- Email: [email protected]
The second exteroceptive suppression is affected by psychophysiological factors
Journal of Psychosomatic Research 66 (2009) 521 – 529
The second exteroceptive suppression is affected by psychophysiological factors Thomas Forkmann a,⁎, Marco Heins b , Timon Bruns b , Walter Paulus c , Birgit Kröner-Herwig b b
a Institute of Medical Psychology and Medical Sociology, University Hospital of RWTH Aachen University, Aachen, Germany Department for Clinical Psychology and Psychotherapy, Institute of Psychology, University of Göttingen, Göttingen, Germany c Department of Clinical Neurophysiology, Medical Faculty, University of Göttingen, Göttingen, Germany
Received 7 April 2008; received in revised form 18 November 2008; accepted 16 December 2008
Abstract Objective: The second exteroceptive suppression (ES2) is assumed to be an indicator of central antinociceptive processing, although some conflicting data have been produced. We examined the impact of experimentally induced psychophysiological conditions on the latency and duration of the ES2. Also, the association to the subjective evaluation of the painful electrical stimulation by which the ES2 is elicited was studied. Methods: ES2 was assessed in 46 healthy volunteers running through four experimentally induced psychophysiological conditions: stress, relaxation, depressed mood, and heterotopic pressure pain. Conditions were presented in a repeated measure design in permuted sequences. Ten stimulation-recording sequences per condition were averaged. ES2
parameters were compared to a baseline condition and correlated to subjective pain perception. Results: ES2 duration was found to be prolonged and ES2 latency to be shortened under the impact of relaxation and depressed mood. The subjective perception of the painful electrical stimulation was affected by the experimental conditions. Conclusion: Data lend support to the hypothesis that the repeatedly observed limited stability of ES2 parameters might be caused by the variability of individual psychophysiological states. Against expectation, subjective pain perception is not systematically correlated with ES2 parameters. Thus it can be questioned whether the ES2 is directly associated with pain processing at all. © 2009 Elsevier Inc. All rights reserved.
Keywords: Depressive mood; Exteroceptive suppression; Heterotopic pressure pain; Psychophysiological state; Relaxation; Stress
Introduction In chronic pain syndromes, e.g., chronic tension-type headache (cTTH), dysfunction of central antinociceptive processing has been discussed as a potential underlying pathophysiological process [1–3]. The second exteroceptive suppression (ES2) of the activity of the M. masseter or M. temporalis has been considered as possibly indicating abnormalities in central pain processing [3–5]. The ES2 is a transitory suppression of the voluntary electromyographic (EMG) activity of the M. masseter or M. temporalis after painful stimulation of the mental nerve [6]. A significantly ⁎ Corresponding author. Institute of Medical Psychology and Medical Sociology, University Hospital of RWTH Aachen University, Pauwelsstraße 30, 52074 Aachen, Germany. Tel.: +49 241 8089003; fax: +49 241 80 33 89003. E-mail address: [email protected] (T. Forkmann). 0022-3999/08/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.jpsychores.2008.12.008
shortened ES2 in patients suffering from cTTH has repeatedly been found and has been interpreted as indicating reduced antinociceptive activity at brainstem level [7–11]. Thus, it has been hypothesized that cTTH as other chronic pain syndromes is at least partly caused or accompanied by abnormalities in central antinociceptive processing and that ES2 duration can be seen as a peripheral marker of this processing [3–5]. Other studies failed to find the expected abnormalities and thus weakened the above conclusions [8,12–14]. Regarding latency of the ES2, until now no systematic findings have been reported. These conflicting results suggest that the ES2 might be subject to influences not systematically assessed, yet. Especially, since the ES2 is mediated via a multisynaptic neuronal net in the brainstem and receives inputs from various brain structures [15,16], it should be receptive to varying psychophysiological conditions in the individual.
522
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
So far, most studies only correlated an organismic variable (e.g., being afflicted by cTTH) to the ES2. However, only an experimental design systematically manipulating psychophysiological states in healthy persons establishes a methodologically sound empirical basis for the interpretation that ES2 is subject to psychophysiologically different states. The modulation of the ES2 by experimentally changing the psychophysiological state of the individual, however, has rarely been studied yet [17]. The current study aimed at the examination of the impact of four experimentally induced psychophysiological states (“stress”, “relaxation”, “depressed mood”, and “heterotopic pressure pain”) on latency and duration of the ES2 in healthy volunteers. These conditions are known to influence the experience of clinical and acute pain [18–23]. We expected ES2 to vary between the different psychophysiological states. Furthermore, ES2 parameters (latency and duration) were expected to correlate with the subjective experience of the painful electrical stimulation within the ES2 assessment procedure. If ES2 can be viewed as a peripheral marker of central antinociceptive processing, then the subjective perception of the pain eliciting the ES2 should be related to ES2 parameters.
Methods Sample Sixty-eight voluntary subjects (graduate and postgraduate students) were recruited within university and gave their informed consent to participate when invited to an informative session. Participants were either paid for their participation (€10) or received credit needed for their degree course. Eleven subjects had to be excluded because of at least one of the following criteria: (a) chronic tensiontype headache, (b) bruxism, (c) migraine, (d) intake of psychotropic drugs, or (e) depression. Criteria (a)–(d) were assessed via self-report. Depression was examined prior to the experimental session using the ADS-K [24], the German version of the Center for Epidemiological Studies Depression Scale. Subjects with a score N23 were not approved for participation. Ten participants did not show any ES2 during the experimental session and thus could not be included into data analysis [8,25]. One person cancelled the recording session. Hence, data analysis was based on the remaining 46 healthy subjects (31 females and 15 males). The participants' mean age was 24.2 years (S.D.=4.7; range=20 to 43 years). The study procedures were in accordance with the Declaration of Helsinki from 1989. Design In a repeated measure design, four treatment conditions inducing different psychophysiological states were realized.
A baseline condition (standard assessment procedure of ES2) served as a comparison. The following psychophysiological states were induced by experimental procedures: stress, relaxation, depressed mood, and heterotopic pressure pain (see also Fig. 1 for details). Treatment conditions Depressed mood Depressed mood was induced via a method developed by Velten [26]; in addition, a piece of music with a gloomy, saddening character was presented via earphones [27]. During the Velten mood induction procedure, 40 selfrelated negative cognitions are presented on a screen one by one with an interval of 10 s. Subjects were requested to read the sentences aloud and to try to get themselves into the mood evoked by the music. The Velten mood induction procedure took 5 min and 30 s. Afterwards, the music continued while ES2 was recorded. Immediately after ES2 recording, participants rated intensity and unpleasantness of the labial stimulation on two visual analogue scales (VAS) ranging from 0 (no pain) to 10 (greatest imaginable pain), and from 0 (not unpleasant at all) to 10 (extremely unpleasant), respectively. A manipulation check questionnaire (MDBF) [28] was filled in by participants immediately after ES2 recording. Heterotopic pressure pain Heterotopic pain was applied to the ring finger of the right hand using a pressure algometer. Participants' hand was positioned on a plate beneath a lever arm of the algometer. Pain was induced by a spike (diameter: 2 mm) fixed at the lever arm which was automatically lowered upon the tip of the participant's finger and rested there for 105 s with a pressure of 3.09 N (1217 kPa) [29]. Five seconds after the onset of the pressure pain stimulus (the spike resting on the finger tip), the ES2 recording was started. After completion of ES2 recording, the lever arm lifted automatically, and subjects immediately rated intensity and unpleasantness of the pressure pain and of the labial stimulation on separate VAS ranging from 0 (no pain) to 10 (greatest imaginable pain), and from 0 (not unpleasant at all) to 10 (extremely unpleasant), respectively. Stress Stress was induced via a counting task based on the Trier Social Stress Test (TSST) [30]. Counting tasks are a common means to provoke stress [31,32]. Subjects were asked to count backwards from 1022 in steps of 13. During the first 2 min of counting, the experimenter instructed the subjects to “go faster please!” and fed back “wrong!” twice (in random order via a talk-back circuit) in order to increase the stress level. The second component of stress induction of the TSST (public speech in front of a live audience) was not implemented because it was not compatible with the experimental setup (not leaving the lab
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
523
Fig. 1. Schematic illustration of the timing of the ES2 recording procedure (A) and each treatment condition (B).
and staying connected to the monitoring devices). However, subjects were supplementary told that their performance and facial expression during the counting task would be judged via a monitoring camera. Monitoring cameras are known to function as “threat” that increases stress [33,34]. After 2 min of counting aloud, the subjects had to proceed counting mentally while ES2 recording was conducted. Immediately after completion of ES2 recording, the subjects rated the level of perceived stressfulness of the task on a VAS ranging from 0 (not stressful at all) to 10 (greatest imaginable stress). Afterwards, intensity and unpleasantness of the labial stimulation were rated on a VAS and the MDBF was filled in.
