Changes in spontaneous overt motor execution immediately after observing others’ painful action: two pilot studies

Changes in spontaneous overt motor execution immediately after observing others’ painful... Research has demonstrated that motor control is directly influenced by observation of others’ action, stimulating the mir - ror neuron system. In addition, there is evidence that both emotion and empathy after observing a painful stimulus affects motor cortical excitability and reaction times. Aim of the present two pilot studies is a) to test for significant influence of observing other’s painful bending of the trunk on execution of the same activity in a self-directed bending action (study 1) and to compare these results with a bending action according to a strict bending protocol (study 2). In addition to study 1, differences between Low Back Pain (LBP) patients versus healthy subjects are tested. Video footage of a (1) neutral, (2) painful, and (3) happy bending action was presented in random order. Changes in flexion–relaxation phenomenon (FRP) of back muscles were studied directly after watching the videos with surface EMG, in study 1 during a self-directed bending action in LBP patients and healthy subjects, in study 2 according to a strict bending protocol. FRP ratios were calculated by a custom-made analysis scheme tested for sufficient reliability prior to both studies. Evoked emotions were measured with an Emotional Questionnaire after each video. A Mixed Model ANOVA was used to test for the effect video and the difference between LBP and healthy subjects on the FRP-rs. Differences in evoked emotion will be tested with a Wilcoxon Signed Rank Test. In study 1, 24 healthy controls and 16 LBP patients FRP-rs were significantly influenced after observing a painful video in all subjects versus a happy and neutral video (p = 0.00). No differences were present between LBP and healthy controls. All subjects experienced more fear after observation of the painful video (p 0.05). In study 2, 6 healthy subjects followed the strict FRP bending protocol for three times after observing each video. No significant changes occurred in FRPs per video compared to FRPs of six healthy subjects carrying out the spontaneous bending activity. Observing a painful action in another person changes motor performance and increases fear in both people with and without back pain, during self-directed trunk flexion, but not during a protocolled trunk flexion. Keywords Low back pain · Motor control · Action observation · Empathy · Mirror neuron system * Annelies Pool-Goudzwaard Introduction a.l.pool-goudzwaard@vu.nl Rehabilitation strategies in low back pain (LBP) patients Amsterdam Movement Sciences, Faculty of Behaviour and Movement Sciences, Vrije Universiteit Amsterdam, Van often focus on training trunk coordination, strengthening, der Boechorststraat 7, 1081BT Amsterdam, The Netherlands and endurance training of muscles of the trunk (Delitto Somt University of Physiotherapy, Amersfoort, et al. 2012). Theoretical basis for this intervention is alter- The Netherlands ations in motor control of lumbar spinal muscles demon- Department of Neuroscience, Faculty of Health Sciences strated to be present in this specific patient group (D’hooge and Medicine, ErasmusMC University, Rotterdam, et al. 2013a, b; Dickx et al. 2008; Geisser 2007; Hodges The Netherlands et al. 2001, 2003; Kalichman et al. 2010; MacDonald et al. Menzies Health Institute Queensland, Griffith University, 2010; Tsao et  al. 2010; Etemadi et  al. 2016; Sánchez- Gold Coast, Australia Zuriaga et al. 2015). Typical for altered motor control is Faculty of Psychology and Educational Sciences, Open the change in paraspinal muscle activity during forward University of the Netherlands, Heerlen, The Netherlands bending in these patients, the so-called flexion–relaxa- School of Health and Rehabilitation Sciences, The University tion phenomenon (Ahern et  al. 1988; Alschuler et  al. of Queensland, Brisbane, Australia Vol.:(0123456789) 1 3 Experimental Brain Research 2009; Ambroz et al. 2000; Geisser et al. 2000; Watson Even more, mirror neurons are also directly influenced et al. 1997; Sanchez-Zuriaga et al. 2015). Among normal by emotions (Enticott et  al. 2008, 2011, 2012; Gazzola healthy subjects, activity of the lumbar paraspinal mus- et al. 2006; Budell et al. 2015). A study revealed the effect cles during flexion initially increases, and then decreases of observation of emotion in others on motor cortex excit- as the ligaments begin to support