Electroencephalography and chmcal Neurophystologv, 82 (1992) 387-390

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© 1992 Elsevier Scientific Pubhshers Ireland, Ltd 0013-4649/92/$05 00

E E G 91535 Short communication

Relationship between vertex potentials and magnitude of pre-pain and pain sensations evoked by electrical skin stimuli Jannlck Brennum a and Troels S. Jensen b Laboratory of Sensory Physiology, Department of Neurology, Gentofte Hospttal, Umversltv of Copenhagen, Hellerup (Denmark), and I, Laboratory of Sensory Physiology, Department of Neurology, Aarhus Untterslty Hospaal, Aarhus (Denmark) (Accepted for publication 21 January 1992)

Summary Vertex potentials evoked by painful and non-painful electrical skin stimuli were recorded in 10 healthy male volunteers Peak-to-peak amplitudes of the major vertex potential components were compared with subjective rating of the stimuli While a significant correlation was observed between peak-to-peak amplitudes and stimulus rating following non-painful stimuli, generally no such correlation was present following stimulations above the pain threshold These findings suggest that vertex potentials elicited by electrical skin s h m u h may reflect central processing of non-noxious afferent information rather than of pare-related information

Key words Afferent fibers, Electrical stimuli. Pain. Vertex potentials

Vertex potentials evoked by painful stlmuh have been proposed as a neurophyslologlcal correlate of pain Although the neuronal generator(s) of vertex potentials are unknown, they have been proposed to reflect secondary processing of afferent information, such as stimulus recognition and magnitude estimation (Bromm 1985) Although correlatmn between vertex potential a m p h t u d e s and a range of electrical stimulation intensities evoking both non-painful and painful cutaneous sensations has been reported (Bromm et al 1983), it is unknown whether this correlation is present both in the pre-paln and In the pain range We therefore decided to investigate the possible relation between peak-to-peak amplitudes of the vertex potentml and the subjective ratings of non-painful and painful electrical cutaneous stimuli Methods and matermls

After informed consent 10 healthy non-medicated male volunteers, 21-28 years of age, p a r t l o p a t e d m the study, which was approved by the Mumcipal Ethical Committee of C o p e n h a g e n All subjects participated in two identical experimental sessmns separated by an interval of not less than 1 week Constant current square wave stimuli of 0 1 or 1 0 msec duration (DISA, Neuromatlc 2000C, D e n m a r k ) were delivered through an intracutaneous electrode, corlslstmg of a stainless steel pin 1 m m in diameter and 1 m m in length m o u n t e d on a polycarbonate base A small groove was prepared In the pulp of the third right finger with a dental burr The groove was made deeper until a 0 1 m A (1 0 msec) stimulus was perceived by the subject Care was taken to avoid damage of the c o n u m A n indifferent ring electrode was placed at the base of the same finger

Correspondence to Jannlck Brennum, M D , Laboratory of Senspry Physiology, Dept of Neurology, Gentofte Hospital, DK-2900 Hellerup (Denmark) Tel 4531651200. ext 6207, Fax 4531650802

Subjects rated stlmuh on a 6-point scale 0 = no sensation. 1 = slight sensation, 2 = distinct sensation, 3 = shght pam. 4 = moderate pain, and 5 = strong pain Vertex potentials were built by on-hne averaging of twenty 500 msec post-stimulus electroencephalogram (EEG) segments recorded monopolarly between vertex and left earlobe (DISA N e u r o m a h c 2000C, bandpass 0 5 - 1 0 0 Hz ( - 3 dB)) Registrations were performed in a quiet room at 2 0 + I°C Subjects were supine and focused on markers m the ceiling to minimize electrooculogram artifacts At the beginning and end of each day the subjects rated 10 intensities of 0 1 msec stimuli (0 5 - 5 0 mA, 0 5 m A increments) and 10 intensities of 1 0 msec stimuli (0 15-1 5 mA, 0 15 m A increments), each appearing 3 times in randomized order with randomized time intervals (10-15 sec) Pain thresholds were calculated as the m e a n intensity rated as slight pain (3) by the subJeCt Vertex potentials were evoked by 6 intensities of 0 1 msec electrical stimuli (0 5, 1, 2, 3, 4 and 5 m A ) and 6 lntenslhes of 1 0 msec stlmuh (0 12, 0 25, 0 5. 0 75, 1 0 and 1 5 m A ) Stlmuh were apphed in randomized order and with randomized time intervals (10-15 sec) Three seconds after each stimulus subjects were asked for a rating according to the 6-point scale SLX stimulation blocks, which lasted approximately 7 ram, were separated by 5 mln intervals m which the subject was encouraged to walk about, in order to avoid drowsiness Peak-to-peak amplitudes (P1-N1 N1-P2, P2-N2) and peak lateno e s of these 4 major components were measured In order to minimize variation between subjects, peak-to-peak a m p h t u d e s were calculated as percentages of the subjects' m e a n peak-to-peak amplitudes for all stimulation intensities This standardization procedure was performed separately for each stimulus d u r a t m n and examination day Ratings were averaged across identical stimuli for each sublect The correlation between peak-to-peak amplitudes and ratings of non-painful (ratings < 3) and painful stimuli (ratings /> 3) and the correlation between ratings and stimulation intensities were analyzed separately with Kendall's rank correlation analysis F n e d m a n n ' s analysis of variance was used for investigation of intensity-related