Relaxation A guided imagery technique was used to induce relaxation [35]. Instructions described a sunlit seaside scenery, the sensation of warm sand, and the sound of incoming waves. Accompanied by soft music, the instructions covered 3 min and 47 s. ES2 recording started immediately afterwards. While the ES2 recording was carried out, the music continued for an additional 1.5 min. After completion of ES2 recording, the subjects immediately rated the level of achieved relaxation on a VAS ranging from 0 (not at all) to 10 (greatest imaginable relaxation). Intensity and unpleasantness of the labial stimulation were then immediately rated on a VAS and the MDBF was filled in.
524
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
Manipulation check In addition to the different VAS, the Multidimensional Well-Being Questionnaire (MDBF) was given for manipulation check purposes assessing the actual state of wellbeing [28]. It asked subjects to indicate their level of agreement with a list of items describing psychophysiological states (e.g., tense, relaxed, tired) on a scale ranging from 1 (not agreeing at all) to 5 (very much agreeing). Scores were calculated for two scales (positive–negative mood; calmness–tenseness), with higher scores indicating a more positive mood or being more calm, respectively. Scales were constituted by different items [28]. The MDBF was filled in at the end of the informative session, after the ES2 recording following the baseline, the mood, stress, and relaxation condition, and at the very end of the experiment. Mean scores of the MDBF calmness–agitation scale at the informative session, baseline, and end of experiment were compared to the scores related to the stress and relaxation conditions. Mean scores of the MDBF mood scale at the informative session, baseline, and end of experiment were compared to the score related to the depressed mood condition. Dependent variables Latency and duration of ES2 Recording of the EMG activity of the M. temporalis was conducted using self-adhesive disposable Ag/AgCl electrodes with a diameter of 5 mm, impregnated with electrode gel. The recording and stimulation device was a DELL OptiPlex GXi combined with the software Neuroscreen, version 1.63. The affixing of the recording
electrodes followed prior published recommendations [36]. The left temporalis muscle was palpated near the hairline during maximal voluntary jaw closing and the site was cleaned with alcohol. A ground electrode was attached to the left wrist. The recording parameters were determined as follows: sensitivity, 400 μV/division; filter, 20–3000 Hz. To elicit the ES2, the labial commissure of the participant was electrically stimulated with an intensity of 20 mA and an impulse length of 200 μs that after pretests was expected to be slightly painful. Ten stimuli per recording session were applied with a frequency of 0.1 Hz [37]. The two poles of the stimulation electrode with a diameter of 3 mm each were attached to the ipsilateral labial commissure with a distance of 7 mm. The EMG signal was rectified. Ten stimulation-recording sequences per assessment were performed and averaged. The recording started 30 ms after each stimulation and ended 120 ms after each stimulation (Fig. 1). To determine the latency and duration of the ES2, the specification of the onset and offset of EMG suppression is crucial. Two strategies are reported in the literature: (1) ES2 is defined as the period where 80% of the baseline EMG activity is suppressed [37]. Although this criterion is widely used, serious difficulties have been reported. Particularly, artificially augmented suppression periods have been described when applying this criterion [38]. (2) In several studies, a standardized visual analysis procedure has been adopted instead [39,40]. In the present study, the latter method was applied. A list of visual criteria to determine the onsets and offsets of the ES2 were applied, which were geared to morphological characteristics of the EMG curves and in accordance with the procedures deployed in previous studies (see Fig. 2).
Fig. 2. Exemplary illustration of a typical ES2 curve and the applied criteria (1–5) to determine ES2 onset and offset.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
1. Within the second phase of visible EMG suppression, the point of the EMG curve with the same distance to the preceding and subsequent period with visible EMG activity had to be determined. 2. Starting there, the lowest point after the clearly visible decrement of the facilitation period marks the onset of the ES2. 3. The offset of the ES2 is the lowest point of the EMG curve preceding the clearly visible reset of muscle activity. 4. The onset and the offset of the ES2 had to be on approximately similar EMG levels. 5. Peaks within the suppression period of less than 5 ms duration were ignored [38]. 6. Peaks within the suppression period of more than 5 ms duration had to be considered for determining the onsets and offsets of the ES2, respectively. All recorded EMG curves were evaluated by two independent judges. Interjudge agreement was high (kappa=.972). In case of disagreement of more than 1 ms between the two judges, a third judge evaluated the EMG curves and ES2 onsets and offsets were determined by the decision of the majority. Potentially interfering variables According to previous research, intake of nicotine and caffeine, age, sex, and time of testing were considered to possibly influence ES2 parameters [3,25,41,42]. Therefore, subjects were advised to abstain from nicotine and caffeine for at least 1 h and from alcohol for at least 12 h prior to the experimental session. At the day of the experimental session, subjects were requested to report how long they actually had abstained from intake of these substances. Data on time since last intake as well as age, gender, and time of testing were controlled statistically prior to ES2 analysis. Procedure An informative session took place at least 1 day before the experimental session. All subjects were asked to fill in the MDBF. A questionnaire was given to assess the potentially interfering variables and check the exclusion criteria. If any of them was identified, the subjects were informed immediately that they were not eligible to participate. The experimental session was conducted in a sound-proof room where the subjects were seated in a comfortable chair. The experimenter controlled and supervised the progression of the experiment from outside. After a period of 2 min during which subjects could habituate to the experimental room, baseline ES2 recording was performed. Subjects were asked via headphone to clench their teeth maximally and to relax their jaw muscles alternately with an interval of 10 s. These intervals were visually signaled to the subjects. Ten trials were performed. Electrical stimulation of the labial
525
commissure to elicit ES2 was accomplished 4 s after teeth clenching started. EMG activity during maximal teeth clenching 30 ms before and 120 ms after electrical stimulation was recorded. After completion of baseline ES2 recording, participants were asked to immediately fill in the VAS assessing the intensity and unpleasantness of the painful labial stimulation and the MDBF. This procedure was identical for all induced psychophysiological conditions. The timing of the different treatment conditions is visualized in Fig. 1. The sequence of the experimental conditions except the baseline condition was counterbalanced. However, “stress” always preceded “relaxation” because the stress response was expected to spread to the following condition if not counteracted by relaxation. Counterbalancing resulted in six orders with baseline assessment always constituting the first recording period: (1) baseline, stress, relaxation, mood, pain; (2) b, s, r, p, m; (3) b, p, m, s, r; (4) b, m, s, r, p; (5) b, p, s, r, m; (6) b, m, p, s, r. Data analysis Student's t tests (PN.05) were used to compare the ES2 parameters as well as the subjective ratings recorded in the four treatment conditions to baseline. The impact of the potentially interfering variables (caffeine and alcohol, age, gender, and time of testing) was assessed using analyses of covariance (COVA). All analyses were carried out using SPSS 12.0.1 for Windows. Results Potentially interfering variables To test the effects of caffeine, alcohol, age, gender, and time of testing, a COVA for repeated measures was computed for each variable. None of them indicated a significant impact on ES2 parameters (PN.05). There were no differences between the six sequences of conditions in the dependent variables (PN.05). Manipulation check The MDBF subscale “positive–negative mood” after the induction of depressed mood was compared to the following three periods via t test: end of the informative session, baseline, and end of the experimental session. As expected, mean scores were significantly larger in all control measures indicating that “negative mood” was more pronounced after the induction of depressive mood (Pb.001). The three control periods did not differ significantly (PN.11; see Table 1). To test for the successful induction of stress and relaxation, the MDBF subscale “calmness–agitation/arousal” was used. Mean score was expected to be highest during the relaxation condition and lowest in the stress
526
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
Table 1 Manipulation check: ratings of the experimental condition “depressed mood” on the subscale “positive–negative mood” of the MDBF in comparison to control periods Comparisons
t
df
P
Depressed mood–IS Depressed mood–baseline Depressed mood–ES IS–Baseline IS–ES Baseline—ES
−6.204 −5.219 −7.467 2.660 .929 −2.273
46 46 45 46 45 45
b.001 ⁎⁎ b.001 ⁎⁎ b.001 ⁎⁎ .110 .358 .028 ⁎
IS: informative session; ES: end of experimental session. ⁎ αb.05. ⁎⁎ αb.01.
