European Journal of Neuroscience

Volumn 27, Issue 3, 2008, Pages 739-749

  Mohr, C ^a   Leyendecker, S ^a   Helmchen, C ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Capsaicin; Contact heat; fMRI; Human; Self administered pain; Thermal hyperalgesia

Indexed keywords

CAPSAICIN;

ADULT; ARTICLE; CINGULATE GYRUS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAT SENSATION; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; INSULA; MALE; NERVE POTENTIAL; NORMAL HUMAN; PAIN; PREFRONTAL CORTEX; PRIORITY JOURNAL; SOMATOSENSORY CORTEX;

ADAPTATION, PSYCHOLOGICAL; ADULT; BRAIN; BRAIN MAPPING; CAPSAICIN; CEREBRAL CORTEX; CHRONIC DISEASE; COGNITION; DATA INTERPRETATION, STATISTICAL; FUNCTIONAL LATERALITY; GYRUS CINGULI; HEAT; HUMANS; HYPERALGESIA; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; NEUROPSYCHOLOGICAL TESTS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; SELF ADMINISTRATION; SOMATOSENSORY CORTEX;

EID: 39049093172     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06036.x     Document Type: Article

References (66)

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, 463 484.
2. Bantick, S.J., Wise, R.G., Ploghaus, A., Clare, S., Smith, S.M. Tracey, I. (2002) Imaging how attention modulates pain in humans using functional MRI. Brain, 125, 310 319.
3. Baron, R., Baron, Y., Disbrow, E. Roberts, T.P. (1999) Brain processing of capsaicin-induced secondary hyperalgesia: a functional MRI study. Neurology, 53, 548 557.
4. Blakemore, S.J., Frith, C.D. Wolpert, D.M. (1999) Spatio-temporal prediction modulates the perception of self-produced stimuli. J. Cogn. Neurosci., 11, 551 559.
5. Blakemore, S.J., Goodbody, S.J. Wolpert, D.M. (1998) Predicting the consequences of our own actions: the role of sensorimotor context estimation. J. Neurosci., 18, 7511 7518.
6. Blakemore, S.J., Wolpert, D. Frith, C. (2000) Why can't you tickle yourself? Neuroreport, 11, R11 R16.
7. 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, 1326 1336.
8. Buchel, C., Bornhovd, K., Quante, M., Glauche, V., Bromm, B. Weiller, C. (2002) Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: a parametric single-trial laser functional magnetic resonance imaging study. J. Neurosci., 22, 970 976.
9. Carlsson, K., Andersson, J., Petrovic, P., Petersson, K.M., Ohman, A. Ingvar, M. (2006) Predictability modulates the affective and sensory-discriminative neural processing of pain. Neuroimage, 32, 1804 1814.
10. Casey, K.L., Morrow, T.J., Lorenz, J. Minoshima, S. (2001) Temporal and spatial dynamics of human forebrain activity during heat pain: analysis by positron emission tomography. J. Neurophysiol., 85, 951 959.
11. Coghill, R.C., Gilron, I. Iadarola, M.J. (2001) Hemispheric lateralization of somatosensory processing. J. Neurophysiol., 85, 2602 2612.
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, 1934 1943.
13. Craig, A.D. (2003) Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol., 13, 500 505.
14. Craig, A.D., Chen, K., Bandy, D. Reiman, E.M. (2000) Thermosensory activation of insular cortex. Nat. Neurosci., 3, 184 190.
15. Ducreux, D., Attal, N., Parker, F. Bouhassira, D. (2006) Mechanisms of central neuropathic pain: a combined psychophysical and fMRI study in syringomyelia. Brain, 129, 963 976.
16. Ekerot, C.F., Garwicz, M. Schouenborg, J. (1991) The postsynaptic dorsal column pathway mediates cutaneous nociceptive information to cerebellar climbing fibres in the cat. J. Physiol., 441, 275 284.
17. Farrer, C., Franck, N., Georgieff, N., Frith, C.D., Decety, J. Jeannerod, M. (2003) Modulating the experience of agency: a positron emission tomography study. Neuroimage, 18, 324 333.
18. Friston, K.J., Holmes, A.P., Poline, J.B., Grasby, P.J., Williams, S.C., Frackowiak, R.S. Turner, R. (1995) Analysis of fMRI time-series revisited. Neuroimage, 2, 45 53.
