Royal National Hospital for Rheumatic Diseases in conjunction with the School for Health and Department of Pharmacy and Pharmacology, University of Bath, Bath, 1 Royal Devon and Exeter Hospital (Wonford), Exeter and 2 School of Psychology, University of Cardiff, Cardiff, UK.
Correspondence to: C. S. McCabe, Royal National Hospital for Rheumatic Diseases, Upper Borough Walls, Bath BA1 1RL, UK. E-mail: candy.mccabe{at}rnhrd-tr.swest.nhs.uk
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Abstract |
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Methods. Forty-one consecutively recruited healthy adult volunteers without a history of motor or proprioceptive disorders performed a series of bilateral upper and lower limb movements whilst viewing a mirror/whiteboard, which created varied degrees of sensorymotor conflict during congruent/incongruent limb movements. A qualitative method recorded any changes in sensory experience.
Results. Twenty-seven subjects (66%) reported at least one anomalous sensory symptom at some stage in the protocol despite no peripheral nociceptive input. The most frequent symptoms occurred when incongruent movement was performed whilst viewing the reflected limb in the mirror condition, the time of maximum sensorymotor conflict. Symptoms of pain were described as numbness, pins and needles, moderate aching and/or a definite pain. Other sensations included perceived changes in temperature, limb weight, altered body image and disorientation. There were indications that some individuals were more susceptible to symptom generation than others.
Conclusions. Our findings support the hypothesis that motorsensory conflict can induce pain and sensory disturbances in some normal individuals. We propose that prolonged sensorymotor conflict may induce long-term symptoms in some vulnerable subjects.
KEY WORDS: Pain, Sensory effects, Proprioception, Human information processing, Hypothesis, Experimental approach, Somatosensory system
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Introduction |
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Recent clinical and experimental work indicates that the central nervous system may be critical in generating a feedback-dependent state, which can produce pathological sensations in some patients independent of any initial peripheral pathology [111]. Central nervous systems that generate motor activity are closely coupled to sensory feedback systems and are monitored to detect deviations from that predicted [12]. Increased neuronal activity has been detected within the central nervous system, specifically in the right dorsolateral prefrontal cortex (RDPC), when incongruent information has been received from the periphery suggestive of a mismatch between intention, proprioception and visual feedback [13].
Amputation of a limb generates such an incongruent response, because after amputation the motor output still perceives the limb to be present, but proprioceptive and visual input is absent from the amputated area. Since postamputation pain is very common, it raises the possibility that such incongruent information processing may lead directly to pain. Should this hypothesis be correct, it might also explain conditions such as repetitive strain injury and complex regional pain syndrome. This would be the case if (i) they are sustained by incongruent feedback loops, and (ii) if such incongruence generates pain. Whilst others [14] and we have hypothesized this, direct evidence is lacking.
In this study we modified a test system that is known to activate the RDPC [14] to test our hypothesis that a motorsensory mismatch generates pain in healthy volunteers in the absence of injury or suggestion. Conflict between motor intention, proprioception and visual feedback was generated using bilateral coordination tasks of the upper and lower limbs and a mirror. We used a qualitative method to record the subjective experience of healthy volunteers whilst undergoing this task with particular reference to pain.
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Method |
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Clinical method
The assessment apparatus comprised a metal frame that supported a double-sided board; one side (the intervention side) had a mirror attached and the other (the control side) a whiteboard. The whiteboard was considered an appropriate control as it ensured the limb behind it was hidden from view (as when the mirror was used), but there was no reflective image from the visible limb and therefore sensory feedback was not being deliberately distorted. The board containing the mirror/whiteboard could be moved up or down a central supporting pillar and pivoted so that the mirror or whiteboard could be positioned on the left- or right-hand side. Its size was such that when it was positioned at the subject's midline one limb could be obscured from view (Fig. 1).