the trunk as the angle ability, providing support that direct emotion perception is of flexion increases (Alschuler et al. 2009). However, in closely linked to action systems (Borgomaneri et al. 2012). people with LBP, this paraspinal relaxation in maximum This is in line with several studies, indicating that empathy voluntary flexion tends to be absent or decreased (Ahern for people in pain may be based on ‘mirror-matching’ simu- et al. 1988; Alschuler et al. 2009; Ambroz et al. 2000; Col- lation of others’ state (Gallese 2003; Morrison 2004; Singer loca and Hinrichs 2005; Descarreaux et al. 2008; Geisser et al. 2004; Budell et al. 2015). Avenanti and Aglioti (2006) 2007; Maher et al. 2005; Mayer et al. 2009; Watson et al. demonstrated that not only the affective nodes in the pain 1997; Schinkel-Ivy et  al. 2013; Sanchez-Zuriaga et  al. network are concerned with empathy for pain, but also the 2015). The assumption is that this altered motor control is sensomotoric side (Avenanti and Aglioti 2006). Avenanti due to anticipation of the presence of LBP (Hodges et al. et al. (2009a, b) demonstrated that an onlooker to a needle 2003; Moseley and Hodges 2005) leading to a “smudg- penetration of a models hand leads to diminished cortical ing of the brain” on the sensory motor cortex and pos- excitability specific for the muscle and hand observed to be sibly an altered neural drive of muscles (Tsao et al. 2010; penetrated. In contrast, observing a needle penetration in one Chiou et al. 2014). Motor control deficits as demonstrated other’s hand leads to a generalized corticospinal excitability by alteration of the flexion–relaxation phenomenon are of the opposite hand, leading to a possible freezing response indeed associated with the clinical status of people with (Avenanti et al. 2009a, b). However, the participants in these LBP (Schinkel-Ivy et al. 2013). A significant association studies were not active nor any action was required. One exists between the flexion–relaxation phenomenon ratio might discuss whether motor action preparation and activ- (FRP-r) (i.e., the ratio between activity at maximal flexion ity could have an effect on these results. Indeed, Morrison and during extension) and measures of perceived disabil- et al. (2007) demonstrated altered reaction times such as ity, a measure of clinical pain, pain-related fear as well speeding withdrawal response and slowing approach move- as range of motion during flexion and elicitation of pain ments with the hand/finger pressing keys when observing a during straight leg raise (Alschuler et  al. 2009). Based needle pricking a finger (Morrison et al. 2007). Gallang et al. on these findings, it seems logical to train motor control (2017) stated that these responses contrast muscle specific deficits in LBP patients. inhibition after pain observation often found in transcranial Since rehabilitation in people with LBP often take magnetic stimulation (TMS) studies. Furthermore, Gal- place in groups, especially in a multidisciplinary setting lang et al. (2017) demonstrated that participants actually another important factor can influence motor control in responded faster (increased excitability) after observation of these patients. Motor control of muscles is also influenced a painful stimulus to the hand than a non-painful stimulus, by observation of others. Observing someone performing irrelevant if the participants responded with the foot or the an action is known to influence motor execution and even hand. Even more, the delay (500 ms) of a Go/No go signal motor skills (Ferrari 1996; Hodges et al. 2007; Lepage even increased the speed of the response. It seems that sen- et al. 2010; Vogt and Thomaschke 2007; Wulf and Mornell sorimotor contagion of emotion leads to altered excitability, 2008; Murata et al. 2016; Behrendt et al. 2014; Morrison studied by reaction times to a Go/No go task after observing et  al. 2007). The neuronal mechanism of this influence a painful stimulus. However, these studies cannot answer the may rely on the mirror neuron system. Mirror neurons are question whether people with LBP in a rehabilitation group neurons that are activated not only during the execution might be influenced in their overt motor activity by observ - of an action, but also during the observation of the same ing others in pain. After all, these people with LBP do not action performed by someone else (Di Pellegrino et al. observe “a painful damaging stimulus” but a painful activ- 1992; Fadiga and Craighero 2003; Gallese et al. 1996; Gal- ity