condition with baseline values in between. T tests for paired samples demonstrated that subjects reported to be significantly less aroused in the relaxation condition than under stress (Pb.001). However, the comparisons between baseline and stress/relaxation did not differ significantly (PN.10; see Table 2). Duration and latency of the ES2 Latency and duration of ES2 during treatment conditions were compared to baseline via t test. A significantly shorter latency and a longer duration were obtained during the relaxed state (tlatency=−4.6, df=43, Pb.01; tduration=2.5, df=43, P=.02) and depressed mood (tlatency=−3.7, df=45, Pb.01; tduration=2.4, df=45, P=.02) than during the baseline condition. There were no significant differences between mean latency and duration of the ES2 obtained during stress (tlatency=−1.5, df=43, P=.15; tduration=−1.6, df=44, P=.13) and heterotopic pressure pain (tlatency=−2.0, df=43, P=.06; tduration=0.3, df=43, P=.79) compared to baseline (see Fig. 3). Perception of electrical stimulation The perception of the electrical stimulation of the labial commissure (pain intensity/pain unpleasantness) was also affected by the variation of experimental conditions. Under stress, subjects reported pain as being significantly less intense (t=2.8, df=46, Pb.01) and less unpleasant (t=4.3, df=46, Pb.01) than under baseline conditions. During relaxation, perceived pain intensity did not change significantly (t= −.65, df=45, P=.52), while pain unpleasantness declined (t=2.5, df=45, Pb.05). Furthermore, pain was stated as being more intense when subjects' mood was depressed (t=−3.4, df=46, Pb.01), whereas pain unpleasantness did not change significantly (t=.48, df=46, P=.63). Compared to baseline, subjects perceived the labial stimulation as significantly less unpleasant when the heterotopic pressure pain stimulus was presented concomitantly (t=2.6, df=46, Pb.05), while pain intensity remained stable (t=−.67, df=46, P=.51; see Fig. 3). Pain intensity and pain unpleasantness correlated significantly in all experimental conditions (.57brb.76). Under
the influence of heterotopic pressure pain, ES2 duration showed a significant negative correlation with the rated unpleasantness of the heterotopic pressure pain stimulus (r= −.32; Pb.05). No significant correlations regarding perceived intensity or unpleasantness of the painful labial stimulation with the dependent variables duration and latency of the ES2 were found (PN.30). Discussion The objective of the present study was to examine the impact of the variation of psychophysiological states (stress, relaxation, depressed mood, heterotopic pressure pain) on latency and duration of the ES2 in an experimental design. Moreover, the relationship of the subjective evaluation of the perception of the labial stimulation with the ES2 parameters was studied. It was shown that the induction of depressed mood as well as the induction of relaxation resulted in a prolongation of the duration of ES2. Latency was significantly reduced under both conditions. The induction of stress and heterotopic pressure pain tended to augment latency and to shorten duration of ES2, but both effects failed to reach significance. Thus, treatment conditions clearly affected ES2. Although an experimental analysis of psychological state effects so far had not been carried out, these results somehow agree with earlier research on the link between ES2 and psychological variables. Wang et al. [43] for example found that aggression as a trait variable correlates with ES2 duration: ES2 duration was reduced in persons with high aggression scores. Dawans et al. [44] found ES2 to be shortened in five subjects with major depression (MD). Experimentally induced depressed mood thus appears to exert an influence on ES2 other than that of MD. However, all results must be viewed with caution because of absent replications and small samples. Unexpectedly, a successful induction of stress and relaxation could not be fully confirmed as there were no significant differences in the subjective level of perceived stress and relaxation, respectively, compared to baseline ratings. It is assumed that the impact of stress on ES2 parameters would have been more prominent if the induction procedures had resulted in a more distinct change in the psychophysiological state.
Table 2 Manipulation check: ratings on the subscale “calmness - agitation” of the MDBF of the experimental conditions “stress” and “relaxation” in comparison to baseline Comparisons
t
df
P
Baseline–stress Baseline–relaxation Stress–relaxation
1.2 −1.7 −3.88
46 45 45
.235 .096 b.001 ⁎
⁎ αb.01.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
527
Fig. 3. Latency and duration of ES2 and perceived intensity and unpleasantness of electrical labial stimulation separated by experimental condition. ⁎⁎Significant at α≤.01; ⁎significant at α≤.05.
ES2 was expected to correlate with subjective pain perception of the eliciting stimulation to warrant its interpretation as a marker of central antinociceptive processing. However, in the present study, duration and latency of ES2 did not correlate with subjective perception of the labial stimulation (pain intensity/pain unpleasantness). Hansen et al. [45] supposed that ES2 is mediated by nociceptive and nonnociceptive fibers converging on central interneurons, an assumption further supported by our results. This leads to the conclusion that ES2 may be not essentially related to pain processing [45]. The impact of psychophysiological states on ES2 suggests that descending inhibitory control pathways may be triggered by stress tasks or heterotopic pressure pain and that depressed mood or relaxation may result in a downregulation of these pathways [3]. The lack of systematic linkage of the ES2 parameters duration and latency to the experience of pain might be seen to principally endanger the theory that ES2 reflects generically important central mechanisms of pain processing. The assumption that antinociceptive processing at brainstem level is not or only in part represented by the ES2 cannot fully be refuted [46]. To summarize, the present study supports the expectation that duration and latency of the ES2 reflex are
influenced by the prevailing psychophysiological state of the individual. Thus, the repeatedly observed limited stability of ES2 parameters can at least partly be attributed to the variability of individual psychological states that were not controlled in prior studies. However, as subjective pain perception is not systematically correlated to ES2 parameters across the different experimental conditions, the question must be posed whether ES2 is directly associated with central pain processing at all. Contradicting results from other studies regarding especially tension-type headache add to this uncertainty. Future studies are needed to further examine and replicate our results demonstrating the dependence of ES2 on psychophysiological states. Also, an incorporation of clinical samples seems worthwhile to test whether this experimental procedure leads to valid information regarding mechanisms in the processing of acute and chronic pain. Acknowledgments The authors would like to thank Dr. Antonia Barke for her helpful comments on this paper and Dr. Peter Breuer for his technical support in conducting the study.
