ORIGINAL ARTICLE

Mirror therapy for phantom limb pain: Brain changes and the role of body representation J. Foell1,2*, R. Bekrater-Bodmann1*, M. Diers1, H. Flor1 1 Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany 2 Department of Psychology, Florida State University, Tallahassee, USA

Correspondence Herta Flor E-mail: herta.fl[email protected] Funding sources This work was supported by the PHANTOM MIND project (Phantom phenomena: a window to the mind and the brain), which receives research funding from the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC Grant Agreement No. 230249, and by a subproject of the Collaborative Research Project ‘Bionic-Hand’ funded by the Bundesministerium für Bildung und Forschung (V4UKF02). This manuscript reflects only the authors’ views, and the Community is not liable for any use that may be made of the information contained therein. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the production of this manuscript. Conflicts of interest None declared.

Abstract Background: Phantom limb pain (PLP) is a common consequence of amputation and is difficult to treat. Mirror therapy (MT), a procedure utilizing the visual recreation of movement of a lost limb by moving the intact limb in front of a mirror, has been shown to be effective in reducing PLP. However, the neural correlates of this effect are not known. Methods: We investigated the effects of daily mirror training over 4 weeks in 13 chronic PLP patients after unilateral arm amputation. Eleven participants performed hand and lip movements during a functional magnetic resonance imaging (fMRI) measurement before and after MT. The location of neural activity in primary somatosensory cortex during these tasks was used to assess brain changes related to treatment. Results: The treatment caused a significant reduction of PLP (average decrease of 27%). Treatment effects were predicted by a telescopic distortion of the phantom, with those patients who experienced a telescope profiting less from treatment. fMRI data analyses revealed a relationship between change in pain after MT and a reversal of dysfunctional cortical reorganization in primary somatosensory cortex. Pain reduction after mirror training was also related to a decrease of activity in the inferior parietal cortex (IPC). Conclusions: Experienced body appearance seems to be an important predictor of mirror treatment effectiveness. Maladaptive changes in cortical organization are reversed during mirror treatment, which also alters activity in the IPC, a region involved in painful perceptions and in the perceived relatedness to an observed limb.

*These authors contributed equally to this work. Accepted for publication 6 November 2013 doi:10.1002/j.1532-2149.2013.00433.x

1. Introduction After the amputation of a limb, most patients report awareness of a phantom (Giummarra et al., 2007), i.e., the continuing perception of the missing limb, with or

without proportional distortions. Additionally, 60–90% (Jensen et al., 1983; Hanley et al., 2009) of amputees report phantom limb pain (PLP), a sensation of pain located in the amputated limb, which has a high rate of chronicity and is difficult to treat (Weeks

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Mirror therapy for phantom limb pain

What’s already known about this topic? • It is known that mirror therapy provides relief for some patients with chronic phantom limb pain. • We also know that the intensity of this pain is correlated with the extent of cortical reorganization in primary somatosensory cortex. What does this study add? • This study shows that the pain relief induced by mirror therapy is accompanied by a reversion of cortical reorganization, and that the treatment effect is dependent on properties of the phantom limb.

et al., 2010). Central changes have been proposed to contribute to PLP (Flor et al., 2006). Reorganization of somatosensory (cf. Flor et al., 1995; Birbaumer et al., 1997) and motor cortex (cf. Karl et al., 2001; Koppelstaetter et al., 2007) – e.g., the invasion of areas neighbouring the representation of the amputated limb into the cortical representation zone – was shown to be related to PLP intensity, suggesting that it may be related to this change after amputation (Flor et al., 2006). Since there is a strong influence of vision on the perception (Hunter et al., 2003) and movement (Brodie et al., 2003) of a phantom, the use of experimental set-ups inducing the illusion of two intact limbs might influence these central alterations (Ramachandran and Rogers-Ramachandran, 1996). When persons with PLP are asked to place their healthy limb in front of a mirror such that its reflection visually replaces the missing limb, this can result in pain alleviation in some patients. Chan et al. (2007) published a randomized placebo-controlled study showing significant PLP decrease with recently amputated leg amputees after 4 weeks of training. However, in subacute pain spontaneous recovery can occur (Schley et al., 2008), requiring a study of these effects in chronic patients. The mechanisms behind the mode of action of mirror therapy (MT) are not clear. One possible mechanism is the representational restitution of the missing limb in the brain (Foell et al., 2011) by the convergence of concurrent visual and proprioceptive input. Additionally, previous evidence indicates that an external object can be more easily integrated into one’s own body representation if there is a high degree of congruence between sensory modalities (Tsakiris, 2010). For example, deviations between the seen and felt position of an artificial limb impede the sensation

