Pain and non-pain processing during hypnosis: a thulium-YAG event-related fMRI study.

[en] The neural mechanisms underlying the antinociceptive effects of hypnosis still remain unclear. Using a parametric single-trial thulium-YAG laser fMRI paradigm, we assessed changes in brain activation and connectivity related to the hypnotic state as compared to normal wakefulness in 13 healthy volunteers. Behaviorally, a difference in subjective ratings was found between normal wakefulness and hypnotic state for both non-painful and painful intensity-matched stimuli applied to the left hand. In normal wakefulness, non-painful range stimuli activated brainstem, contralateral primary somatosensory (S1) and bilateral insular cortices. Painful stimuli activated additional areas encompassing thalamus, bilateral striatum, anterior cingulate (ACC), premotor and dorsolateral prefrontal cortices. In hypnosis, intensity-matched stimuli in both the non-painful and painful range failed to elicit any cerebral activation. The interaction analysis identified that contralateral thalamus, bilateral striatum and ACC activated more in normal wakefulness compared to hypnosis during painful versus non-painful stimulation. Finally, we demonstrated hypnosis-related increases in functional connectivity between S1 and distant anterior insular and prefrontal cortices, possibly reflecting top-down modulation.

Disciplines :

Neurology
Anesthesia & intensive care

Author, co-author :

Vanhaudenhuyse, Audrey ; Université de Liège - ULiège > Centre de recherches du cyclotron

Boly, Mélanie ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie

Balteau, Evelyne ; Université de Liège - ULiège > Centre de recherches du cyclotron

Schnakers, Caroline ; Université de Liège - ULiège > Centre de recherches du cyclotron

Moonen, Gustave ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Luxen, André ; Université de Liège - ULiège > Centre de Recherches du cyclotron - Département de chimie (sciences) > Chimie organique de synthèse - Centre de recherches du cyclotron

Lamy, Maurice ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation

Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron

Brichant, Jean-François ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation

Maquet, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron - Département des sciences cliniques

Faymonville, Marie ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation

Language :

English

Title :

Pain and non-pain processing during hypnosis: a thulium-YAG event-related fMRI study.

Publication date :

2009

Journal title :

NeuroImage

ISSN :

1053-8119

eISSN :

1095-9572

Publisher :

Elsevier Science, Orlando, United States - Florida

Volume :

Issue :

Pages :

1047-54

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.coma.ulg.ac.be/papers/hypnosis.html

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
EU - European Commission
JSMF - James S McDonnell Foundation [US-MO]
MSF - Mind Science Foundation [US-TX]
French Speaking Community Concerted Research Action
FMRE - Fondation Médicale Reine Elisabeth [BE]

Available on ORBi :