528
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
References [1] Banic B, Petersen-Felix S, Andersen OK, Radanov BP, Villiger PM, Nielsen L-A, et al. Evidence of spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004; 107:7–15. [2] Katsarava Z, Giffin NJ, Diener H-C, Kaube H. Abnormal habituation of nociceptive blink reflex in migraine - evidence for increased excitability of trigeminal nociception. Cephalalgia 2003; 23:814–9. [3] Schoenen J. Exteroceptive suppression of temporalis muscle activity in patients with chronic headache and in normal volunteers: Methodology, clinical and pathophysiological relevance. Headache 1993;33: 3–17. [4] Ebinger F. Exteroceptive suppression of masseter muscle activity in juvenile migraineurs. Cephalalgia 2006;26:722–30. [5] Keidel M, Rieschke P, Stude P, Eisentraut R, van Schayck R, Diener H-C. Antinociceptive reflex alteration in acute posttraumatic headache following whiplash injury. Pain 2001;92:319–26. [6] Schoenen J. Exteroceptive silent periods of temporalis muscle in headache. EMG of jaw reflexes in man. In: Van Steenberghe D, De Laat A, editors. EMG of jaw reflexes in man. Leuven: University Press, 1989. p. 357–68. [7] Nakashima K, Takahashi K. Exteroceptive suppression of the masseter, temporalis and trapezius muscles produced by mental nerve stimulation in patients with chronic headaches. Cephalalgia 1991;11:23–8. [8] Paulus W, Raubüchl O, Straube A, Schoenen J. Exteroceptive suppression of temporalis muscle activity in various types of headache. Headache 1992;32:41–4. [9] Schoenen J, Jamart B, Gerard P, Lenarduzzi P, Delwaide PJ. Exteroceptive suppression of temporalis muscle activity in chronic headache. Neurology 1987;37:1834–6. [10] Schoenen J. Tension-type headache: Pathophysiological evidence for a disturbance of “limbic” pathways to the brainstem. Headache 1990;30: 314–5. [11] Wallasch T-M, Lindner V, Soyka D. Temporalis-inhibitory reflex in the assessment of the functional state of the pain control system in chronic headache sufferers. Headache Q 1992;3:431–3. [12] Bendtsen L, Jensen R, Brennum J, Arendt-Nielsen L, Olesen J. Exteroceptive suppression of temporalis muscle activity is normal in chronic tension-type headache and not related to actual headache state. Cephalalgia 1996;16:251–6. [13] Lipchik GL, Holroyd KA, France CR, Kvaal SA, Segal D, Cordingley GE, et al. Central and peripheral mechanisms in chronic tension-type headache. Pain 1996;64:467–75. [14] Tataroglu C, Kanik A, Sahin G, Özge A, Yalcinkaya D, Idiman F. Exteroceptive suppression patterns of masseter and temporalis muscles in central and peripheral headache disorders. Cephalalgia 2002;22: 444–52. [15] Andersen RK, Lund JP, Puil E. Excitation and inhibition of neurons in the trigeminal nucleus caudalis following periaqueductal gray stimulation. Can J Physiol Pharmacol 1978;56:157–61. [16] Godaux E, Desmedt JE. Exteroceptive suppression and motor control of masseter and temporalis muscles in normal man. Brain Res 1975;85: 447–58. [17] Wallasch T-M, Niemann U, Kropp P, Weinschütz T. Exteroceptive silent periods of temporalis muscle activity: Correlation with neuropsychological findings. Headache 1993;33:121–4. [18] al'Absi M, Petersena KL. Blood pressure but not cortisol mediates stress effects on subsequent pain perception in healthy men and women. Pain 2003;106:285–95. [19] Janke EA, Holroyd KA, Romanek K. Depression increases onset of tension-type headache following laboratory stress. Pain 2004;111: 230–8. [20] Jones DA, Rollman GB, Brooke RI. The cortisol response to psychological stress in temporomandibular dysfunction. Pain 1997; 72:171–82.
[21] Lampe A, Söllner W, Krismer M, Rumpold G, Kantner-Rumplmair W, Ogon M, et al. The impact of stressful life events on exacerbation of chronic low-back pain. J Psychosom Res 1998;44:555–63. [22] Lanteri-Minet M, Radat F, Chautard MH, Lucas C. Anxiety and depression associated with migraine: influence on migraine subject's disability and quality of life, and acute migraine management. Pain 2005;118:319–26. [23] Petzke F, Harris RE, Williams DA, Clauw DJ, Gracely RH. Differences in unpleasantness induced by experimental pressure pain between patients with fibromyalgia and healthy controls. Eur J Pain 2005;9: 325–35. [24] Hautzinger M, Bailer M. Allgemeine Depressionsskala: ADS. Göttingen: Beltz-Test, 1993. [25] Zwart J-A, Sand T. Exteroceptive suppression of temporalis muscle activity: A blind study of tension-type headache, migraine and cervicogenic headache. Headache 1995;35:338–43. [26] Velten EJ. A laboratory task for induction of mood states. Behav Res Ther 1968;6:473–82. [27] Spies K, Hesse FW, Gerrards-Hesse A, Ueffing E. Experimentelle Induktion emotionaler Zustände - Verbessert die zusätzliche Darbietung von Musik die Wirksamkeit selbstbezogener Aussagen? Z Exp Angew Psychol 1991;38:321–42. [28] Steyer R, Schwenkmezger P, Notz P, Eid M. Der Mehrdimensionale Befindlichkeitsfragebogen (MDBF). Göttingen: Hogrefe, 1997. [29] Göbel H, Westphal W. Experimentelle Schmerzinduktion im algesimetrischen Humanversuch. Schmerz 1989;3:85–93. [30] Kirschbaum C, Pirke K-M, Hellhammer DH. The “Trier Social Stress Test” — a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993;28:76–81. [31] Soufer R, Bremner JD, Arrighi JA, Cohen I, Zaret BL, Burg MM, et al. Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease. Proc Natl Acad Sci U S A 1998; 95:6454–9. [32] Noto Y, Sato T, Kudo M, Kurata K, Hirota K. The relationship between salivary biomarkers and state-trait anxiety inventory score under mental arithmetic stress: a pilot study. Anesth Analg 2005;101: 1873–6. [33] Childs E, Vicini LM, de Wit H. Responses to the Trier Social Stress Test (TSST) in single versus grouped participants. Psychophysiology 2006;43:366–71. [34] Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 2004;130:355–91. [35] Techniker Krankenkasse. Progressive Muskelentspannung: Ausgeglichen durch den Alltag. Hamburg: TK, 2005. [36] Cram JR, Kasman GS, Holtz J. Introduction to surface electromyography. Gaithersburg: Aspen, 1998. [37] Göbel H, Schoenen J. Exteroceptive suppression in headache research. Discussion summary. Cephalalgia 1993;13:20. [38] Raubüchl O. Exterozeptive Suppression der Temporalismuskelaktivität bei verschiedenen Kopfschmerzformen (Dissertation). Munich: Ludwig-Maximilians-University, 1992. [39] Bär KJ, Greiner W, Letsch A, Köbele R, Sauer H. Influence of gender and hemispheric lateralization on heat pain perception in major depression. J Psychiatr Res 2003;37:345–53. [40] Hansen PO, Svensson P, Arendt-Nielsen L, Jensen TS. Human masseter inhibitory reflexes evoked by repetitive electrical stimulation. Clin Neurophysiol 2002;113:236–42. [41] Göbel H, Dworschak M, Kropp P, Heinze A, Heuss D. Die exterozeptive Suppression der Aktivität des M. temporalis in der Analyse von Schmerzmechanismen. Schmerz 1996;10:121–9. [42] Komiyama O, Wang K, Svensson P, Arendt-Nielsen L, De Laat A. Gender difference in masseteric exteroceptive suppression period and pain perception. Clin Neurophysiol 2005;116:2599–605. [43] Wang W, Sun G, Ye X, Shen M, Zhu R, Xu Y. Exteroceptive suppression of temporalis muscle activity in subjects with high and low aggression traits. Neurophysiol Clin 2006;36:63–9.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529 [44] Dawans A, Schoenen J, Timsit M, Timsit-Berthier M. Correlative study of psychopathological features and temporalis second exteroceptive silent period in chronic tension-type headache. Cephalalgia 1991;11:310–1. [45] Hansen PO, Svensson P, Arendt-Nielson L, Jensen TS. Relation between perceived stimulus intensity and exteroceptive reflex
529
responses in the human masseter muscles. Clin Neurophysiol 1999; 110:1290–6. [46] Hansen PO, Svensson P, Nielsen J, Arendt-Nielsen L, Jensen TS. Exteroceptive suppression of masseter muscle: assessment of two methods for quantitating suppression periods. Acta Neurol Scand 1998;97:204–13.