19. Friston, K.J., Penny, W.D. Glaser, D.E. (2005) Conjunction revisited. Neuroimage, 25, 661 667.
20. Frot, M., Magnin, M., Mauguiere, F. Garcia-Larrea, L. (2007) Human SII and posterior insula differently encode thermal laser stimuli. Cereb. Cortex., 7, 610 620.
21. Gusnard, D.A. Raichle, M.E. (2001) Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci., 2, 685 694.
22. Helmchen, C., Mohr, C., Erdmann, C. Binkofski, F. (2004) Cerebellar neural responses related to actively and passively applied noxious thermal stimulation in human subjects: a parametric fMRI study. Neurosci. Lett., 361, 237 240.
23. Helmchen, C., Mohr, C., Erdmann, C., Binkofski, F. Buchel, C. (2006) Neural activity related to self- versus externally generated painful stimuli reveals distinct differences in the lateral pain system in a parametric fMRI study. Hum. Brain Mapp., 27, 755 765.
24. Helmchen, C., Mohr, C., Erdmann, C., Petersen, D. Nitschke, M.F. (2003) Differential cerebellar activation related to perceived pain intensity during noxious thermal stimulation in humans: a functional magnetic resonance imaging study. Neurosci. Lett., 335, 202 206.
25. Hofbauer, R.K., Rainville, P., Duncan, G.H. Bushnell, M.C. (2001) Cortical representation of the sensory dimension of pain. J. Neurophysiol., 86, 402 411.
26. 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, 931 947.
27. Kalisch, R., Wiech, K., Critchley, H.D. Dolan, R.J. (2006) Levels of appraisal: a medial prefrontal role in high-level appraisal of emotional material. Neuroimage, 30, 1458 1466.
28. Kerns, J.G., Cohen, J.D., MacDonald, A.W., 3rd, Cho, R.Y., Stenger, V.A. Carter, C.S. (2004) Anterior cingulate conflict monitoring and adjustments in control. Science, 303, 1023 1026.
29. Kong, J., Gollub, R.L., Rosman, I.S., Webb, J.M., Vangel, M.G., Kirsch, I. Kaptchuk, T.J. (2006a) Brain activity associated with expectancy-enhanced placebo analgesia as measured by functional magnetic resonance imaging. J. Neurosci., 26, 381 388.
30. Kong, J., White, N.S., Kwong, K.K., Vangel, M.G., Rosman, I.S., Gracely, R.H. Gollub, R.L. (2006b) Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum. Brain Mapp., 27, 715 721.
31. 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, 383 393.
32. Lorenz, J., Minoshima, S. Casey, K.L. (2003) Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. Brain, 126, 1079 1091.
33. Maihofner, C., Forster, C., Birklein, F., Neundorfer, B. Handwerker, H.O. (2005) Brain processing during mechanical hyperalgesia in complex regional pain syndrome: a functional MRI study. Pain, 114, 93 103.
34. Maihofner, C. Handwerker, H.O. (2005) Differential coding of hyperalgesia in the human brain: a functional MRI study. Neuroimage, 28, 996 1006.
35. Maihofner, C., Handwerker, H.O. Birklein, F. (2006) Functional imaging of allodynia in complex regional pain syndrome. Neurology, 66, 711 717.
36. Maihofner, C., Handwerker, H.O., Neundorfer, B. Birklein, F. (2004a) Cortical reorganization during recovery from complex regional pain syndrome. Neurology, 63, 693 701.
37. Maihofner, C., Schmelz, M., Forster, C., Neundorfer, B. Handwerker, H.O. (2004b) Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur. J. Neurosci., 19, 3211 3218.
38. Maldjian, J.A., Laurienti, P.J., Kraft, R.A. Burdette, J.H. (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19, 1233 1239.
39. Mohr, C., Binkofski, F., Erdmann, C., Buchel, C. Helmchen, C. (2005) The anterior cingulate cortex contains distinct areas dissociating external from self-administered painful stimulation: a parametric fMRI study. Pain, 114, 347 357.
40. Nichols, T. Hayasaka, S. (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat. Meth. Med. Res., 12, 419 446.
41. Petrovic, P., Dietrich, T., Fransson, P., Andersson, J., Carlsson, K. Ingvar, M. (2005) Placebo in emotional processing - induced expectations of anxiety relief activate a generalized modulatory network. Neuron, 46, 957 969.