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Before assessment, the participants were asked to remove any identifying jewellery and articles of clothing on the parts of the limbs involved (e.g. watch, shoes, socks). This ensured that when the subject viewed the reflected image in the mirror it appeared similar to the hidden limb behind the apparatus. Subjects were seated on a couch, with the mirror/whiteboard in front of them positioned at right angles to the subject's body (Fig. 1). All subjects were requested to put one limb either side of the whiteboard until they were in a comfortable position but, critically, could not see the limb on the other side. For lower limb assessments the couch was raised so that the feet did not touch the floor to ensure that no additional sensory cues about their hidden limb's position could be gained, such as through touching the floor. A horizontal line was drawn on the mirror and whiteboard surfaces, which was level with the participant's umbilicus (upper limb assessment) or the great toe when the leg was fully extended and the ankle flexed (lower limb). A reference point on the subject's body was selected over one marked on the test apparatus to accommodate variation in height between subjects. All participants were asked to flex and extend both arms in a congruent manner from the elbow (or legs from the knees) whilst attending to the horizontal line on the whiteboard side for a timed 20-s period (Fig. 1A, E). Fink et al. [13] did not state the duration of movements in their protocol, but 20 s was chosen as an appropriate length of time as we were concerned that muscle fatigue may influence our findings with a longer period of exercise. Only the limb adjacent to the whiteboard could be seen throughout this assessment; the board hid the contralateral limb. The request to attend to a reference point on the whiteboard was included to ensure that attention was maintained during the short focused assessments, and that the same level of attention was employed during the control and intervention stages. At the end of the 20 s, subjects were asked to position both hands (or feet) level with the reference point in the horizontal plane and with palms (soles) downwards. As subjects were only able to view one limb, the hidden limb had to be placed at the same perceived height as the visible one. Subjects were then asked a series of open questions: How did that feel? followed by the further prompt Were you aware of any changes in either limb? No specific direct enquiry was made about possible sensory changes to prevent leading the subjects and inducing a possible source of bias. Where painful sensations were reported the subjects were asked to rate these on a verbal rating scale, where 0 = no pain and 10 = the worst possible pain. This scale is a modified Likert scale [17], which has been shown to reliably measure changes in pain [18]. A verbal rather than written scale was selected to minimize interruptions in the procedure and thereby aid the subject's concentration and recall skills.
The mirror/whiteboard was then pivoted so that the contralateral limb could be assessed in the same manner as above, and the procedure was repeated until the effect on each limb had been assessed whilst performing congruent and incongruent movements, first viewing the whiteboard and then the mirror. Upper and lower limb assessments were conducted consecutively and the order randomized between subjects.
Data analysis and management
Data analysis
Qualitative data, generated from the subjects responses to the open questions were tabulated in Microsoft Excel and analysed using content analysis [19, 20]. Subjects were each allocated a unique code and the responses to the open questions were typed against the individual's code under the relevant stage in the protocol. Colour coding was used to indicate categories and subcategories within emerging themes. The frequency of report of a particular sensation was totalled for each stage of the protocol. Quantitative data relating to the verbal rating scales for sensation severity were stored and analysed on SPSS. These were tabulated against each individual's code for the relevant stage in the protocol.
No formal statistical analysis was performed on this quantitative data as this was primarily a qualitative study and therefore not powered for statistical analysis.
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Results (Table 1) |
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Types of sensory changes reported
Discomfort to mild pain
The phenomenological descriptions included under this theme ranged from a tingly sensation and pins and needles to an ache, slight pain or shooting pain. During the control phases one subject (subject A) reported that they felt a light, tingling sensation in their left lower arm (right hand dominant) as they performed congruent and incongruent movements with their left arm hidden from view. When the mirror image of the limb was viewed, this tingly sensation was again described: Fairly quickly my left arm felt tingly from the fingertips to elbow (incongruent intervention, subject A) and I felt a tingling in my right hand (congruent intervention, subject B). An aching sensation was also describedI felt a slight achy feeling in my right arm (incongruent intervention, subject J)as was pins and needlesI had pins and needles in both feet (incongruent intervention, right lower limb hidden, subject C). Others reported a definite pain: I wanted to rest both legs as they felt ... slightly painful. (incongruent intervention, left lower limb hidden, subject D); There was a little bit of pain in my left hand, shooting down from the elbow (congruent intervention, subject D). All subjects quantified their pain as <2/10 on a verbal rating scale.
Temperature change
A change in temperature in the hidden limb was reported when incongruent movement was performed whilst subjects viewed the mirror image of one limb. One subject described their limbs becoming warmerboth hands felt quite hot (left upper limb hidden, subject D)and another coolermy right foot felt cold (subject B). The researcher found no obvious difference in temperature to touch.