in others, nor have to respond in a predefined activity to lese 2003). Results from experimental studies demonstrate this stimulus as quickly as possible. Still, these patients will facilitation of movement execution (Villiger et al. 2011), observe others moving with pain while performing the same specifically of the initiation and optimization of move- functional activities. ment, when observing congruent action in others (Ménoret The aim of the first pilot study was (a) to demonstrate et al. 2013). Murata et al. (2016) state that control of one’s differences in an overt bending motor action measured with own action and the mirror neuron system are shared with EMG, after watching a painful bending activity versus a the “who” system, which is related to the recognition of bending activity in a neutral and happy condition and (b) action. whether this is different for people with LBP and healthy controls. The aim of the second study was to demonstrate 1 3 Experimental Brain Research the differences between following a strict bending protocol of a few seconds bending forward, a few seconds maximal versus a self-directed bending action after observing the flexion and a few seconds extension of the lumbar spine same videos. (Ahern et al. 1988; Alschuler et al. 2009; Ambroz et al. 2000; Geisser et al. 2000; McGorry and Lin 2012; Watson et al. 1997). We hypothesized that after watching a painful Materials and methods bending action, the motor excitability of the trunk muscles would be increased and that the relaxation of the erector Design spinae muscles would not occur while bending, even more evident in LBP patients. Two fundamental experimental pilot studies have been per- For the first experiment, we decided that the official flex- formed. Medical ethical approval was obtained by the Open ion relaxation protocol being a predefined time framed pro- University of The Netherlands. tocol of flexion and extension of the trunk did not reflect normal movement patterns as bending forwards in healthy Study 1 subjects nor in LBP patients during rehabilitation programs. We decided to focus on a spontaneous change in the flex- Participants ion relaxation phenomenon evoked by observing a similar bending activity in others. Therefore, we adapted the flexion For the first study, healthy subjects (n = 24) are recr uited relaxation protocol to a more spontaneous activity as pick- from the Department of Neuroscience at the ErasmusMC ing up an object, like a wallet from the ground. At first, we University, Rotterdam. People with LBP (n = 16) are established a mean standardized time frame by measuring recruited from primary care physiotherapy clinic. All sub- the speed of picking up a wallet from the ground multiple jects voluntary participated in the study after reading an times prior to the research. A mean standardized time frame information flyer and signed an informed consent. Inclusion could be calculated of 0.1-s maximal voluntary flexion after criteria were age between 20 and 60 year old en being able to bending forward picking up the wallet and 0.3 s coming up read and understand Dutch. Exclusion criteria were specific straight. During the experiment, continuous SEMG meas- LBP due to malignant processes and systematic disease as urements were performed of the erector spinae muscles high well as inability to bend forward. (height L1) and low (height L4) (see Fig.  1a). All EMG electrodes were connected to a portable EMG registration Questionnaires system (TMS porti: Twente Medical Systems International, Oldenzaal, The Netherlands). EMG signals were band pass Prior to the measurements, all subjects filled in a question- filtered (10–1000 Hz). A Notch filter of 50.2–49.8 Hz sup- naire containing the Roland Disability Questionnaire (RDQ), pressed possible power-line interference of 50 Hz. a pain Numeric Rating Scale (NRS) and additional questions For study 1, we measured not only erector spinae activity on socio-demographic data. The Roland disability question- with SEMG, but also facial muscles: the frontalis, corrugator naire has proven sufficient to good reliability and validity supercilii, orbicularis oculi, and zygomaticus major on the to measure disability due to LBP (Smeets et al. 2011). The left and right sides (Lapatki et al. 2010) (see Fig. 1b). NRS is a scale between 0 (no pain) and 10 (excruciating Increased activity in facial muscles can be used in two pain). The psychometric qualities of both instruments are ways. At first, increased activity of facial muscles can be good (Ostelo and de