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ORIGINAL ARTICLES |
From the Department of Anesthesiology, Pain Clinic (M.K., N.R.-M., A.G.), the Department of Biometrics (L.H.), and the Department of Clinical Psychiatry and Psychotherapy (M.B., T.P.), Hannover Medical School, Hannover, Germany.
Address correspondence and reprint requests to Priv.-Doz. Dr. Matthias Karst, Hannover Medical School, Department of Anesthesiology, Pain Clinic, D-30625 Hannover, Germany. E-mail: karst.matthias{at}mh-hannover.de
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ABSTRACT |
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Methods: Responses to tactile stimulation were assessed in four groups of subjects (N = 40): patients with fibromyalgia, patients with somatoform pain disorder, patients with schizophrenia with auditory hallucinations and/or passivity experiences, and normal control subjects. The subjects were asked to rate the perception of a tactile sensation on their left and right hands. The tactile stimulation was either self-produced by movement of the subject's right or left hand or externally produced by the experimenter.
Results: Normal control subjects experienced self-produced stimuli as less intense than identical, externally produced tactile stimuli. In contrast, patients with fibromyalgia, patients with somatoform pain disorder, and patients with schizophrenia with auditory hallucinations and/or passivity experiences gave the same perceptual ratings for tactile stimuli produced by themselves as those produced by the experimenter (intergroup difference, p = .043; 95% confidence interval [CI], 0.16–0.68). Post hoc tests revealed that this significance was mainly caused by the fibromyalgia (p = .046; 95% CI, –1.66––0.13) and the somatoform pain disorder group (p = .033; 95% CI, –1.71––0.06).
Conclusions: We conclude that central pain disorders such as fibromyalgia and somatoform pain disorders interfere with the correct functioning of the self-monitoring mechanism that normally allows us to distinguish self-produced from externally produced tactile stimuli.
Key Words: fibromyalgia • somatoform pain disorder • schizophrenia • forward model • tickling
Abbreviations: FM = fibromyalgia; SPD = somatoform pain disorder; HP = hallucinations and/or passivity; NS = normal subjects; ACR = American College of Rheumatology; ICD = International Classification of Diseases; BPRS = Brief Psychiatric Rating Scale; SOMS = Screening for Somatoform Symptoms; DSM = Diagnostic and Statistical Manual of Mental Disorders; STAI = State-Trait-Anxiety Inventory; VAS = visual analog scale; SPS = self-produced tactile stimulus; EPS = externally produced tactile stimulus; ANOVA = one-way analysis of variance.
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INTRODUCTION |
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Blakemore et al. (6,7) and Weiskrantz et al. (8) have previously shown that normal subjects perceived self-produced tactile stimuli as less intense, less sensitive, and less pleasant than externally produced tactile stimuli. These results were interpreted in terms of sensory predictions made by a forward model of the motor system (9). Impairment in this self-monitoring forward model as part of a self-monitoring mechanism was observed in subjects with auditory hallucinations and passivity phenomena (HP) associated with schizophrenia (10), but not in patients with schizophrenia who do not have HP. It has been suggested that these abnormal experiences arise through a lack of awareness of intended actions and predicted limb position (11).
Patients with chronic pain often report abnormal tactile sensitivity in the affected area, varying from hypoesthesia to allodynia (12). Earlier studies have indicated that alterations in afferent input lead to cortical reorganization of the sensory maps corresponding to the affected area (13). However, very little is known about the possible effects of chronic widespread pain on central tactile processing in general and on the self-monitoring mechanism in particular.
It was suggested that chronic widespread pain may not only affect tactile thresholds, but also the self-monitoring mechanism. It has been hypothesized that this effect is more pronounced in disturbances of central nervous origin. Therefore, we have assumed that there is a spectrum in the abnormality of the self-monitoring mechanism, ranging from patients with acute schizophrenia and patients with SPD to patients with FM and normal subjects (NS).
We examined this hypothesized association by comparing patients with FM and those with SPD with patients with acute schizophrenia (with HP) and NS, testing whether they could distinguish the sensory consequences of their own actions from externally produced tactile stimulation.
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METHOD |
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The patients with FM had a clinical presentation and examination consistent with the American College of Rheumatology (ACR) criteria, including the presence of chronic widespread pain in at least three body quadrants, as well as the axial skeleton and 11 to 18 fibromyalgia (FM) tender points, located at the occipital and lower cervical area, trapezius and supraspinatus muscle, second costosternal junction, both lateral epicondyles, gluteus muscle, greater trochanteric area, and the medial fat pads of the knees (14).