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of ownership (Lloyd, 2007). These results might be of significance in MT, as perceived distortions of the phantom might complicate the integration of visual and proprioceptive input into a coherent percept and reduce the effects of mirror treatment. This might be one factor why about 40% of the PLP patients do not benefit from MT (Weeks et al., 2010). The identification of predictors that influence the effectiveness of MT would help to understand the mechanism of this treatment and could improve its clinical use. This study was designed to (1) evaluate the effects of MT on pain in chronic PLP patients, (2) compare the brain changes related to treatment effects before and after therapy and (3) identify predictors of treatment success. Our hypotheses were (1) a subset of patients will benefit from MT, and (2) these patients will display an individual reduction of dysfunctional cortical shift, which will be stronger in patients with large treatment benefit.

2. Materials and methods 2.1 Patients The sample consisted of 13 patients with major unilateral upper limb amputation [four women, mean age 50.6, standard deviation (SD) = 15.8 years, range: 26–74 years] who experienced PLP regularly at least once a week with an average intensity of at least 20 on a visual analogue scale (VAS; ranging from 0 to 100) and who had been amputated for more than 2 years to rule out acute PLP (average time since amputation 21.3, SD = 12.7 years, range: 6–49 years). All subjects reported feeling a phantom limb. Supporting Information Table S1 provides information on all participants, including cause of amputation, prosthesis use, pain medication, PLP frequency and intensity, and the experience of telescoping. All participants gave written informed consent prior to taking part in the study, and the Ethics Committee of the Medical Faculty Mannheim of Heidelberg University approved the protocol, which adhered to the Declaration of Helsinki. Two patients were excluded from the functional magnetic resonance imaging (fMRI) measurements or analysis (due to a tattoo in one case and an incidental finding in anatomic images in another); thus, 11 patients were included in the brain imaging part of the study (four women, mean age 49.3 years, SD = 15.3, range: 26–68 years; average time between amputation and measurement 21.3 years, SD = 13.8, range: 6–49 years), whereas all 13 patients participated in the mirror treatment. PLP intensity as assessed by the German version of the West Haven-Yale Multidimensional Pain Inventory (MPI; Kerns et al., 1985; Flor et al., 1990; modified to separately assess phantom and residual limb pain) averaged 2.23 (SD = 0.72) for the entire group and 2.12 (SD = 0.70) for the fMRI subgroup. Twelve patients reported that they experienced non-painful phantom phenomena, such as a feeling of pressure or slight

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tingling, at least several times per week. The mean intensity for these sensations was 48.38 (SD = 26.58, range: 0–92) on VAS from 0 = no sensation to 100 = very intense sensation (fMRI subgroup: mean 46.27, SD = 26.09, range: 0–92). Patients experiencing a telescope (n = 8) reported a mean intensity of 80.0 (SD = 26.4, range: 23–100) for this sensation, measured using VAS, ranging from 0 = no telescope to 100 = very intense (fMRI subgroup: mean 89.50, SD = 9.01, range: 77–100). Over the course of the study, one patient (patient 1) used a steady amount of pain medication (a non-steroidal antiinflammatory drug) everyday for 8 weeks of the study. Three patients (3, 7 and 13) used analgesics occasionally, i.e., on 5 or fewer days spread over the entire 8 weeks of the study (patient 3: an opioid, patients 7 and 13: a non-steroidal anti-inflammatory drug).