The second exteroceptive suppression is affected by psychophysiological factors Thomas Forkmann a,⁎, Marco Heins b , Timon Bruns b , Walter Paulus c , Birgit Kröner-Herwig b b
a Institute of Medical Psychology and Medical Sociology, University Hospital of RWTH Aachen University, Aachen, Germany Department for Clinical Psychology and Psychotherapy, Institute of Psychology, University of Göttingen, Göttingen, Germany c Department of Clinical Neurophysiology, Medical Faculty, University of Göttingen, Göttingen, Germany
Received 7 April 2008; received in revised form 18 November 2008; accepted 16 December 2008
Abstract Objective: The second exteroceptive suppression (ES2) is assumed to be an indicator of central antinociceptive processing, although some conflicting data have been produced. We examined the impact of experimentally induced psychophysiological conditions on the latency and duration of the ES2. Also, the association to the subjective evaluation of the painful electrical stimulation by which the ES2 is elicited was studied. Methods: ES2 was assessed in 46 healthy volunteers running through four experimentally induced psychophysiological conditions: stress, relaxation, depressed mood, and heterotopic pressure pain. Conditions were presented in a repeated measure design in permuted sequences. Ten stimulation-recording sequences per condition were averaged. ES2
parameters were compared to a baseline condition and correlated to subjective pain perception. Results: ES2 duration was found to be prolonged and ES2 latency to be shortened under the impact of relaxation and depressed mood. The subjective perception of the painful electrical stimulation was affected by the experimental conditions. Conclusion: Data lend support to the hypothesis that the repeatedly observed limited stability of ES2 parameters might be caused by the variability of individual psychophysiological states. Against expectation, subjective pain perception is not systematically correlated with ES2 parameters. Thus it can be questioned whether the ES2 is directly associated with pain processing at all. © 2009 Elsevier Inc. All rights reserved.
Keywords: Depressive mood; Exteroceptive suppression; Heterotopic pressure pain; Psychophysiological state; Relaxation; Stress
Introduction In chronic pain syndromes, e.g., chronic tension-type headache (cTTH), dysfunction of central antinociceptive processing has been discussed as a potential underlying pathophysiological process [1–3]. The second exteroceptive suppression (ES2) of the activity of the M. masseter or M. temporalis has been considered as possibly indicating abnormalities in central pain processing [3–5]. The ES2 is a transitory suppression of the voluntary electromyographic (EMG) activity of the M. masseter or M. temporalis after painful stimulation of the mental nerve [6]. A significantly ⁎ Corresponding author. Institute of Medical Psychology and Medical Sociology, University Hospital of RWTH Aachen University, Pauwelsstraße 30, 52074 Aachen, Germany. Tel.: +49 241 8089003; fax: +49 241 80 33 89003. E-mail address: [email protected] (T. Forkmann). 0022-3999/08/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.jpsychores.2008.12.008
shortened ES2 in patients suffering from cTTH has repeatedly been found and has been interpreted as indicating reduced antinociceptive activity at brainstem level [7–11]. Thus, it has been hypothesized that cTTH as other chronic pain syndromes is at least partly caused or accompanied by abnormalities in central antinociceptive processing and that ES2 duration can be seen as a peripheral marker of this processing [3–5]. Other studies failed to find the expected abnormalities and thus weakened the above conclusions [8,12–14]. Regarding latency of the ES2, until now no systematic findings have been reported. These conflicting results suggest that the ES2 might be subject to influences not systematically assessed, yet. Especially, since the ES2 is mediated via a multisynaptic neuronal net in the brainstem and receives inputs from various brain structures [15,16], it should be receptive to varying psychophysiological conditions in the individual.
522
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
So far, most studies only correlated an organismic variable (e.g., being afflicted by cTTH) to the ES2. However, only an experimental design systematically manipulating psychophysiological states in healthy persons establishes a methodologically sound empirical basis for the interpretation that ES2 is subject to psychophysiologically different states. The modulation of the ES2 by experimentally changing the psychophysiological state of the individual, however, has rarely been studied yet [17]. The current study aimed at the examination of the impact of four experimentally induced psychophysiological states (“stress”, “relaxation”, “depressed mood”, and “heterotopic pressure pain”) on latency and duration of the ES2 in healthy volunteers. These conditions are known to influence the experience of clinical and acute pain [18–23]. We expected ES2 to vary between the different psychophysiological states. Furthermore, ES2 parameters (latency and duration) were expected to correlate with the subjective experience of the painful electrical stimulation within the ES2 assessment procedure. If ES2 can be viewed as a peripheral marker of central antinociceptive processing, then the subjective perception of the pain eliciting the ES2 should be related to ES2 parameters.
Methods Sample Sixty-eight voluntary subjects (graduate and postgraduate students) were recruited within university and gave their informed consent to participate when invited to an informative session. Participants were either paid for their participation (€10) or received credit needed for their degree course. Eleven subjects had to be excluded because of at least one of the following criteria: (a) chronic tensiontype headache, (b) bruxism, (c) migraine, (d) intake of psychotropic drugs, or (e) depression. Criteria (a)–(d) were assessed via self-report. Depression was examined prior to the experimental session using the ADS-K [24], the German version of the Center for Epidemiological Studies Depression Scale. Subjects with a score N23 were not approved for participation. Ten participants did not show any ES2 during the experimental session and thus could not be included into data analysis [8,25]. One person cancelled the recording session. Hence, data analysis was based on the remaining 46 healthy subjects (31 females and 15 males). The participants' mean age was 24.2 years (S.D.=4.7; range=20 to 43 years). The study procedures were in accordance with the Declaration of Helsinki from 1989. Design In a repeated measure design, four treatment conditions inducing different psychophysiological states were realized.
A baseline condition (standard assessment procedure of ES2) served as a comparison. The following psychophysiological states were induced by experimental procedures: stress, relaxation, depressed mood, and heterotopic pressure pain (see also Fig. 1 for details). Treatment conditions Depressed mood Depressed mood was induced via a method developed by Velten [26]; in addition, a piece of music with a gloomy, saddening character was presented via earphones [27]. During the Velten mood induction procedure, 40 selfrelated negative cognitions are presented on a screen one by one with an interval of 10 s. Subjects were requested to read the sentences aloud and to try to get themselves into the mood evoked by the music. The Velten mood induction procedure took 5 min and 30 s. Afterwards, the music continued while ES2 was recorded. Immediately after ES2 recording, participants rated intensity and unpleasantness of the labial stimulation on two visual analogue scales (VAS) ranging from 0 (no pain) to 10 (greatest imaginable pain), and from 0 (not unpleasant at all) to 10 (extremely unpleasant), respectively. A manipulation check questionnaire (MDBF) [28] was filled in by participants immediately after ES2 recording. Heterotopic pressure pain Heterotopic pain was applied to the ring finger of the right hand using a pressure algometer. Participants' hand was positioned on a plate beneath a lever arm of the algometer. Pain was induced by a spike (diameter: 2 mm) fixed at the lever arm which was automatically lowered upon the tip of the participant's finger and rested there for 105 s with a pressure of 3.09 N (1217 kPa) [29]. Five seconds after the onset of the pressure pain stimulus (the spike resting on the finger tip), the ES2 recording was started. After completion of ES2 recording, the lever arm lifted automatically, and subjects immediately rated intensity and unpleasantness of the pressure pain and of the labial stimulation on separate VAS ranging from 0 (no pain) to 10 (greatest imaginable pain), and from 0 (not unpleasant at all) to 10 (extremely unpleasant), respectively. Stress Stress was induced via a counting task based on the Trier Social Stress Test (TSST) [30]. Counting tasks are a common means to provoke stress [31,32]. Subjects were asked to count backwards from 1022 in steps of 13. During the first 2 min of counting, the experimenter instructed the subjects to “go faster please!” and fed back “wrong!” twice (in random order via a talk-back circuit) in order to increase the stress level. The second component of stress induction of the TSST (public speech in front of a live audience) was not implemented because it was not compatible with the experimental setup (not leaving the lab
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
523
Fig. 1. Schematic illustration of the timing of the ES2 recording procedure (A) and each treatment condition (B).
and staying connected to the monitoring devices). However, subjects were supplementary told that their performance and facial expression during the counting task would be judged via a monitoring camera. Monitoring cameras are known to function as “threat” that increases stress [33,34]. After 2 min of counting aloud, the subjects had to proceed counting mentally while ES2 recording was conducted. Immediately after completion of ES2 recording, the subjects rated the level of perceived stressfulness of the task on a VAS ranging from 0 (not stressful at all) to 10 (greatest imaginable stress). Afterwards, intensity and unpleasantness of the labial stimulation were rated on a VAS and the MDBF was filled in.
