A psychophysical study of endogenous analgesia: The role of the conditioning pain in the induction and magnitude of conditioned pain modulation
Rony-Reuven Nir
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorYelena Granovsky
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorCorresponding Author
David Yarnitsky
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Department of Neurology, Rambam Health Care Campus, P.O.B. 9602, Haifa 31096, Israel. Tel.: +972 4 854 2605; fax: +972 4 854 2944 [email protected].Search for more papers by this authorElliot Sprecher
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorMichal Granot
Faculty of Social Welfare and Health Sciences, University of Haifa, Haifa, Israel
Search for more papers by this authorRony-Reuven Nir
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorYelena Granovsky
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorCorresponding Author
David Yarnitsky
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Department of Neurology, Rambam Health Care Campus, P.O.B. 9602, Haifa 31096, Israel. Tel.: +972 4 854 2605; fax: +972 4 854 2944 [email protected].Search for more papers by this authorElliot Sprecher
Department of Neurology, Rambam Health Care Campus, Haifa, Israel
Laboratory of Clinical Neurophysiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel
Search for more papers by this authorMichal Granot
Faculty of Social Welfare and Health Sciences, University of Haifa, Haifa, Israel
Search for more papers by this authorAbstract
Endogenous analgesia (EA) can be examined experimentally using a conditioned pain modulation (CPM) paradigm. While noxious conditioning stimulation intensities (CSIs) are mainly used, it has not been fully investigated in the same experimental design whether the experienced conditioning pain level affects CPM responses. The principal goal of the present study was to characterize CPM induction and magnitudes evoked by various conditioning pain levels. Furthermore, we explored associations between conditioning pain reports and CPM responses across various CSIs. Thirty healthy, young, right-handed males were tested with a parallel CPM paradigm. Three different CSIs (hand water-immersion) induced mild, moderate and intense pain levels, rated 12.41±7.85, 31.57±9.56 and 58.1±11.43, respectively (0–100 numerical pain scale) (P<0.0001). Contact-heat ‘test-stimulus’ levels were compared before and during conditioning. Within the group, (i) CPM was induced only by the moderate and intense CSIs (Ps≤0.001); (ii) no difference was demonstrated between the magnitudes of these CPM responses. Regression analysis revealed that CPM induction was independent of the perceived conditioning pain level, but associated with the absolute CSI (P<0.0001). Conditioning pain levels were correlated across all CSIs, as were CPM magnitudes (Ps≤0.01). We conclude that among males, (i) once a CPM response is evoked by a required conditioning pain experience, its magnitude is not further affected by increasing conditioning pain and (ii) CPM magnitudes are inter-correlated, but unrelated to conditioning pain reports. These observations may suggest that CPM responses represent an intrinsic element of an individual's EA processes, which are not significantly affected by the experienced conditioning pain.
References
- L. Arendt-Nielsen K.A. Sluka H.L. Nie Experimental muscle pain impairs descending inhibition. Pain 140 2008 465–471.
- L. Baad-Hansen H.F. Poulsenb H.M. Jensenc P. Svensson Lack of sex differences in modulation of experimental intraoral pain by diffuse noxious inhibitory controls (DNIC). Pain 116 2005 359–365.
- F.W. Bertelsmann J.J. Heimans E.J. Weber E.A. van der Veen J.A. Schouten Thermal discrimination thresholds in normal subjects and in patients with diabetic neuropathy. J Neurol Neurosurg Psychiat 48 1985 686–690.
- M.C. Bushnell M.B. Taylor G.H. Duncan R. Dubner Discrimination of innocuous and noxious thermal stimuli applied to the face in human and monkey. Somatosens Res 1983 119–129.
- D. Chitour A.H. Dickenson D. Le Bars Pharmacological evidence for the involvement of serotonergic mechanisms in diffuse noxious inhibitory controls (DNIC). Brain Res 25 1982 329–337.
- P.J. Dyck E.W. Lambert P.C. Nichols Quantitative measurement of sensation related to compound action potential and number and sizes of myelinated and unmyelinated fibers of sural nerve in health, Friedreich's ataxia, hereditary sensory neuropathy, and tabes dorsalis. A. Remond Handbook of electroencephalography and clinical neurophysiology 1971 Elsevier: Amsterdam 83–118.
- R.R. Edwards T.J. Ness D.A. Weigent R.B. Fillingim Individual differences in diffuse noxious inhibitory controls (DNIC): association with clinical variables. Pain 106 2003a 427–437.
- R.R. Edwards R.B. Fillingim T.J. Ness Age-related differences in endogenous pain modulation: a comparison of diffuse noxious inhibitory controls in healthy older and younger adults. Pain 101 2003b 155–165.
- E. Eisenberg A. Midbari M. Haddad D. Pud Predicting the analgesic effect to oxycodone by ‘static’ and ‘dynamic’ quantitative sensory testing in healthy subjects. Pain 151 2010 104–109.
- K. Fujii K. Motohashi M. Umino Heterotopic ischemic pain attenuates somatosensory evoked potentials induced by electrical tooth stimulation: diffuse noxious inhibitory controls in the trigeminal nerve territory. Eur J Pain 10 2006 495–504.