The patients with SPD had a clinical presentation and examination consistent with the International Classification of Diseases, 10th revision (ICD-10) criteria (15) for somatoform pain disorder (F.45.4), including chronic widespread pain associated with psychologic factors that could not be explained by any organic pathology or pathophysiological mechanism (3). Patients with a typical FM pattern and distribution of tender points were not considered as patients with SPD, even though psychologic factors were important features of their symptomatology.
The patients with the diagnosis of schizophrenia who had had auditory hallucinations and/or passivity experiences within the prior 6 weeks were diagnosed by clinical interview (by M.B.) using the ICD-10 criteria (15).
Age-matched healthy volunteers (NS) as controls were recruited by two of the authors (A.G., M.B.). Any specific diseases or disorders were excluded by a comprehensive clinical interview.
All patients and normal subjects were also assessed with the Brief Psychiatric Rating Scale (BPRS). We used a short form of the BPRS consisting of 18 symptom constructs (somatic concern, anxiety, emotional withdrawal, conceptual disorganization, guilt feelings, tension, mannerisms and posturing, grandiosity, depressive mood, hostility, suspiciousness, hallucinatory behavior, motor retardation, uncooperativeness, unusual thought content, blunted affect, excitement, disorientation), each to be rated by trained clinicians (M.B., M.K.) on a seven-point scale of severity ranging from "not present" to "extremely severe" (16). Additionally, all patients and normal subjects completed the Screening for Somatoform Symptoms (SOMS). The SOMS includes all somatic symptoms relevant for somatization disorder according to the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV), as well as according to ICD-10. The questionnaire consisted of 53 somatization symptoms, each to be rated on a four-point scale of severity ranging from "not present" to "extremely severe" (17,18). Furthermore, all patients and normal subjects completed the State-Trait-Anxiety Inventory (STAI X1 for the current state of the individual in terms of the level of transitory anxiety at the time the questionnaire was completed and STAI X2 to measure the general level of background anxiety with which an individual operates in normal life) (19), the visual analog scale for anxiety (VAS, range 0–10; 0 = no anxiety, 10 = strongest anxiety) (with VAS-anxiety: 1 = level of anxiety before the first 8 measurements and VAS-anxiety: 2 = level of anxiety before the second eight measurements), and, when appropriate, the VAS for pain (range 0–10; 0 = no pain, 10 = strongest pain), and a questionnaire about their medication.
The study protocol was approved by the Institutional Review Board, and written informed consent was obtained from all patients and volunteers.
Procedure
The tactile stimulus device consisted of a hand-fixing device in which a plastic pointer can be moved on the palm of the left or right hands. Thus, the hand was put on a hand layer and was fixed between a palmar and a padded dorsal wall. In the palmar wall, the pointer was projected through a U-shaped slot in which it could be moved. The pointer had a spherical tip of 1 mm in diameter and was counterweighted with a spring in a plastic rod to maintain a constant pressure of approximately 17 g on the palm (Figures 1 and 2). Subjects sat facing the table with their left arm perpendicular to the table and the left hand in the apparatus with the palm fixed tightly to the plastic pointer. The rod with the plastic pointer at its end could either be moved by the subjects using the right hand or by the experimenter. To examine the palm of the right hand, the whole apparatus was rotated 180°. The movement followed the U-shaped form of the slot on the palm and took place once per second for 4 seconds. Movements were synchronized with the beat of a metronome. Each subject was given eight trials in which the two conditions (self-administration of the tactile sensation or tactile sensation by the experimenter) were presented successively on the same palm for 4 seconds. To control for a possible sequence effect throughout the 16 trials, the sequence of the two conditions was balanced.
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Statistical Analysis
Based on the expected differences (mean perceptual rating difference between self-produced [SPS] and externally produced tactile stimulation [EPS] conditions for the four subject groups: HP, 0.1; SPD, 0.3; FM, 0.5; NS, 0.5) between mean values, the sample size required to achieve 90% power was calculated as 40 subjects for the whole group, assuming that the common standard deviation is 2.50. The differences were expected from the results of Blakemore et al. (7), who found a mean perceptual rating difference between self-produced and externally produced tactile stimulation conditions of approximately 0.5 for the normal control subjects and patients with schizophrenia without symptoms, in contrast to less than 0.1 in patients with schizophrenia with specific symptoms (HP).