Relaxation A guided imagery technique was used to induce relaxation [35]. Instructions described a sunlit seaside scenery, the sensation of warm sand, and the sound of incoming waves. Accompanied by soft music, the instructions covered 3 min and 47 s. ES2 recording started immediately afterwards. While the ES2 recording was carried out, the music continued for an additional 1.5 min. After completion of ES2 recording, the subjects immediately rated the level of achieved relaxation on a VAS ranging from 0 (not at all) to 10 (greatest imaginable relaxation). Intensity and unpleasantness of the labial stimulation were then immediately rated on a VAS and the MDBF was filled in.
524
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
Manipulation check In addition to the different VAS, the Multidimensional Well-Being Questionnaire (MDBF) was given for manipulation check purposes assessing the actual state of wellbeing [28]. It asked subjects to indicate their level of agreement with a list of items describing psychophysiological states (e.g., tense, relaxed, tired) on a scale ranging from 1 (not agreeing at all) to 5 (very much agreeing). Scores were calculated for two scales (positive–negative mood; calmness–tenseness), with higher scores indicating a more positive mood or being more calm, respectively. Scales were constituted by different items [28]. The MDBF was filled in at the end of the informative session, after the ES2 recording following the baseline, the mood, stress, and relaxation condition, and at the very end of the experiment. Mean scores of the MDBF calmness–agitation scale at the informative session, baseline, and end of experiment were compared to the scores related to the stress and relaxation conditions. Mean scores of the MDBF mood scale at the informative session, baseline, and end of experiment were compared to the score related to the depressed mood condition. Dependent variables Latency and duration of ES2 Recording of the EMG activity of the M. temporalis was conducted using self-adhesive disposable Ag/AgCl electrodes with a diameter of 5 mm, impregnated with electrode gel. The recording and stimulation device was a DELL OptiPlex GXi combined with the software Neuroscreen, version 1.63. The affixing of the recording
electrodes followed prior published recommendations [36]. The left temporalis muscle was palpated near the hairline during maximal voluntary jaw closing and the site was cleaned with alcohol. A ground electrode was attached to the left wrist. The recording parameters were determined as follows: sensitivity, 400 μV/division; filter, 20–3000 Hz. To elicit the ES2, the labial commissure of the participant was electrically stimulated with an intensity of 20 mA and an impulse length of 200 μs that after pretests was expected to be slightly painful. Ten stimuli per recording session were applied with a frequency of 0.1 Hz [37]. The two poles of the stimulation electrode with a diameter of 3 mm each were attached to the ipsilateral labial commissure with a distance of 7 mm. The EMG signal was rectified. Ten stimulation-recording sequences per assessment were performed and averaged. The recording started 30 ms after each stimulation and ended 120 ms after each stimulation (Fig. 1). To determine the latency and duration of the ES2, the specification of the onset and offset of EMG suppression is crucial. Two strategies are reported in the literature: (1) ES2 is defined as the period where 80% of the baseline EMG activity is suppressed [37]. Although this criterion is widely used, serious difficulties have been reported. Particularly, artificially augmented suppression periods have been described when applying this criterion [38]. (2) In several studies, a standardized visual analysis procedure has been adopted instead [39,40]. In the present study, the latter method was applied. A list of visual criteria to determine the onsets and offsets of the ES2 were applied, which were geared to morphological characteristics of the EMG curves and in accordance with the procedures deployed in previous studies (see Fig. 2).
Fig. 2. Exemplary illustration of a typical ES2 curve and the applied criteria (1–5) to determine ES2 onset and offset.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
1. Within the second phase of visible EMG suppression, the point of the EMG curve with the same distance to the preceding and subsequent period with visible EMG activity had to be determined. 2. Starting there, the lowest point after the clearly visible decrement of the facilitation period marks the onset of the ES2. 3. The offset of the ES2 is the lowest point of the EMG curve preceding the clearly visible reset of muscle activity. 4. The onset and the offset of the ES2 had to be on approximately similar EMG levels. 5. Peaks within the suppression period of less than 5 ms duration were ignored [38]. 6. Peaks within the suppression period of more than 5 ms duration had to be considered for determining the onsets and offsets of the ES2, respectively. All recorded EMG curves were evaluated by two independent judges. Interjudge agreement was high (kappa=.972). In case of disagreement of more than 1 ms between the two judges, a third judge evaluated the EMG curves and ES2 onsets and offsets were determined by the decision of the majority. Potentially interfering variables According to previous research, intake of nicotine and caffeine, age, sex, and time of testing were considered to possibly influence ES2 parameters [3,25,41,42]. Therefore, subjects were advised to abstain from nicotine and caffeine for at least 1 h and from alcohol for at least 12 h prior to the experimental session. At the day of the experimental session, subjects were requested to report how long they actually had abstained from intake of these substances. Data on time since last intake as well as age, gender, and time of testing were controlled statistically prior to ES2 analysis. Procedure An informative session took place at least 1 day before the experimental session. All subjects were asked to fill in the MDBF. A questionnaire was given to assess the potentially interfering variables and check the exclusion criteria. If any of them was identified, the subjects were informed immediately that they were not eligible to participate. The experimental session was conducted in a sound-proof room where the subjects were seated in a comfortable chair. The experimenter controlled and supervised the progression of the experiment from outside. After a period of 2 min during which subjects could habituate to the experimental room, baseline ES2 recording was performed. Subjects were asked via headphone to clench their teeth maximally and to relax their jaw muscles alternately with an interval of 10 s. These intervals were visually signaled to the subjects. Ten trials were performed. Electrical stimulation of the labial
525
commissure to elicit ES2 was accomplished 4 s after teeth clenching started. EMG activity during maximal teeth clenching 30 ms before and 120 ms after electrical stimulation was recorded. After completion of baseline ES2 recording, participants were asked to immediately fill in the VAS assessing the intensity and unpleasantness of the painful labial stimulation and the MDBF. This procedure was identical for all induced psychophysiological conditions. The timing of the different treatment conditions is visualized in Fig. 1. The sequence of the experimental conditions except the baseline condition was counterbalanced. However, “stress” always preceded “relaxation” because the stress response was expected to spread to the following condition if not counteracted by relaxation. Counterbalancing resulted in six orders with baseline assessment always constituting the first recording period: (1) baseline, stress, relaxation, mood, pain; (2) b, s, r, p, m; (3) b, p, m, s, r; (4) b, m, s, r, p; (5) b, p, s, r, m; (6) b, m, p, s, r. Data analysis Student's t tests (PN.05) were used to compare the ES2 parameters as well as the subjective ratings recorded in the four treatment conditions to baseline. The impact of the potentially interfering variables (caffeine and alcohol, age, gender, and time of testing) was assessed using analyses of covariance (COVA). All analyses were carried out using SPSS 12.0.1 for Windows. Results Potentially interfering variables To test the effects of caffeine, alcohol, age, gender, and time of testing, a COVA for repeated measures was computed for each variable. None of them indicated a significant impact on ES2 parameters (PN.05). There were no differences between the six sequences of conditions in the dependent variables (PN.05). Manipulation check The MDBF subscale “positive–negative mood” after the induction of depressed mood was compared to the following three periods via t test: end of the informative session, baseline, and end of the experimental session. As expected, mean scores were significantly larger in all control measures indicating that “negative mood” was more pronounced after the induction of depressive mood (Pb.001). The three control periods did not differ significantly (PN.11; see Table 1). To test for the successful induction of stress and relaxation, the MDBF subscale “calmness–agitation/arousal” was used. Mean score was expected to be highest during the relaxation condition and lowest in the stress
526
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
Table 1 Manipulation check: ratings of the experimental condition “depressed mood” on the subscale “positive–negative mood” of the MDBF in comparison to control periods Comparisons
t
df
P
Depressed mood–IS Depressed mood–baseline Depressed mood–ES IS–Baseline IS–ES Baseline—ES
−6.204 −5.219 −7.467 2.660 .929 −2.273
46 46 45 46 45 45
b.001 ⁎⁎ b.001 ⁎⁎ b.001 ⁎⁎ .110 .358 .028 ⁎
IS: informative session; ES: end of experimental session. ⁎ αb.05. ⁎⁎ αb.01.