Vet 2005; Soer et al. 2012; van der used as a reference for maximal bending forward, since Roer et al. 2006). With a positive score on the RDQ > 0 and activity in facial muscles increases during extension after NRS > 0, a subject entered the LBP group. Prior and during bending forward. An intensity graph of SEMG of the facial the measurements, an “Emotional Questionnaire” was used. muscles plotting the amplitude in color versus time demon- This is a small questionnaire scoring six separate emotions strated the highest activity in facial muscles related to bend- (surprise, happiness, fear, irritation, disgust, and sadness) ing forward and maximal flexion (see Fig.  2). SEMG data on a five-point Likert scale from not at all present (0) to during the mean standardized time frame of 0.1 s of maximal very strong (5). flexion and 0.3 s extension with the highest facial activity were used for analysis. Second, increased activity of facial Bending motor action–flexion relaxation phenomenon muscles can reveal the subjects’ affective state evoked by the videos (de Wied et al. 2006; Ekman et al. 1981; Lapatki In the literature, the flexion–relaxation phenomenon (FRP) et al. 2010; Larsen et al. 2003). These positive and negative is described as relaxation of the paraspinal Erector Spinae affective states can be reliably distinguished by facial EMG muscle in full flexion. This can be measured by Surface (Larsen et al. 2003). Electro-MyoGraphy (SEMG) during a predefined protocol 1 3 Experimental Brain Research Fig. 1 Electrode position of the back muscles (a) and on the face (b) we tested the test–retest reliability in ten healthy subjects Experimental setup and protocol executing 3 × 3 bending actions (ICC 0.67 during flexion and 0.78 during extension). Since ICC was sufficient, we All subjects were measured in a separate area, created by room dividers, to avoid emotional contagion and EMG decided that one measurement could be used per video in study 1. During study 1, the bending action was carried out activity by the presence of the researchers (see Fig. 3). All subjects sat on a chair behind a table on which two printed by placing a wallet on a mark on the ground beside the table. After each video, the subject was instructed to pick up the emotional questionnaires were placed. All subjects watched three separate custom-made videos: (a) a video with a per- wallet and to sit down on the chair and fill in one emotional questionnaire. After completion, the subject was instructed son picking up a wallet from the floor extending to erect posture and walking on (neutral video); (b) picking up the to return the wallet to the marking on the ground. All sepa- rate actions (start video, emotion evoking moment during same wallet hardly able to raise himself to erect posture due to excruciating acute LBP (painful video); and (c) picking the video, ending of the video, standing up, bending for- ward, return to chair, etc.) were marked with a marker on the up the same wallet coming to erect posture with someone else responding enthusiastic and glad that their wallet was 16th channel of the SEMG-recording system. After the final video, the subjects were asked to stand erect for 3 s, while found (happy video). The videos were displayed in random order on a projection screen in front of them, one ‘condi- three consecutive SEMG “rest activity” measurements were performed of the erector spinae muscles to make it possible tion’ video (3 conditions neutral, happy and painful) per subject. We choose not to repeat any videos to mimic ‘nor- to normalize SEMG data by dividing the SEMG value dur- ing the flexion and extension by the mean average SEMG mal life observing other subjects bending and raising again as well as LBP patients in a rehabilitation clinic since view- during standing of the same erector spinae muscle. ing another LBP patient hurting his or her back, hardly able to raise again. It is not natural for such a patient to repeat this movement over and over. This indicated that we could only execute one bending action per video. Prior to study 1, 1 3 Experimental Brain Research Fig. 2 Three seconds of SEMG data registered after the marker signalling picking up a wallet. The upper part shows the inten- sity graph of facial muscles, the lower part shows the 4 channels of the erector spinae muscles (9, left erector spinae high; 10, right erector spinae high; 11, left erector spinae low; 12, right erector spinae low). The 0.1 s of maximal flexion and 0.3 s of extension as a fixed time frame are selected at the