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VERTEX POTENTIALS AND PAIN was a significant correlation between ratings and mtensltmS of nonpainful as well as painful stimuli, with both stimulus durations ( P < 0 01 for all correlations)

Vertex potentials The P1, N1, and P2 vertex potential components were identified in all sweeps whereas the N2 component was only recognmed in 60% of the sweeps, equally represented following non-painful and painful stlmuh (Fig 1) There was a significant correlation between peak-topeak amplitudes and ratings of non-painful stimuli (P < 0 01 for 11 out of 12 correlations) except for the P2-N2 amphtude on the second day with 1 0 msec stimulus duration ( P = 0 06) In contrast there was no correlation between peak-to-peak amphtudes and ratings of painful stimuli ( P > 0 1) (Figs 2 and 3), except for the N1-P2 amplitude on the first day with 1 0 msec stimulus duration (P < 0 05) Peak latencles were slmdar for 0 1 msec stlmuh and 1 0 msec stimuli and did not vary s~gntficantly with the stimulation intensity (median peak latencles P1 93 msec, N1 147 msec, P2 275 msec, N2 393 msec)

Discussion

The main finding of this study was a significant correlation between vertex potential amplitude and magnitude rating of nonpainful stimuli, whereas generally no correlation was observed between vertex potential amplitude and rating of painful stlmuh A mmdar celhng effect of potentials evoked by median nerve stimulation was observed by Uttal and Cook (1964) The failure to see a correlation between vertex potential amplitude and magnitude rating of painful stimuli could be due to several factors Firstly, it Is possible that the stimulus-reduced variations in the pare range were too small We consider this posslblhty less likely since the highest stimulus intensity was more than twice the pain detection threshold which is comparable to intensmes used in other studies (Bromr0 ~nd Scharem 1982, Boulu et al 1985) Secondly, it is possible that mtermdlvldual variation in pain detection threshold could play a role In the present study there were only minor variations between subjects m the stimulus intensity necessary to evoke pain Thirdly, tt is possible that long-term habituation could play a role m the lack of relationship between vertex potential amplitude and magmtude rating in the pain range Although this possibility cannot be dismissed, we consider it less likely since habituation would be expected to affect all stimulation intensities equally and would therefore not change the relationship between vertex potential amplitude and magnitude rating Taken together, the present findings suggest that there is no correlation between vertex potential peak-to-peak amplitude and pare intensity evoked by electrical cutaneous stimuli This notion is supported by studies of Boulu et al (1985) and Davis et al (1980) Bromm et al (1983) reported a significant correlation between vertex potential amplitude and pain rating evoked by mtracutaneous electrical stlmuh However, the correlation analysis was based on a mixture of painful and non-painful stimuli Bromm et al (1983) concluded that pain relief may be estimated by measuring the amplitude of vertex potentials, based on the observation that tdldme, an oplold, depressed the vertex potential and pain rating in parallel The graphs presented in that study (Bromm et al 1983) demonstrate that all vertex potentials were depressed, whether evoked by painful or non-pamful stimuli Similar effects of oplolds on electrically evoked vertex potentmls may be found In two other studies (Davis et al 1980, Buchsbaum et al 1981) Opmtes change both the vigilance level and attention as well as the frequency composmon of the EEG (Kunkel 1984), all factors that are known to have an influence on the amplitude of vertex potentials (Bromm and Scharem 1982, Mdtner et al 1989), which might explain the observed depression of vertex potential amphtudes Thus, the available data apparently do not support the conclusion that depresmon of vertex potentml amplitude reflects pain relief