condition with baseline values in between. T tests for paired samples demonstrated that subjects reported to be significantly less aroused in the relaxation condition than under stress (Pb.001). However, the comparisons between baseline and stress/relaxation did not differ significantly (PN.10; see Table 2). Duration and latency of the ES2 Latency and duration of ES2 during treatment conditions were compared to baseline via t test. A significantly shorter latency and a longer duration were obtained during the relaxed state (tlatency=−4.6, df=43, Pb.01; tduration=2.5, df=43, P=.02) and depressed mood (tlatency=−3.7, df=45, Pb.01; tduration=2.4, df=45, P=.02) than during the baseline condition. There were no significant differences between mean latency and duration of the ES2 obtained during stress (tlatency=−1.5, df=43, P=.15; tduration=−1.6, df=44, P=.13) and heterotopic pressure pain (tlatency=−2.0, df=43, P=.06; tduration=0.3, df=43, P=.79) compared to baseline (see Fig. 3). Perception of electrical stimulation The perception of the electrical stimulation of the labial commissure (pain intensity/pain unpleasantness) was also affected by the variation of experimental conditions. Under stress, subjects reported pain as being significantly less intense (t=2.8, df=46, Pb.01) and less unpleasant (t=4.3, df=46, Pb.01) than under baseline conditions. During relaxation, perceived pain intensity did not change significantly (t= −.65, df=45, P=.52), while pain unpleasantness declined (t=2.5, df=45, Pb.05). Furthermore, pain was stated as being more intense when subjects' mood was depressed (t=−3.4, df=46, Pb.01), whereas pain unpleasantness did not change significantly (t=.48, df=46, P=.63). Compared to baseline, subjects perceived the labial stimulation as significantly less unpleasant when the heterotopic pressure pain stimulus was presented concomitantly (t=2.6, df=46, Pb.05), while pain intensity remained stable (t=−.67, df=46, P=.51; see Fig. 3). Pain intensity and pain unpleasantness correlated significantly in all experimental conditions (.57brb.76). Under
the influence of heterotopic pressure pain, ES2 duration showed a significant negative correlation with the rated unpleasantness of the heterotopic pressure pain stimulus (r= −.32; Pb.05). No significant correlations regarding perceived intensity or unpleasantness of the painful labial stimulation with the dependent variables duration and latency of the ES2 were found (PN.30). Discussion The objective of the present study was to examine the impact of the variation of psychophysiological states (stress, relaxation, depressed mood, heterotopic pressure pain) on latency and duration of the ES2 in an experimental design. Moreover, the relationship of the subjective evaluation of the perception of the labial stimulation with the ES2 parameters was studied. It was shown that the induction of depressed mood as well as the induction of relaxation resulted in a prolongation of the duration of ES2. Latency was significantly reduced under both conditions. The induction of stress and heterotopic pressure pain tended to augment latency and to shorten duration of ES2, but both effects failed to reach significance. Thus, treatment conditions clearly affected ES2. Although an experimental analysis of psychological state effects so far had not been carried out, these results somehow agree with earlier research on the link between ES2 and psychological variables. Wang et al. [43] for example found that aggression as a trait variable correlates with ES2 duration: ES2 duration was reduced in persons with high aggression scores. Dawans et al. [44] found ES2 to be shortened in five subjects with major depression (MD). Experimentally induced depressed mood thus appears to exert an influence on ES2 other than that of MD. However, all results must be viewed with caution because of absent replications and small samples. Unexpectedly, a successful induction of stress and relaxation could not be fully confirmed as there were no significant differences in the subjective level of perceived stress and relaxation, respectively, compared to baseline ratings. It is assumed that the impact of stress on ES2 parameters would have been more prominent if the induction procedures had resulted in a more distinct change in the psychophysiological state.
Table 2 Manipulation check: ratings on the subscale “calmness - agitation” of the MDBF of the experimental conditions “stress” and “relaxation” in comparison to baseline Comparisons
t
df
P
Baseline–stress Baseline–relaxation Stress–relaxation
1.2 −1.7 −3.88
46 45 45
.235 .096 b.001 ⁎
⁎ αb.01.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
527
Fig. 3. Latency and duration of ES2 and perceived intensity and unpleasantness of electrical labial stimulation separated by experimental condition. ⁎⁎Significant at α≤.01; ⁎significant at α≤.05.
ES2 was expected to correlate with subjective pain perception of the eliciting stimulation to warrant its interpretation as a marker of central antinociceptive processing. However, in the present study, duration and latency of ES2 did not correlate with subjective perception of the labial stimulation (pain intensity/pain unpleasantness). Hansen et al. [45] supposed that ES2 is mediated by nociceptive and nonnociceptive fibers converging on central interneurons, an assumption further supported by our results. This leads to the conclusion that ES2 may be not essentially related to pain processing [45]. The impact of psychophysiological states on ES2 suggests that descending inhibitory control pathways may be triggered by stress tasks or heterotopic pressure pain and that depressed mood or relaxation may result in a downregulation of these pathways [3]. The lack of systematic linkage of the ES2 parameters duration and latency to the experience of pain might be seen to principally endanger the theory that ES2 reflects generically important central mechanisms of pain processing. The assumption that antinociceptive processing at brainstem level is not or only in part represented by the ES2 cannot fully be refuted [46]. To summarize, the present study supports the expectation that duration and latency of the ES2 reflex are
influenced by the prevailing psychophysiological state of the individual. Thus, the repeatedly observed limited stability of ES2 parameters can at least partly be attributed to the variability of individual psychological states that were not controlled in prior studies. However, as subjective pain perception is not systematically correlated to ES2 parameters across the different experimental conditions, the question must be posed whether ES2 is directly associated with central pain processing at all. Contradicting results from other studies regarding especially tension-type headache add to this uncertainty. Future studies are needed to further examine and replicate our results demonstrating the dependence of ES2 on psychophysiological states. Also, an incorporation of clinical samples seems worthwhile to test whether this experimental procedure leads to valid information regarding mechanisms in the processing of acute and chronic pain. Acknowledgments The authors would like to thank Dr. Antonia Barke for her helpful comments on this paper and Dr. Peter Breuer for his technical support in conducting the study.