since 27 October 2009

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Bibliography

Augustine J.R. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Rev. 22 (1996) 229-244
Boly M., Balteau E., Schnakers C., Degueldre C., Moonen G., Luxen A., Phillips C., Peigneux P., Maquet P., and Laureys S. Baseline brain activity fluctuations predict somatosensory perception in humans. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 12187-12192
Boly M., Tshibanda L., Vanhaudenhuyse A., Noirhomme Q., Schnakers C., Ledoux D., et al. Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum. Brain Mapp. (April 6). (2009)
Brown P., and Marsden C.D. What do the basal ganglia do?. Lancet 351 (1998) 1801-1804
Buchel C., Bornhovd K., Quante M., Glauche V., Bromm B., and Weiller C. 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 (2002) 970-976
Charlton E. Ethical guidelines for pain research in humans. Committee on Ethical Issues of the International Association for the Study of Pain. Pain 63 (1995) 277-278
Coghill R.C., Talbot J.D., Evans A.C., Meyer E., Gjedde A., Bushnell M.C., and Duncan G.H. Distributed processing of pain and vibration by the human brain. J. Neurosci. 14 (1994) 4095-4108
Courtney S.M., Petit L., Haxby J.V., and Ungerleider L.G. The role of prefrontal cortex in working memory: examining the contents of consciousness. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353 (1998) 1819-1828
Craig A.D., Bushnell M.C., Zhang E.T., and Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 372 (1994) 770-773
Craig A.D., Reiman E.M., Evans A., and Bushnell M.C. Functional imaging of an illusion of pain. Nature 384 (1996) 258-260
Craig A.D., Chen K., Bandy D., and Reiman E.M. Thermosensory activation of insular cortex. Nat. Neurosci. 3 (2000) 184-190
Davidson R.J. Anterior cerebral asymmetry and the nature of emotion. Brain Cogn. 20 (1992) 125-151
Defechereux T., Meurisse M., Hamoir E., Gollogly L., Joris J., and Faymonville M.E. Hypnoanesthesia for endocrine cervical surgery: a statement of practice. J. Altern. Complement. Med. 5 (1999) 509-520
Defechereux T., Degauque C., Fumal I., Faymonville M.E., Joris J., Hamoir E., and Meurisse M. Hypnosedation, a new method of anesthesia for cervical endocrine surgery. Prospective randomized study. Ann. Chir. 125 (2000) 539-546
Derbyshire S.W., and Jones A.K. Cerebral responses to a continual tonic pain stimulus measured using positron emission tomography. Pain 76 (1998) 127-135
Derbyshire S.W., Jones A.K., Gyulai F., Clark S., Townsend D., and Firestone L.L. Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73 (1997) 431-445
Derbyshire S.W., Whalley M.G., Stenger V.A., and Oakley D.A. Cerebral activation during hypnotically induced and imagined pain. NeuroImage 23 1 (2004) 392-401
Desseilles M., Balteau E., Sterpenich V., Dang-Vu T.T., Darsaud A., Vandewalle G., Albouy G., Salmon E., Peters F., Schmidt C., Schabus M., Gais S., Degueldre C., Phillips C., Luxen A., Ansseau M., Maquet P., and Schwartz S. Abnormal neural filtering of irrelevant visual information in depression. J. Neurosci. 29 (2009) 1395-1403
Egner T., Jamieson G., and Gruzelier J. Hypnosis decouples cognitive control from conflict monitoring processes of the frontal lobe. NeuroImage 27 (2005) 969-978
Elkins G., Jensen M.P., and Patterson D.R. Hypnotherapy for the management of chronic pain. Int. J. Clin. Exp. Hypn. 55 (2007) 275-287
Faymonville M.E., Fissette J., Mambourg P.H., Roediger L., Joris J., and Lamy M. Hypnosis as adjunct therapy in conscious sedation for plastic surgery. Reg. Anesth. 20 (1995) 145-151
Faymonville M.E., Mambourg P.H., Joris J., Vrijens B., Fissette J., Albert A., and Lamy M. Psychological approaches during conscious sedation. Hypnosis versus stress reducing strategies: a prospective randomized study. Pain 73 (1997) 361-367