location of most increased facial activity Data analysis when calculating normalized values for maximal voluntary flexion and 0.78 for normalized extension. In study 1, data analysis was performed in a custom-made Affective facial EMG responses were calculated using the smoothed, rectified maximum EMG output during a LabVIEW 8.2 application-DaqSys 16 player. Three com- plete seconds of data after markers 3 and 9 (indicating short interval of 100 ms after each marker related to the emotion evoking moment in the pain and happy videos. picking up the wallet from the floor directly after watching the videos) were used. The FRP was localized by study- These max. EMG values per muscles and side were stand- ardized as a proportion of 3  s of baseline EMG ampli- ing SEMG activity of the erector spinae muscles (four channels) (see Fig.  1). At first, SEMG data during the tudes per subject (Boxtel van 2010). Higher proportions of zygomaticus major and orbicularis oculi muscle activity flexion relaxation phenomenon of all erector spinae chan - nels were normalized by dividing the maximum SEMG are expected during an elementary positive emotion of happiness, while frontalis and corrugator supercilii mus- during extension and the average SEMG during maximal flexion by the mean SEMG of 3 s of rest activity in stand- cle activity is expected during a pain-related or negative emotion like fear, anger, or sadness (Boxtel van 2010). ing. According to the strict analyses protocol to define the Flexion–Relaxation Phenomenon ratio (FRP-r) with the Statistical analysis highest association with clinical measures in LBP patients as pain and disability (Alschuler et al. 2009), the FRP-r To demonstrate changes in emotional status after observa- was calculated by dividing the normalized maximum SEMG during extension (0.3  s) to the average normal- tion of a painful, happy, or neutral video, at first, all scores were calculated for change from the initial values on the ized SEMG during maximal voluntary flexion (0.1 s) (Als- chuler et al. 2009), see Fig. 4 for the signal processing flow emotional questionnaire to eliminate confounding effect of higher scores on emotional status prior to the measurement. of the SEMG. Reproducibility of this procedure in obser- vation of a pain-free video was tested with 3 × 3 repetitions These delta scores per video were tested for significant dif- ferences overall and per group (LBP versus healthy subjects) per video in ten healthy subjects, prior to this research and demonstrated an intra-class correlation coefficient of 0.67 1 3 Experimental Brain Research Fig. 3 Experimental setup using a Wilcoxon signed rank test and a Mann–Whitney U Study 2 test, respectively. Differences in affective state (positive versus negative Subjects facial EMG muscle activity) evoked by the videos were tested for significant difference between positive and nega- For the second study, students and employees of the VU tive facial mimicry using a Paired T test. University in Amsterdam were asked to participate. With A Mixed Model ANOVA was used to test for the effect a difference in FRP-rs of 1.1 between the healthy sub- of the observed video and the difference between LBP jects watching a painful (2.6 ± 0.9) versus a neutral video and healthy subjects on the FRP-rs, with the three video (1.55 ± 0.7) and the expectation that this similar difference conditions (Painful, Happy, and Neutral) as a within-sub- will be present between a flexion relaxation phenomenon jects factor and participant type (LBP and Healthy) as the according to a strict protocol and a non-strict protocol with between-subjects factor. Possible confounding effect of order an alpha of 0.05 and a power of 0.8, we need a sample size of videos was taken into account. All data were tested for of n = 12 (n = 6 for the strict protocol and n = 6 for the spon- normal distribution. Logistic transformation of all skewed taneous action). The last group will be derived from study 1 data was carried out prior to statistical analysis. by an ad random selection of every fourth healthy subject. The same Mixed Model ANOVA was used to test for the Another six healthy subjects participated in study 2. effect in the second study. Protocol The protocol described by McGorry and Lin (2012) was followed to measure the FRP in study 2 with standing still for 4 s, bending forwards in 4 s, remaining fully flexed for 1 3 Experimental Brain Research Fig. 4 Signal flow and process- ing 4 s and extending for 4 s. For study 2, we recorded and cal- Statistical analyses