We calculated the mean differences (EPS-SPS) between the perceptual ratings for SPS and EPS. Statistical analyses used one-way analysis of variance (one-way ANOVA). To compare each group against the normal subject group (NS), the two-sided post hoc Dunnett t test was used, with the NS group as control. To test for between-subject effects in regard to different medication, univariate analysis of variance with covariates was used. Differences were regarded as significant with p < .05. Results are reported as means ± standard deviations.
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RESULTS |
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DISCUSSION |
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The baseline values of the clinically carefully characterized patient groups and the normal control subjects were well balanced with respect to age, gender, anxiety levels, and VAS-pain (FM and SPD group), giving a well-matched study population. Although there was a strong tendency to higher anxiety values in the HP group and the anxiety levels before the second eight measurements were significant higher (p = .006) than in the other groups, the differences in anxiety were not as marked as expected. This may be related to the trial setting, in which at least one of the investigators was almost always well known to the particular patient or volunteer.
The observed greater sensitivity in both the FM and the SPD groups than in the control group is concordant with the finding of hypersensitivity in such patient groups (4,5). Surprisingly, the pain disorder groups contributed more to the significantly reduced difference between the perceptual ratings for self-produced and externally produced stimuli than did the HP group, which argues against the spectrum theory mentioned in the "Introduction." Also surprisingly, there were essentially no differences in the results between the FM and SPD groups, which may be partly caused by the diagnostic overlap between the pain groups (see subsequently). The smaller difference in the perceptual rating differences in the HP group may be associated with a reduction in symptomatology by the treatment of current acute symptoms at the time of the investigation. This seems to correspond to the results of Blakemore et al. (10), who found that the presence of hallucinations and/or passivity experiences, and not the diagnosis "schizophrenia" itself, was associated with dysfunction of self-monitoring.
The limitations of the study are the small sample size in each group and the different distribution of medications across groups. However, if all medications or each medication had been included as additional covariates, no between-subject effects could have been calculated. Furthermore, antidepressants may reduce the perception of cutaneous stimulation (20). Although in our study a high proportion of patients in the pain groups took antidepressants, their ratings for cutaneous stimuli were 25% to 30% higher than the ratings of normal subjects. In addition, although each of the different compounds may impair the power of concentration, patients in the SPD and FM groups had been on stable doses for years, implying that acute cognitive impairment is unlikely. Another limitation of the study is the possibility of overlap between FM and SPD that could not have been totally ruled out by using the criteria mentioned here. Our patients with FM had an even higher score than the patients with SPD with respect to the SOMS scale, confirming that somatization is more common in patients with FM (21,22). An additional limitation may be seen in the lack of a control group with organically caused pain, in the traditional sense of the word, like cancer-related pain. However, although all patients with chronic pain specified their pain with the level of at least "modest to severe pain" (VAS 6–8), no one appeared to be obviously distressed during the tests. Therefore, we suggest that the observed effect is mainly caused by the central nervous dysfunction and not by spontaneous pain. This hypothesis is supported by functional imaging data, which indicated that a self-produced physical pain stimulus is modulated in a different way than a self-produced tactile stimulus (6,23).
We conclude that central pain disorders such as fibromyalgia and somatoform pain disorders interfere with the correct functioning of the self-monitoring mechanism, as defined by the work of Frith et al. (11). Results of the present study suggest that the amount of sensory attenuation after self-produced sensory stimuli decreases in patients who are chronically exposed to endogenous pain signals. It may be hypothesized that the attenuation of the ability to distinguish between internal and external stimuli may be caused by dedifferentiation of the highly complex psychophysiological feedback systems, equivalent to an earlier phylogenetic pattern of functioning. The neurophysiological background for this may be different activities of modulating cerebellar structures (6) that are probably more involved in acute (23–25) and chronic pain conditions than is usually recognized.
Future studies could combine the presented results with functional magnetic resonance imaging.
The authors thank Gabriele Huwald, RN (Pain Clinic, Hannover Medical School) for her skillful technical assistance and all patients and volunteers for their patient participation in this study.
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NOTES |
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DOI:10.1097/01.psy.0000146327.73705.9c
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