Faymonville M.E., Meurisse M., and Fissette J. Hypnosedation: a valuable alternative to traditional anaesthetic techniques. Acta Chir. Belg. 99 (1999) 141-146
Faymonville M.E., Laureys S., Degueldre C., DelFiore G., Luxen A., Franck G., Lamy M., and Maquet P. Neural mechanisms of antinociceptive effects of hypnosis. Anesthesiology 92 (2000) 1257-1267
Faymonville M.E., Roediger L., Del Fiore G., Delgueldre C., Phillips C., Lamy M., Luxen A., Maquet P., and Laureys S. Increased cerebral functional connectivity underlying the antinociceptive effects of hypnosis. Cogn. Brain Res. 17 (2003) 255-262
Frenay M.C., Faymonville M.E., Devlieger S., Albert A., and Vanderkelen A. Psychological approaches during dressing changes of burned patients: a prospective randomised study comparing hypnosis against stress reducing strategy. Burns 27 (2001) 793-799
Friston K.J., Ashburner J., Frith C., Poline J., Heather J., and Frackowiak R. Spatial realignment and normalization of images. Hum. Brain Mapp. 2 (1995) 165-189
Friston K.J., Holmes A.P., Poline J.B., Grasby P.J., Williams S.C., Frackowiak R.S., and Turner R. Analysis of fMRI time-series revisited. NeuroImage 2 (1995) 45-53
Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., and Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6 (1997) 218-229
Gandhi B., and Oakley D.A. Does 'hypnosis' by any other name smell as sweet? The efficacy of 'hypnotic' inductions depends on the label 'hypnosis'. Conscious Cogn. 14 (2005) 304-315
Gitelman D.R., Penny W.D., Ashburner J., and Friston K.J. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage 19 (2003) 200-207
Grondahl J.R., and Rosvold E.O. Hypnosis as a treatment of chronic widespread pain in general practice: a randomized controlled pilot trial. BMC Musculoskelet. Disord. 9 124 (2008)
Hilgard E.R., Lauer L.W., and Morgan A.H. Manual for Standard Profile Scales of Hypnotic Susceptibility (1963), Forms I and II, Palo Alto, CA
Hofbauer R.K., Rainville P., Duncan G.H., and Bushnell M.C. Cortical representation of the sensory dimension of pain. J. Neurophysiol. 86 (2001) 402-411
Hylands-White N., and Derbyshire S. Modifying pain perception: is it better to be hypnotisable or feel that you are hypnotised?. Contemp. Hypn. 24 (2007) 143-153
Jensen M.P., Barber J., Hanley M.A., Engel J.M., Romano J.M., Cardenas D.D., Kraft G.H., Hoffman A.J., and Patterson D.R. Long-term outcome of hypnotic-analgesia treatment for chronic pain in persons with disabilities. Int. J. Clin. Exp. Hypn. 56 (2008) 156-169
Jones A.K., Brown W.D., Friston K.J., Qi L.Y., and Frackowiak R.S. Cortical and subcortical localization of response to pain in man using positron emission tomography. Proc. Biol. Sci. 244 (1991) 39-44
Kaiser J., Barker R., Haenschel C., Baldeweg T., and Gruzelier J.H. Hypnosis and event-related potential correlates of error processing in a stroop-type paradigm: a test of the frontal hypothesis. Int. J. Psychophysiol. 27 (1997) 215-222
Kallio S., Revonsuo A., Hamalainen H., Markela J., and Gruzelier J. Anterior brain functions and hypnosis: a test of the frontal hypothesis. Int. J. Clin. Exp. Hypn. 49 (2001) 95-108
Laureys S., Faymonville M.E., Peigneux P., Damas P., Lambermont B., Del Fiore G., Degueldre C., Aerts J., Luxen A., Franck G., Lamy M., Moonen G., and Maquet P. Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. NeuroImage 17 (2002) 732-741
Majerus S., Belayachi S., De Smedt B., Leclercq A.L., Martinez T., Schmidt C., Weekes B., and Maquet P. Neural networks for short-term memory for order differentiate high and low proficiency bilinguals. NeuroImage 42 (2008) 1698-1713
Maquet P., Faymonville M.E., Degueldre C., Delfiore G., Franck G., Luxen A., and Lamy M. Functional neuroanatomy of hypnotic state. Biol. Psychiatry 45 (1999) 327-333
Melzack R., and Wall P.D. Pain mechanisms: a new theory. Science 150 (1965) 971-979