2.2 Design Each patient gave daily reports of pain (using VAS) for a total of 8 weeks, commencing 2 weeks prior to therapy (prephase) to assess the baseline level of PLP, followed by a 4-week training phase with daily mirror exercises and concluding with 2 weeks without any treatment (but with daily pain ratings; post-phase) to evaluate possible long-term effects of the therapy. On the day before the first training unit as well as after the last one, the patients’ brain activation was assessed: Patients performed (1) mirrored hand movements and (2) a lip-pursing task during fMRI measurement (cf. Lotze et al., 2001; MacIver et al., 2008). During the same visit, patients were asked about the frequency, intensity and relieving factors for current and past PLP as well as current and past non-painful phantom sensations (including telescoping) using a structured interview (Winter et al., 2001). For everyday of the study (pre-phase, training phase and post-phase), patients were asked about any pain medication they were using.

2.3 Mirror training Patients received specific verbal and written instructions for 4-week mirror training during a one-on-one appointment prior to the training phase. Patients were instructed to try to consciously relate the movement observed in the mirror to their phantom at any point during the training and to keep their attention focused on the task. Each instruction was explained verbally, demonstrated by a therapist and performed by the patient in front of her or him. Patients then trained on their own everyday for a period of 4 weeks. Five different movement tasks were devised to improve patient compliance and to reduce the risk of straining. The tasks included (1) opening and closing of fingers: repeated converging of the fingertips, starting with a loosely opened hand, palm towards the mirror, but without any tactile contact among the fingers or between fingertips and palm; (2) stretching of fingers, with palm towards the mirror; (3) turning the hand, so that the palm alternately faced upwards

Mirror therapy for phantom limb pain

and downwards; (4) sequential converging of fingertips and thumb, palm towards the mirror, without actual contact between the fingertips; and (5) tracing figures with the index finger in the manner of a concert conductor. All these tasks were designed for maximum visibility of the movement while excluding any kind of tactile feedback. Patients were instructed to perform each task for 3 min (total: 15 min daily) and to record the actual amount of time they needed to perform each of the tasks on each day. Patients were advised to keep the frequency of the hand movements constant (at approximately 0.5 Hz), but this was not enforced; instead, patients were free to use the frequency that best enabled them to relate the observed movement to the movement of their phantom limb. They were instructed to abort any movement task if it intensified their pain level and to document if this happened. After explanation and demonstration of all tasks, the patients practiced the tasks themselves and received a detailed written explanation of the movement tasks including colour photographs. No patient reported a lack of understanding of or an inability to perform the mirrored movement task. Patients received a large transportable mirror (30 × 50 cm or 12 × 20 in.) and were required to give a daily report on the intensity of PLP on that day in general (on VAS with the endpoints ‘no pain’ and ‘very intense pain’, ranging from 0 to 100) and the occurrence and intensity of PLP during the training (on a scale from 0 for ‘none at all’ to 6 for ‘most intense pain ever experienced’, taken from the MPI; Flor et al., 1990). They were also asked daily about the degree to which they were able to relate the movement seen in the mirror to their phantom limb, on a scale from 0 (not at all) to 6 (as vivid as a real perceptual experience), and whether they felt movement in the phantom limb (on the same scale as the item before). Patients were contacted by phone at least once a week to check for questions or problems, and were instructed to contact the experimenters if any problems should arise. The entire procedure of the study, except for the time spent in the MRI scanner and the explanation of the fMRI measurement procedure, was identical for the patients with and without fMRI data.

2.4 MRI scanning session The MRI measurements took place at the beginning and at the end of the 4-week training period. During the first appointment, patients were informed about the purpose of the study and the exact movement tasks to perform in the MRI scanner. Before the measurement, patients were trained to execute the requested hand movements with the intact hand without producing muscle activity in the residual arm (using an electromyography feedback procedure prior to the first measurement; see Lotze et al., 2001). Lip and hand movements were demonstrated to the patients and practiced by the patients before the measurement. During the fMRI scan, the patients’ gaze was redirected using a mirror attached to the MRI head coil. This way, they could easily

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view their intact hand lying on the abdomen, as well as its reflection, which was produced using a mirror placed on the patient’s body. For the hand movement condition, patients were instructed to close their hand to a fist (yet without any actual touching of the fingertips to the palm or between the fingers) and to open it again whenever they heard a sound signal. This signal was presented with a frequency of 0.5 Hz during activity phases (on-block; duration: six scans or 19.8 s), whereas no sound was given during the resting phase (off-block; duration: six scans or 19.8 s), for which patients were instructed to lie still, watching their hand and the mirror image. For the on-block, they were explicitly instructed to imagine their phantom hand moving in accordance with the reflected intact hand. For the lip-pursing condition, also assessed with an fMRI measurement, patients were asked to lie still with their eyes closed and to purse their lips whenever they heard the sound signal (which was again presented with a frequency of 0.5 Hz during activity phases).