Weight change
Subjects hidden limbs were perceived as either becoming heavier or lighter. When attention was focused on the whiteboard one subject reported that there was a bit of heaviness in both elbows (congruent control, left upper limb hidden, subject D) and another that the right hand felt a lot lighter (hidden limb, congruent control, subject B). When the mirror image of a limb was attended to, subject D still experienced the increased weight of their elbows (congruent intervention) and subject B now reported My right foot felt very light at the end of the exercise (congruent and incongruent intervention). This reduction in weight was also described as a slightly floaty sensation in my left arm (congruent intervention, subject E) and my right arm was floating so I was not sure precisely where it was (incongruent intervention, subject G). For one subject the perceived increase in weight of their hidden limb impeded their movement so that at the end of the exercise The left arm felt so heavy I was unable to lift it to the same height as the right (incongruent intervention, subject B).
Perceived loss of or additional limbs
The visual illusion created by the mirror of having one arm visible, one in the mirror and another concealed behind it produced in some subjects a feeling that they had lost a limb and others that they had a third one. The most distal end of the moving hidden limb was always affected when these sensations were experienced but the degree to which the remainder of the limb was involved varied between individuals. However, even during the control stages subjects reported a loss of sensation in the hidden limb. Subject A stated that they were less aware of the right hand (congruent control) and subject B had no idea where the right foot was (congruent control). The left foot felt as if it wasn't there from the mid-calf down (subject B, incongruent control). This loss of limb was so real to subject II had no idea where my left foot was (congruent control)that they had problems locating their foot when the exercise was complete and found it difficult to bring it to the reference mark.
When the mirror was viewed, this report of perceived loss of limb was described as took a second to find my right hand (congruent intervention, subject K), I had a delayed reaction to where my right hand was (congruent intervention, subject L), left arm was no longer present (incongruent intervention, subject E) and it took a second to find my right hand ... the left leg disappeared (incongruent movement, subject K). Normal perception of the affected area returned rapidly when the limb was either visualized or touched by the subject.
Conversely, some subjects experienced the perception of an additional limb: I felt I had three hands (incongruent intervention, subject M); I felt I had two right hands and my real one was drifting off (incongruent intervention, subject D), I feel I have three legs (incongruent intervention, subject N). Again, this illusion was quickly dismissed once movement stopped.
Feeling of peculiarity
This category encompasses the type of experience reported by most of the subjects in the functional imaging study by Fink et al. [13]. Subjects in our study often reported a range of feelings in the non-seen hand and there were such comments as a bit odd (control congruent, subject B) very weird (congruent intervention, subject C), disliked it (congruent intervention, subject K) and bizarre (congruent intervention, subject E).
For some the visual effect generated the illusion that the reflected image was moving at a different pace to their hidden limb: The leg in the mirror looks as if it is going slower because the real one is going in the opposite direction (incongruent intervention, subject G). Others found that the movement became mechanical (congruent intervention, subject I) and they had to really concentrate to keep the right leg moving in the opposite direction (incongruent intervention, subject A). Some experienced a loss of control (subject B) and their leg movements became wild (incongruent intervention). Nausea, confusion, dizziness and disorientation were also described (incongruent intervention, subjects A, O and P).
Frequency of report (Table 2)
Sensory changes were reported through all phases of the protocol: control (congruent movement n = 6, 15%; incongruent movement, n = 4, 10%) and intervention, but the maximum number of reports of anomalous sensations occurred when the subjects moved their limbs incongruently but perceived, via mirror, that they were moving them congruently (congruent movement, n = 17, 41%; incongruent movement, n = 27, 66%). No inferences can be drawn from the influence of hand dominance, as the majority were right-handed; only three out of the total study population (7.3%) left-handed. These three were scattered across the different vulnerability groups, one reporting sensations typical of the moderate group, one typical of the minimum and the third reporting no abnormal sensory disturbances.