389 Since A/3 fibers are activated at lower stimulation intensities than the slower conducting A8 and C fibers, an alteranon m the shape of the vertex potential above the pain detection threshold would be expected with the appearance of additional late components if pare-related activity were reflected m the vertex potentml However, we observed no difference m the configuration of the vertex potentml whether evoked by non-painful or painful stlmuh, nor have we found reports of such changes m the literature Vertex potential amphtudes decrease when the lntersttmulus interval is decreased below 10 sec (Chapman et al 1981, Wilier et al 1985) Furthermore Bromm and Treede (1987) noted that It was only possible to record ultralate EP components related to C fiber activity when faster conducting fibers were blocked by compression Thus, the vertex potential has a short absolute refractory period and a following l't~latlve refractory period of approximately 10 sec Since the afferent barrage in A3 fibers reaches the central nervous system only shortly after the afferent barrage m A/3 fibers It seems hkely that only actmty in the fastest conducting fibers (Aft) is represented m the vertex potential Observations of vertex potentials with normal configuration evoked by electrical stlmuh in a patient with congenital msensltlvlty to pain (Chatnan et al 1975) and in patients with impaired pain and temperature sense (Halhday and Wakefield 1963) further indicate that vertex potentials evoked by electrical stimuli reflects neuronal actmty which may not be considered as specifically related to painful afferent information This study has been supported by grants from Wacherhausens Foundation, the Danish Medical Research Council, the NOVO Foundation and the Lundbeck Foundation

References

Boulu, P , De Broucker, T , Maitre, P , Memer, S and Wdler, J °C Potentml 6voqu~ somesth6slque et douleur I Etude des r6ponses cort~cales tardwes obtenues par dlff6rents nweaux de stimulation Rev E E G Neurophyslol, 1985, 15 19-25 Bromm, B Evoked cerebral potential and pain In H L Fields et al (Eds), Advances in Pain Research and Therapy. Vol 9 Raven Press, New York, 1985 305-329 Bromm, B and Schareln, E Principal component analysis of pare-related cerebral potentials to mechanical and electrical stimulation in man Electroencph chn Neurophyslol, 1982, 53 94-103 Bromm, B and Treede, R D Pain related cerebral potentials late and ultralate components Int J Neuroscl, 1987, 33 15-23 Bromm, B, Meier, W and Schareln, E Antagonism between tihdme and naloxone on cerebral potentials and pain ratings in man Eur J Pharmacol, 1983, 87 431-439 Buchsbaum, M S, Davis, G C , Coppola, R and Naber, P Opiate pharmacology and mdmdual differences II Somatosensory evoked potentials Pain, 1981, 10 367-377 Chapman, C R , Colpltts, Y H , Mayeno, J K and Gaghardl, G J Rate of stimulus repetition changes evoked potential amplitude dental and auditory modahtles compared Exp Brain Res, 1981, 43 246-252 Chatnan, G E , Farrell, D F , Canfield, R C and Lettlch, E Congenital msensltwlty to noxaous stlmuh Arch Neurol, 1975, 32 141-145 Cruccu, G , Fornarelh, M , Inghfllerl, M and Manfredl, M The hmlts of tooth pulp evoked potentmls for pain quantification Physlol Behav, 1983, 31 339-342 Davis, C G , Buchsbaum, M S, Naber, D and Kammen, D P Effect of opiates and opiate antagonists on somatosensory evoked potenUals m patients with schizophrenia and normal adults Adv BIol Psychtat, 1980, 4 73-80 Halllday, A M and Wakefield, G S Cerebral evoked potentmls in patients with dissociated sensory loss J Neurol Neurosurg Psychlat, 1963, 26 211-219

390 Kunkel, H Pharmaco-electroencephalography Methods and problems In B Bromm (Ed), Pare Measurement m Man Neurophysiological Correlates of Pare Elsevier, Amsterdam, 1984 153-166 Mdtner, W , Johnson, R , Braun, C and Larblg, W Somatosensory event-related potentials to painful and non-painful stimuli effects of stimulation Pam, 1989, 38 303-312

J BRENNUM, T S JENSEN Uttal, W R and Cook, L Systemat~cs of the evoked somatosensory cortical potential a psychophyslcal-electrophys~cal comparison Ann NYAcad Scl, 1964, 112 60-80 Wdler, J -C, Meumer, S, Maitre, P , De Broucker, T and Boulu, P Potentlel 6voqu6 et douleur II Etude comparatwe des sensations subjectwes, des composants tardwes du potenUel cortical et des vol~es aff~rentes Rev E E G Neurophyslol, 1985, 15 27-36

Relationship between vertex potentials and magnitude of pre-pain and pain sensations evoked by electrical skin stimuli.

Vertex potentials evoked by painful and non-painful electrical skin stimuli were recorded in 10 healthy male volunteers. Peak-to-peak amplitudes of th...
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