2.5 Image acquisition and analysis The fMRI scans were conducted with a 3 Tesla Siemens Trio MR (Siemens AG, Erlangen, Germany) scanner using echoplanar imaging (matrix 64 × 64, TE 45 ms, TR 3.3 s) and 40 slices of 2.3 mm thickness, tilted in accordance with the transverse plane adjusted to include all frontal, central, parietal and occipital cortical areas as well as upper parts of the temporal cortex and the cerebellum. Seventy-eight wholebrain scans including six blocks of hand or lip movements with six scans each paired with seven blocks of six scans of rest were gathered per condition, and the first three volumes were excluded from the analysis to allow for signal stability following onset transients. For anatomical reference, a T1-weighted anatomical data set (magnetization-prepared rapid acquisition with gradient echo; slice thickness 1.1 mm, TR 2300 ms, TE 2.98 ms, flip angle 9°) was obtained. fMRI data were evaluated using SPM8 (Wellcome Institute of Imaging Neuroscience, London, UK) implemented in Matlab 7.1 (MathWorks Inc., Natick, MA, USA). The echoplanar images of each subject were coregistered to the individual anatomical data sets after the anterior commissure had been manually defined as the reference point. Further pre-processing included motion– and slice–time correction, normalization to the standard space using a template [Montreal Neurological Institute (MNI)] and smoothing with a Gaussian kernel of 8 mm3 (full width at half maximum) to decrease spatial noise. For group-level analyses, the images acquired from patients with a right-hand amputation were flipped (cf. Lotze et al., 2001; MacIver et al., 2008; Diers et al., 2010) so that the hemisphere unaffected by (i.e., ipsilateral to) the amputation is always shown on the left. For the individual analyses of cortical reorganization (lip movement data), this flip was not performed. The hemispheres of the patients’ brains that were ipsilateral to the amputation served as control for the measured changes in cortical activity since no pain-specific alterations were expected on the intact hemisphere as a consequence of the study. Whole-

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brain activation during lip-pursing and hand movement tasks, both before and after treatment, was observed, and differences in activation during hand movement, before and after treatment, in areas related to the processing of bodyrelated information and pain [primary and secondary somatosensory cortex (S1 and S2), primary motor cortex (M1), anterior cingulate cortex, insula, parietal cortex] were correlated with the benefit from therapy.

2.6 Statistical analysis of clinical and behavioural data The average daily pain ratings were aggregated into weekly averages, and the mean ratings before training were then compared with those after training using a one-tailed pairedsample t-test. As a measure of effect size, Cohen’s d was calculated using the means and SDs of the pain ratings before and after treatment. Connections between non-painful phantom phenomena (i.e., telescoping and the feeling of relatedness between phantom hand and mirrored hand, time since amputation) and PLP as well as individual treatment effect were calculated using Spearman’s rank correlations. Missing values caused by a patient skipping some daily ratings were replaced by the averaged value of the day before and the day after. Ratings about the relatedness between the mirror image and the phantom hand were gathered after the performance of each of the five tasks. For the depiction of results, these values were summed up over 3 days each. The averaged value for the first 3 days of the training was taken as an indicator for the individual trait of the patient. A 3-day period was used in order to ensure that the rating was not influenced by either an initial first-day surprise effect or a training effect caused by the mirror treatment. Scores were averaged over the five tasks.