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Discussion |
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The environment, the musculoskeletal system and sensory receptors all influence the transformation of motor commands to their sensory consequences [23]. These sensations in turn influence the subsequent motor commands. Therefore, a feed-forward and feedback system is constantly in action, and it is at the interaction between the twowhere actual sensory input meets the predicted sensory input, or efference copythat sensory disturbances may be generated (Fig. 2). Indeed, in most cases normal awareness and experience of our limb is often based on the predicted state rather than the actual state, unless that system monitoring the actual feedback detects a deviation from that predicted [12]. The consequence of this chain of actions is that sensory events are analysed in terms of the appropriate motor response.
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Wall [28] stated that the reason sensory events are analysed in terms of appropriate motor response is evolutionary, so that an individual can act promptly to any threat, seeking safety or preparing for action. We would propose that the capability to generate sensory abnormalities within this motor control system fits well within his theory. If one requirement of this system is to alert the individual to danger, then it must have a means to achieve this, and we know that pain can have a dramatic effect upon an individual's actions. We suggest that the milder sensory changes are an early warning system alerting the individual to abnormalities within information processing, but if these persist and the threat is perceived as greater, then ultimately pain will be produced. These monitoring mechanisms can be triggered by externally produced conflict (e.g. incongruent movement whilst viewing the mirror) or internally (e.g. the ageing process leading to inaccurate execution of movement and/or altered proprioception, or disease damage in RA [1] resulting in stiffness). Flor and colleagues have shown that phantom limb pain significantly positively correlates to the level of cortical reorganization [29], but when patients received feedback on sensory discrimination of the residual limb there was a dramatic reduction in pain and cortical reorganization [30]. This suggests that appropriate feedback can correct the mismatch and thereby reduce symptoms, as previously demonstrated in mirror visual feedback therapy for amputees [31] and those with CRPS [32].
In the case of CRPS we suggest that impaired efferent copies (either peripherally generated from protracted dysfunctional proprioceptive input or centrally altered) leads to a prediction that intended or attempted movements of the limb will result in pain. Since, as Frith et al. [12] have argued, much of our conscious awareness of limb movements is largely derived from the predicted rather than feedback from the peripheral joints themselves, the impaired efferent copy serves to activate brain mechanisms responsible for monitoring the effects of motor intention. These in turn generate a qualitatively altered perception (dysaesthesia, paraesthesia and pain) on the basis of the impaired efferent information, which is experienced and reported as an abnormal sensation by the patient.
The concept that a motorsensory mismatch gives rise to anomalous sensations including pain is new and thus far has found most of its evidence from the study of patients with chronic pain. The results of our study provide additional support for the concept in that many normal subjects (without clinical pathology) experienced a wide range of sensory disturbances, including localized pain, when exposed to transient motorsensory conflict. The speed with which these sensations were produced was surprising, considering the brief 20-s exposure, the majority occurring almost immediately limb movement started. Significantly, once normal visual input was restored, the anomalous sensations rapidly resolved.
The motor control system may be one of many such central monitoring mechanisms within the body. We have termed these ominory, from the Latin word ominor, meaning to prophesy, predict, foreboding [33]. Another ominory mechanism could generate motion sickness when there is discordance between body position, balance and equilibrium. The key feature of these mechanisms is that when they are triggered they generate sensory disturbances, such as nausea with motion sickness, pain in a phantom limb and a multitude of unpleasant sensations in CRPS. These resultant states we have termed dissensory, from the Latin word dissensio, meaning conflict, disagreement [33]. These are feedback-dependent states, which will continue to trigger the ominory mechanism; ultimately, either via duration or intensity of this state, the subject will suffer pain. However, not all our subjects experienced sensory disturbances. It would appear that innate susceptibility plays a part, with some individuals more vulnerable to, or perhaps simply better at detecting, these sensations. Perhaps those who are far more aware of changes in their bodies, and report recurrent multiple medical symptoms which have no organic cause, have a reduced threshold to these normal sensory changes, and start to report them as abnormal symptoms. This may explain the constant flitting of symptoms in those with fibromyalgia, who, like the healthy volunteers, describe changes in body schema, mild generalized pain and changes in body temperature [34, 35]. Further work is required to identify exactly what these individual influencing factors may be.
In conclusion, a mismatch between motor output and sensory input triggers a warning ominory mechanism based within the motor control system, which generates a dissensory state. In this state, the individual may experience a range of sensory disturbances, included within which may be pain.
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Acknowledgments |
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The authors have declared no conflicts of interest.
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References |
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