Mesulam M.M., and Mufson E.J. Insula of the old world monkey. III: Efferent cortical output and comments on function. J. Comp. Neurol. 212 (1982) 38-52
Meurisse M. Thyroid and parathyroid surgery under hypnosis: from fiction to clinical application. Bull. Mem. Acad. R. Med. Belg. 154 (1999) 142-150 discussion 150-144
Meurisse M., Faymonville M.E., Joris J., Nguyen Dang D., Defechereux T., and Hamoir E. Endocrine surgery by hypnosis. From fiction to daily clinical application. Ann. Endocrinol. (Paris) 57 (1996) 494-501
Mikl M., Marecek R., Hlustik P., Pavlicova M., Drastich A., Chlebus P., et al. Effects of spatial smoothing on fMRI group inferences. Magn. Reson. Imaging 26 4 (2008) 490-503
Oneal B.J., Patterson D.R., Soltani M., Teeley A., and Jensen M.P. Virtual reality hypnosis in the treatment of chronic neuropathic pain: a case report. Int. J. Clin. Exp. Hypn. 56 (2008) 451-462
Penny, W., Holmes, A., 2003. In: Frackowiak R.F.K., Frith C., Dolan R., Price C., Zeki S., Ashburner J., Penny W. (Academic, London) (Ed.), Hum. Brain Funct., p. 1114.
Peyron R., Laurent B., and Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol. Clin. 30 (2000) 263-288
Ploghaus A., Tracey I., Gati J.S., Clare S., Menon R.S., Matthews P.M., and Rawlins J.N. Dissociating pain from its anticipation in the human brain. Science 284 (1999) 1979-1981
Ploner M., Schmitz F., Freund H.J., and Schnitzler A. Differential organization of touch and pain in human primary somatosensory cortex. J. Neurophysiol. 83 (2000) 1770-1776
Price D.D., Milling L.S., Kirsch I., Duff A., Montgomery G.H., and Nicholls S.S. An analysis of factors that contribute to the magnitude of placebo analgesia in an experimental paradigm. Pain 83 (1999) 147-156
Raij T.T., Numminen J., Narvanen S., Hiltunen J., and Hari R. Brain correlates of subjective reality of physically and psychologically induced pain. Proc. Natl. Acad. Sci. U. S. A. 102 6 (2005) 2147-2151
Rainville P., Duncan G.H., Price D.D., Carrier B., and Bushnell M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277 (1997) 968-971
Rainville P., Carrier B., Hofbauer R.K., Bushnell M.C., and Duncan G.H. Dissociation of sensory and affective dimensions of pain using hypnotic modulation. Pain 82 (1999) 159-171
Rainville P., Hofbauer R.K., Paus T., Duncan G.H., Bushnell M.C., and Price D.D. Cerebral mechanisms of hypnotic induction and suggestion. J. Cogn. Neurosci. 11 (1999) 110-125
Sharar S.R., Miller W., Teeley A., Soltani M., Hoffman H.G., Jensen M.P., and Patterson D.R. Applications of virtual reality for pain management in burn-injured patients. Expert Rev. Neurother. 8 (2008) 1667-1674
The Executive Committee of the American Psychological Association - Division of Psychological Hypnosis. Definition and description of hypnosis. Contemp. Hypn. 11 (1994) 142-162
Timmermann L., Ploner M., Haucke K., Schmitz F., Baltissen R., and Schnitzler A. Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J. Neurophysiol. 86 (2001) 1499-1503
Tracey I. Imaging pain. Br. J. Anaesth. 101 (2008) 32-39
Vanhaudenhuyse A., Boly M., Laureys S., and Faymonville M.E. Neurophysiological correlates of hypnotic analgesia. Contemp. Hypn. 25 3 (2008)
Villemure C., and Bushnell M.C. Mood influences supraspinal pain processing separately from attention. J. Neurosci. 29 (2009) 705-715
Wager T.D., Rilling J.K., Smith E.E., Sokolik A., Casey K.L., Davidson R.J., Kosslyn S.M., Rose R.M., and Cohen J.D. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303 (2004) 1162-1167
Wall P.D. The placebo effect: an unpopular topic. Pain 51 (1992) 1-3
White T., O'Leary D., Magnotta V., Arndt S., Flaum M., and Andreasen N.C. Anatomic and functional variability: the effects of filter size in group fMRI data analysis. NeuroImage 13 4 (2001) 577-588
World Medical Association declaration of Helsinki. Recommendations guiding physicians in biomedical research involving human subjects. JAMA 277 (1997) 925-926