2.7 Brain changes related to treatment Several measures were used to assess treatment effects on neuronal activity. For both hand and lip stimulation, brain activity during the task was observed before and after treatment on a whole-brain level and when anatomical regions of interest (ROIs) were used. For the identification of the lip and hand areas in S1 and M1, the functional ROIs defined by MacIver et al. (2008) were used (MNI coordinates: lip S1: ±58, −18, 24; lip M1: ±52, −8, 36; hand S1: ±34, −30, 58; hand M1: ±34, −34, 52). Differences in activation related to MT were assessed using family-wise error correction. In addition, a multiple regression was performed, using pain reduction after treatment as a covariate in order to reveal differences in activation related to treatment effects. For the investigation of a shift in cortical lip representation, the analysis of the fMRI data of the lip-pursing task was used to determine the location of activity peaks in S1 and M1 using pre- and post-central ROIs (as defined by the Wake Forest University PickAtlas toolbox version 2.4 for SPM8; Maldjian et al., 2003), both on the hemisphere affected by

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the amputation and on the opposing hemisphere. The shift in cortical organization caused by the amputation was defined as the Euclidean distance between the peak activity locations under the assumption that both locations lie in the same hemisphere; this was carried out by multiplying the x-coordinate of the left activity peak with −1, thereby effectively flipping the coordinates of the left side in MNI space onto the right side (cf. MacIver et al., 2008). This procedure allowed us to estimate the position of the mouth representation under healthy conditions and to calculate the distance between this position and the affected position (see Elbert et al., 1994; Karl et al., 2001). The calculation resulted in a measure of the shift that had occurred on the contralateral side of the cortex relative to the ipsilateral side represented as the distance in millimetres, where the distance was calculated using the Euclidean distance formula. The individual amount of this cortical shift was correlated with the individual intensity of pain using Spearman’s rank correlation. The degree of cortical shift as described above immediately before the 4-week training was compared with the same value immediately after the training as a measure for the degree of change in cortical organization, which might have occurred as a result of MT. Cortical reorganization during the training phase was defined as the Euclidean distance between left and right activity peaks (as described above) before training minus that same distance after training. This results in the amount of relative change in location during the training period given in millimetres and creates a measure of activity shift on the affected side back towards a healthy state. Spearman’s rank correlation was used to investigate the connection between this measure and pain ratings. In addition, we calculated the cortical shift from the first to the second measurement in the S1 and M1 regions of the hemisphere ipsilateral to the amputation. This shift was then checked for correlations with benefit from treatment. Since we hypothesized a specific effect of MT only on the affected hemisphere, we expected no significant correlation for the hemisphere ipsilateral to amputation site. In order to assess the contribution of the hand movement (cf. Makin et al., 2013), we also defined functional hand ROIs using group means of M1 and S1 during hand movement (contralateral to amputation site) and defined 5-mm spherical ROIs around these coordinates. We used these ROIs to extract the percentage signal change in these areas (using the REX ROI extraction toolbox version 2.1 for SPM8; Whitfield-Gabrieli, 2009). We correlated the intensity of activation at the first measurement with pain levels before therapy, the activation at the second measurement with pain levels after therapy and the difference in activation intensities with benefit from treatment.

3. Results 3.1 Mirror training performance The patients did not report any problems in performing the mirrored movements or with the duration of

Mirror therapy for phantom limb pain

the training per day, and no patient dropped out of treatment. Three participants skipped individual training days because of time constraints or illness (patients 7 and 13 missed 1 day, patient 12 missed 2 nonconsecutive days). Patients consistently performed all five movement tasks for 3 min each with only minor deviations in training duration (patients 7, 11 and 12, range of duration 2–4 min per task).

3.2 Pain The patients reported stable pain ratings 2 weeks before the training, with a decline after the first week of daily training. The average pain rating in the week after the training was significantly lower than that from the week before start of the training (week 1: M = 28.21, SD = 11.52; week 2: M = 28.26, SD = 16.27; week 7: M = 20.60, SD = 12.80; week 8: M = 23.44, SD = 13.04; week 2 vs. week 7: t12 = 1.78, p = 0.05). Cohen’s d was 0.52, indicating a mediumsized effect of treatment on pain scores. Individual pain ratings before and after the mirror treatment are given in Supporting Information Table S2 and illustrated in Fig. 1A; Fig. 1B shows the average pain ratings before, during and after the mirror treatment.