-
R.H. Gracely
Studies of pain in human subjects. S.B. McMahon M. Koltzenburg
Wall and Melzack's textbook of pain
2006 Elsevier/Churchill Livingstone: Philadelphia 267–289.
10.1016/B0-443-07287-6/50022-9 Google Scholar
- M. Granot I. Weissman-Fogel Y. Crispel D. Pud Y. Granovsky E. Sprecher et al. Determinants of endogenous analgesia magnitude in a diffuse noxious inhibitory control (DNIC) paradigm: do conditioning stimulus painfulness, gender and personality variables matter?. Pain 136 2008 142–149.
- A.T. Hirsh S.Z. George J.E. Bialosky M.E. Robinson Fear of pain, pain catastrophizing, and acute pain perception: relative prediction and timing of assessment. J Pain 9 2008 806–812.
- S.L. Jones Descending noradrenergic influences on pain. Prog Brain Res 88 1991 381–394.
- D.R. Kenshalo J.P. Nafe W.W. Dawson A new method for the investigation of thermal sensitivity. J Psychol 49 1960 29–41.
- M. Larivière P. Goffaux S. Marchand N. Julien Changes in pain perception and descending inhibitory controls start at middle age in healthy adults. Clin J Pain 23 2007 506–510.
- S. Lautenbacher G.B. Rollman Possible deficiencies of pain modulation in fibromyalgia. Clin J Pain 13 1997 189–195.
- S. Lautenbacher S. Roscher F. Strian Inhibitory effects do not depend on the subjective experience of pain during heterotopic noxious conditioning stimulation (HNCS): a contribution to the psychophysics of pain inhibition. Eur J Pain 6 2002 365–374.
- S. Lautenbacher Kunz. Miriam S. Burkhardt The effects of DNIC-type inhibition on temporal summation compared to single pulse processing: does sex matter?. Pain 140 2008 429–435.
- D. Le Bars A.H. Dickenson J.M. Besson Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurons in the rat. Pain 6 1979 283–304.
-
D. Le Bars J.C. Willer
Pain modulation triggered by high-intensity stimulation: implication for acupuncture analgesia. A. Satoh
International congress series
2002 Elsevier: Amsterdam.
10.1016/S0531-5131(02)00412-0 Google Scholar
- W. Maixner R. Fillingim D. Booker A. Sigurdsson Sensitivity of patients with painful temporomandibular disorders to experimentally evoked pain. Pain 63 1995 341–351.
- K. Moriyama H. Ifuku Assessment of cardiac contractility during a cold pressor test by using (dP/dt)/P of carotid artery pulses. Eur J Appl Physiol 100 2007 185–191.
- J. Olesen Clinical and pathophysiological observations in migraine and tension-type headache explained by integration of vascular, supraspinal and myofascial inputs. Pain 46 1991 125–132.
- M.L. Peters A.J.M. Schmidt M.A. Van der Hout R. Koopmans M.E. Sluijter Chronic back pain, acute postoperative pain and activation of diffuse noxious inhibitory controls (DNIC). Pain 50 1992 177–187.
- A. Pielsticker G. Haag M. Zaudig S. Lautenbacher Impairment of pain inhibition in chronic tension-type headache. Pain 118 2005 215–223.
- D. Pud E. Sprecher D. Yarnitsky Homotopic and heterotopic effects of endogenous analgesia in healthy volunteers. Neurosci Lett 380 2005 209–213.
- D. Pud Y. Granovsky D. Yarnitsky The methodology of experimentally induced diffuse noxious inhibitory control (DNIC)-like effect in humans. Pain 144 2009 16–19.
- K.C. Ram E. Eisenberg M. Haddad D. Pud Oral opioid use alters DNIC but not cold pain perception in patients with chronic pain—new perspective of opioid-induced hyperalgesia. Pain 139 2008 431–438.
- J. Schouenborg A. Dickenson Effects of a distant noxious stimulation on A and C fibre-evoked flexion reflexes and neuronal activity in the dorsal horn of the rat. Brain Res 25 1985 23–32.
- M. Serrao P. Rossi G. Sandrini L. Parisi G.A. Amabile G. Nappi et al. Effects of diffuse noxious inhibitory controls on temporal summation of the RIII reflex in humans. Pain 112 2004 260–353.
- R. Staud M.E. Robinson C.J. Vierck Jr D.D. Price Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain 101 2003 167–174.
- A. Streff L.K. Kuehl G. Michaux F. Anton Differential physiological effects during tonic painful hand immersion tests using hot and ice water. Eur J Pain 14 2010 266–272.
- R. Treister E. Eisenberg E. Gershon M. Haddad D. Pud Factors affecting—and relationships between—different modes of endogenous pain modulation in healthy volunteers. Eur J Pain 14 2010 608–614.
- I. Weissman-Fogel Y. Granovsky Y. Crispel A. Ben-Nun L.A. Best D. Yarnitsky et al. Enhanced presurgical pain temporal summation response predicts post-thoracotomy pain intensity during the acute postoperative phase. J Pain 10 2009 628–636.
- J.C. Willer T. De Broucker D. Le Bars Encoding of nociceptive thermal stimuli by diffuse noxious inhibitory controls in humans. J Neurophysiol 62 1989 1028–1038.
- D. Yarnitsky Y. Crispel E. Eisenberg Y. Granovsky A. Ben-Nun E. Sprecher et al. Prediction of chronic post-operative pain: pre-operative DNIC testing identifies patients at risk. Pain 138 2008 22–28.
- D. Yarnitsky L. Arendt-Nielsen D. Bouhassira R.R. Edwards R.B. Fillingim M. Granot et al. Recommendations on terminology and practice of psychophysical DNIC testing. Eur J Pain 14 2010 339.