42. 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, 459 470.
43. 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, 1336 1346.
44. 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, 345 356.
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, 1838 1846.
46. Phan, K.L., Wager, T., Taylor, S.F. Liberzon, I. (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16, 331 348.
47. Ploghaus, A., Becerra, L., Borras, C. Borsook, D. (2003) Neural circuitry underlying pain modulation: expectation, hypnosis, placebo. Trends Cogn. Sci., 7, 197 200.
48. Ploghaus, A., Tracey, I., Gati, J.S., Clare, S., Menon, R.S., Matthews, P.M. Rawlins, J.N. (1999) Dissociating pain from its anticipation in the human brain. Science, 284, 1979 1981.
49. Price, C.J. Friston, K.J. (1997) Cognitive conjunction: a new approach to brain activation experiments. Neuroimage, 5, 261 270.
50. Salomons, T.V., Johnstone, T., Backonja, M.M. Davidson, R.J. (2004) Perceived controllability modulates the neural response to pain. J. Neurosci., 24, 7199 7203.
51. Salomons, T.V., Johnstone, T., Backonja, M.M., Shackman, A.J. Davidson, R.J. (2007) Individual differences in the effects of perceived controllability on pain perception: critical role of the prefrontal cortex. J. Cogn. Neurosci., 19, 993 1003.
52. Sawamoto, N., Honda, M., Okada, T., Hanakawa, T., Kanda, M., Fukuyama, H., Konishi, J. Shibasaki, H. (2000) Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J. Neurosci., 20, 7438 7445.
53. Schmahmann, J.D., Doyon, J., McDonald, D., Holmes, C., Lavoie, K., Hurwitz, A.S., Kabani, N., Toga, A., Evans, A. Petrides, M. (1999) Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage, 10, 233 260.
54. Schreckenberger, M., Siessmeier, T., Viertmann, A., Landvogt, C., Buchholz, H.G., Rolke, R., Treede, R.D., Bartenstein, P. Birklein, F. (2005) The unpleasantness of tonic pain is encoded by the insular cortex. Neurology, 64, 1175 1183.
55. Schweinhardt, P., Glynn, C., Brooks, J., McQuay, H., Jack, T., Chessell, I., Bountra, C. Tracey, I. (2006a) An fMRI study of cerebral processing of brush-evoked allodynia in neuropathic pain patients. Neuroimage, 32, 256 265.
56. Schweinhardt, P., Lee, M. Tracey, I. (2006b) Imaging pain in patients: is it meaningful? Curr. Opin. Neurol., 19, 392 400.
57. Seminowicz, D.A. Davis, K.D. (2006) Cortical responses to pain in healthy individuals depends on pain catastrophizing. Pain, 120, 297 306.
58. Simpson, J.R. Jr., Drevets, W.C., Snyder, A.Z., Gusnard, D.A. Raichle, M.E. (2001) Emotion-induced changes in human medial prefrontal cortex. II. During anticipatory anxiety. Proc. Natl Acad. Sci. USA, 98, 688 693.
59. 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, 40 47.
60. Tracey, I. (2005) Nociceptive processing in the human brain. Curr. Opin. Neurobiol., 15, 478 487.
61. Wiech, K., Kalisch, R., Weiskopf, N., Pleger, B., Stephan, K.E. Dolan, R.J. (2006) Anterolateral prefrontal cortex mediates the analgesic effect of expected and perceived control over pain. J. Neurosci., 26, 11501 11509.
62. Wiech, K., Seymour, B., Kalisch, R., Stephan, K.E., Koltzenburg, M., Driver, J. Dolan, R.J. (2005) Modulation of pain processing in hyperalgesia by cognitive demand. Neuroimage, 27, 59 69.
63. 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, 1817 1824.
64. Witting, N., Kupers, R.C., Svensson, P. Jensen, T.S. (2006) A PET activation study of brush-evoked allodynia in patients with nerve injury pain. Pain, 120, 145 154.
65. Worsley, K.J. Friston, K.J. (1995) Analysis of fMRI time-series revisited - again. Neuroimage, 2, 173 181.
66. Zambreanu, L., Wise, R.G., Brooks, J.C., Iannetti, G.D. Tracey, I. (2005) A role for the brainstem in central sensitisation in humans. Evidence from functional magnetic resonance imaging. Pain, 114, 397 407.