3.2.1 fMRI data: Group-level analysis Lip movement task: At both time points, patients showed significant bilateral activation during lip pursing in S1, M1 and insular cortex. Significant brain activations both before and after treatment are described in Supporting Information Table S3. Mirrored hand movement task: The mirrored hand movements caused significant bilateral activation in somatosensory and motor regions before and after treatment, as well as in the insular cortex and, at the first time point, in the inferior parietal cortex (IPC) and thalamus (Supporting Information Table S4). Both before and after treatment, activation in S1 cortex was less intense on the hemisphere affected by the amputation. A paired-sample t-test revealed no significant pre-post change in the mirror task in S1 or M1. The multiple regression analysis showed a significant connection between the individual amount of pain reduction during the treatment and a decrease of activity in the IPC on the hemisphere affected by the amputation over the course of therapy (p = 0.001, uncorrected, peak activity: T = 7.31, Z = 4.08, MNI coordinates: x = 52, y = −38, z = 46; see Supporting Information Fig. S1).

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A

Pain rating (VAS, 0–100)

Pre-training Post-training

Subject #

B Training phase

Post-phase

Pain rating (VAS, 0–100)

Pre-phase

(Cohen’s d) of treatment showed no significant result for M1 (r = 0.15, p = 0.34), whereas the amount of reduction in the cortical shift of S1 was found to be significantly positively correlated with the reduction in PLP measured as the difference between the preand post-phases (r = 0.75, p < 0.01). Fig. 3 shows a scatter plot of this relationship. The cortical shift in the control regions, i.e., S1 and M1 in the hemisphere ipsilateral to the amputation, was not significantly correlated with treatment benefit (S1: r10 = 0.18, p = 0.59; M1: r10 = 0.16, p = 0.64). The intensity of activation in the phantom hand region during mirrored hand movements before the training was not significantly correlated with pre-training pain (S1: r10 = −0.24, p = 0.48; M1: r10 = −0.37, p = 0.26), the same activation after the

A

All patients (N = 11)

Pre Post

Week

Figure 1 (A) Individual pre- and post-training pain ratings, ordered from most to least benefit. Triangles denote individual patients without a telescopic distortion of the phantom. (B) Daily pain ratings averaged over weeks and over all participants. Error bars depict standard error.

3.2.2 fMRI data: Individual analysis The initial measurement of cortical activation during the lip-pursing task showed an average dysfunctional cortical shift of 15.4 mm (SD = 9.6 mm) in S1 as well as an average shift of 16.6 mm (SD = 6.7 mm) in M1. The comparison of the cortical shift before and after training revealed an average reduction of this shift of 2.9 mm (SD = 11.4 mm) for S1 and 1.5 mm (SD = 10.5 mm) for M1. This difference is not statistically significant on a group level (Z = −0.889, p = 0.37). Fig. 2 displays the difference in distribution of cortical activity for all patients during the lippursing task in S1 on the hemisphere that is affected by the amputation before and after treatment (Fig. 2A), as well as individual data for the amount of dysfunctional shift in S1 before and after treatment (Fig. 2B). The correlation between the individual amount of reduction in the shift and the individual effect size

B Pre-training Post-training

Figure 2 (A) Neuronal activity in somatosensory cortex during lippursing task before (red) and after (blue) mirror therapy. (B) Amount of dysfunctional shift for individual patients before (red) and after (blue) training, ordered from most to least benefit.

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training was not significantly correlated with post-training pain (S1: r10 = −0.40, p = 0.22; M1: r10 = −0.46, p = 0.16), and the difference between the activations before and after was not significantly correlated with treatment benefit (S1: r10 = −0.24, p = 0.47; M1: r10 = −0.17, p = 0.62). 3.2.3 Predictors of treatment effects There was no significant correlation between benefit from treatment and time since amputation (r = −0.27, p = 0.42). Eight of the 13 patients reported a telescopic distortion of the phantom limb (see Supporting Information Table S1). The perceived intensity of this telescope was negatively correlated with the treatment effect (r = −0.94, p < 0.01). Apart from the intensity of the telescope, the mere presence of this phenomenon had an influence on pain alleviation: Five patients without a telescopic distortion reported an average of 51.23% decrease in PLP (pre-phase: M = 32.01, SD = 14.34 vs. post-phase: M = 15.61, SD = 6.64; t4 = 2.20, p < 0.05 one tailed; Cohen’s d = 1.64), whereas the training had almost no effect (changes in PLP ratings

Mirror therapy for phantom limb pain: brain changes and the role of body representation.

Phantom limb pain (PLP) is a common consequence of amputation and is difficult to treat. Mirror therapy (MT), a procedure utilizing the visual recreat...
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