528
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529
References [1] Banic B, Petersen-Felix S, Andersen OK, Radanov BP, Villiger PM, Nielsen L-A, et al. Evidence of spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004; 107:7–15. [2] Katsarava Z, Giffin NJ, Diener H-C, Kaube H. Abnormal habituation of nociceptive blink reflex in migraine - evidence for increased excitability of trigeminal nociception. Cephalalgia 2003; 23:814–9. [3] Schoenen J. Exteroceptive suppression of temporalis muscle activity in patients with chronic headache and in normal volunteers: Methodology, clinical and pathophysiological relevance. Headache 1993;33: 3–17. [4] Ebinger F. Exteroceptive suppression of masseter muscle activity in juvenile migraineurs. Cephalalgia 2006;26:722–30. [5] Keidel M, Rieschke P, Stude P, Eisentraut R, van Schayck R, Diener H-C. Antinociceptive reflex alteration in acute posttraumatic headache following whiplash injury. Pain 2001;92:319–26. [6] Schoenen J. Exteroceptive silent periods of temporalis muscle in headache. EMG of jaw reflexes in man. In: Van Steenberghe D, De Laat A, editors. EMG of jaw reflexes in man. Leuven: University Press, 1989. p. 357–68. [7] Nakashima K, Takahashi K. Exteroceptive suppression of the masseter, temporalis and trapezius muscles produced by mental nerve stimulation in patients with chronic headaches. Cephalalgia 1991;11:23–8. [8] Paulus W, Raubüchl O, Straube A, Schoenen J. Exteroceptive suppression of temporalis muscle activity in various types of headache. Headache 1992;32:41–4. [9] Schoenen J, Jamart B, Gerard P, Lenarduzzi P, Delwaide PJ. Exteroceptive suppression of temporalis muscle activity in chronic headache. Neurology 1987;37:1834–6. [10] Schoenen J. Tension-type headache: Pathophysiological evidence for a disturbance of “limbic” pathways to the brainstem. Headache 1990;30: 314–5. [11] Wallasch T-M, Lindner V, Soyka D. Temporalis-inhibitory reflex in the assessment of the functional state of the pain control system in chronic headache sufferers. Headache Q 1992;3:431–3. [12] Bendtsen L, Jensen R, Brennum J, Arendt-Nielsen L, Olesen J. Exteroceptive suppression of temporalis muscle activity is normal in chronic tension-type headache and not related to actual headache state. Cephalalgia 1996;16:251–6. [13] Lipchik GL, Holroyd KA, France CR, Kvaal SA, Segal D, Cordingley GE, et al. Central and peripheral mechanisms in chronic tension-type headache. Pain 1996;64:467–75. [14] Tataroglu C, Kanik A, Sahin G, Özge A, Yalcinkaya D, Idiman F. Exteroceptive suppression patterns of masseter and temporalis muscles in central and peripheral headache disorders. Cephalalgia 2002;22: 444–52. [15] Andersen RK, Lund JP, Puil E. Excitation and inhibition of neurons in the trigeminal nucleus caudalis following periaqueductal gray stimulation. Can J Physiol Pharmacol 1978;56:157–61. [16] Godaux E, Desmedt JE. Exteroceptive suppression and motor control of masseter and temporalis muscles in normal man. Brain Res 1975;85: 447–58. [17] Wallasch T-M, Niemann U, Kropp P, Weinschütz T. Exteroceptive silent periods of temporalis muscle activity: Correlation with neuropsychological findings. Headache 1993;33:121–4. [18] al'Absi M, Petersena KL. Blood pressure but not cortisol mediates stress effects on subsequent pain perception in healthy men and women. Pain 2003;106:285–95. [19] Janke EA, Holroyd KA, Romanek K. Depression increases onset of tension-type headache following laboratory stress. Pain 2004;111: 230–8. [20] Jones DA, Rollman GB, Brooke RI. The cortisol response to psychological stress in temporomandibular dysfunction. Pain 1997; 72:171–82.
[21] Lampe A, Söllner W, Krismer M, Rumpold G, Kantner-Rumplmair W, Ogon M, et al. The impact of stressful life events on exacerbation of chronic low-back pain. J Psychosom Res 1998;44:555–63. [22] Lanteri-Minet M, Radat F, Chautard MH, Lucas C. Anxiety and depression associated with migraine: influence on migraine subject's disability and quality of life, and acute migraine management. Pain 2005;118:319–26. [23] Petzke F, Harris RE, Williams DA, Clauw DJ, Gracely RH. Differences in unpleasantness induced by experimental pressure pain between patients with fibromyalgia and healthy controls. Eur J Pain 2005;9: 325–35. [24] Hautzinger M, Bailer M. Allgemeine Depressionsskala: ADS. Göttingen: Beltz-Test, 1993. [25] Zwart J-A, Sand T. Exteroceptive suppression of temporalis muscle activity: A blind study of tension-type headache, migraine and cervicogenic headache. Headache 1995;35:338–43. [26] Velten EJ. A laboratory task for induction of mood states. Behav Res Ther 1968;6:473–82. [27] Spies K, Hesse FW, Gerrards-Hesse A, Ueffing E. Experimentelle Induktion emotionaler Zustände - Verbessert die zusätzliche Darbietung von Musik die Wirksamkeit selbstbezogener Aussagen? Z Exp Angew Psychol 1991;38:321–42. [28] Steyer R, Schwenkmezger P, Notz P, Eid M. Der Mehrdimensionale Befindlichkeitsfragebogen (MDBF). Göttingen: Hogrefe, 1997. [29] Göbel H, Westphal W. Experimentelle Schmerzinduktion im algesimetrischen Humanversuch. Schmerz 1989;3:85–93. [30] Kirschbaum C, Pirke K-M, Hellhammer DH. The “Trier Social Stress Test” — a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993;28:76–81. [31] Soufer R, Bremner JD, Arrighi JA, Cohen I, Zaret BL, Burg MM, et al. Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease. Proc Natl Acad Sci U S A 1998; 95:6454–9. [32] Noto Y, Sato T, Kudo M, Kurata K, Hirota K. The relationship between salivary biomarkers and state-trait anxiety inventory score under mental arithmetic stress: a pilot study. Anesth Analg 2005;101: 1873–6. [33] Childs E, Vicini LM, de Wit H. Responses to the Trier Social Stress Test (TSST) in single versus grouped participants. Psychophysiology 2006;43:366–71. [34] Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 2004;130:355–91. [35] Techniker Krankenkasse. Progressive Muskelentspannung: Ausgeglichen durch den Alltag. Hamburg: TK, 2005. [36] Cram JR, Kasman GS, Holtz J. Introduction to surface electromyography. Gaithersburg: Aspen, 1998. [37] Göbel H, Schoenen J. Exteroceptive suppression in headache research. Discussion summary. Cephalalgia 1993;13:20. [38] Raubüchl O. Exterozeptive Suppression der Temporalismuskelaktivität bei verschiedenen Kopfschmerzformen (Dissertation). Munich: Ludwig-Maximilians-University, 1992. [39] Bär KJ, Greiner W, Letsch A, Köbele R, Sauer H. Influence of gender and hemispheric lateralization on heat pain perception in major depression. J Psychiatr Res 2003;37:345–53. [40] Hansen PO, Svensson P, Arendt-Nielsen L, Jensen TS. Human masseter inhibitory reflexes evoked by repetitive electrical stimulation. Clin Neurophysiol 2002;113:236–42. [41] Göbel H, Dworschak M, Kropp P, Heinze A, Heuss D. Die exterozeptive Suppression der Aktivität des M. temporalis in der Analyse von Schmerzmechanismen. Schmerz 1996;10:121–9. [42] Komiyama O, Wang K, Svensson P, Arendt-Nielsen L, De Laat A. Gender difference in masseteric exteroceptive suppression period and pain perception. Clin Neurophysiol 2005;116:2599–605. [43] Wang W, Sun G, Ye X, Shen M, Zhu R, Xu Y. Exteroceptive suppression of temporalis muscle activity in subjects with high and low aggression traits. Neurophysiol Clin 2006;36:63–9.
T. Forkmann et al. / Journal of Psychosomatic Research 66 (2009) 521–529 [44] Dawans A, Schoenen J, Timsit M, Timsit-Berthier M. Correlative study of psychopathological features and temporalis second exteroceptive silent period in chronic tension-type headache. Cephalalgia 1991;11:310–1. [45] Hansen PO, Svensson P, Arendt-Nielson L, Jensen TS. Relation between perceived stimulus intensity and exteroceptive reflex
529
responses in the human masseter muscles. Clin Neurophysiol 1999; 110:1290–6. [46] Hansen PO, Svensson P, Nielsen J, Arendt-Nielsen L, Jensen TS. Exteroceptive suppression of masseter muscle: assessment of two methods for quantitating suppression periods. Acta Neurol Scand 1998;97:204–13.