culated the movements of the spine using an optical tracking system Optotrak, reading two markers on the dorsal side of Another Mixed Model ANOVA was used to test for the the spine at the height of L1 and L5. A marker signal was effect of the observed video with the three video conditions used to synchronize the data of the EMG with the output of (Painful, Happy, and Neutral) as a within-subjects factor. As Optotrak. between-subjects factor the effect of either or not following, Data analyses were performed in a custom-made Matlab a strict FRP protocol was used. R2014b application. Again, all SEMG data during the flex- ion relaxation phenomenon of all erector spinae channels were normalized. During four seconds of maximal flexion Results measured by Optotrak, mean SEMFG of a same time frame as in study 1 of 0.1 s was calculated as well as 0.3 s during As described, 40 subjects participated in study 1 16 LBP the extension. According to the same pre-described protocol, patients and 24 healthy controls and 6 healthy subjects in FRP-rs were calculated as in study 1. study 2. Socio-demographic data are shown in Table 1. No 1 3 Experimental Brain Research significant differences are present between LBP patients and present throughout all videos in all facial muscles. Since healthy controls on socio-demographic data and initial val- low-frequency artifacts such as eye blinking and/or other ues on the EQ. Cronbach’s alpha for internal consistency for movements like activity of neighboring muscles, swallow- positive labeled emotions on the EQ (surprise and happi- ing, etcetera were interfering with the facial data we ques- ness) was 0.67. The Cronbach’s alpha of the negative labeled tioned these data for reliability and did not perform statisti- emotions (fear, irritation, disgust, and sadness) was 0.88. cal analysis on this data. Evoked emotion Influence of observation of pain on FRP‑rs All median scores on changes in emotional status after Differences between FRP-rs per video are displayed in observation of the videos are 0 (see Table 2 for study 1). In Graph 1. Higher FRP-rs are present in the painful condi- the overall group, there is a significant difference of feeling tion versus the neutral and happy condition, indicating more fear (p < 0.05) after observation of a painful action in relatively more f lexion relaxation (less activation) of the both groups with respect to the neutral and happy video in erector spinae at full trunk f lexion. study 1. This, however, is not present in study 2. In study 1, Since sphericity was not present (χ = 1.2, p > 0.05, df significant less fear is present in healthy controls after watch- 1.98 was corrected by Greenhouse–Geisser. The mixed ing a happy video with respect to the pain patients. model ANOVA demonstrates a significant effect of video In contrast with our expectation, EMG facial activity in as a within subject effect F = 3.26, p < 0.05. Follow-up the 100 ms interval after the marker related to emotion evok- paired t tests demonstrated a significant difference in (log ing moment did not show a single peak of muscle activity transformed) FRP-rs after observing the painful video after a “still” period. Multiple peaks in muscle activity were (Mn 0.72, SD 0.37) and after observing the neutral video Table 1 Socio-demographic Subjects All (n = 40) HC (n = 24) LBP patients (n = 16) HC study 2 data and initial values on the EQ Gender (F/M) 19/21 11/13 8/8 4/2 Age (years) 35 (SD ± 12.1) 34 (SD ± 12.3) 37 (SD ± 11.9) 27 (SD ± 11.9) Outcome questionnaires  NRS (mean SD, min, max) 0 4 (SD ± 2.5) min 2, max 7 0  RDQ 0 5.2 (SD ± 4, min 0, max 19) 0 EQ  Surprise 1 (SD ± 0.6) 1 (SD ± 1.1) 0 (SD ± 0.3)  Happiness 2 (SD ± 0.7) 1.5 (SD ± 1.0) 0 (SD ± 0.6)  Fear 0 (SD ± 0.2) 0 (SD ± 0.4) 0 (SD ± 0.1)  Irritation 0 (SD ± 0.2) 0 (SD ± 0.7) 0 (SD ± 0.2)  Disgust 0 (SD ± 0.1) 0 (SD ± 0.3) 0 (SD ± 0.1)  Sadness 0 (SD ± 0.3) 0 (SD ± 0.5) 0 (SD ± 0.1) LBP low back pain, SD standard deviation, F/M female/male, NRS numeric rating scale, RDQ Roland dis- ability questionnaire, EQ emotional questionnaire Table 2 Mean changes in scores per emotion on the emotional questionnaire after observation of a painful (P), neutral (N) and a happy (H) video, overall and per subgroup in study 1 Subjects All (n = 40) HC (n = 24) LBP patients (n = 16) EQ (± SD) N P H N P H N P H  Surprise 0.33 (0.7) 0.23 (0.7) − 0.03 (0.9) 0.30 (0.7) 0.22 (0.6) 0.0 (0.9) 0.38 (0.7) 0.25 (0.9) − 0.8 (0.8)  Happiness 0.08 (0.6) − 0.03 (0.7) − 0.67 (0.7) − 0.04 (0.5) − 0.13 (0.7) 0.65 (0.7) 0.25 (0.7) 0.13 (0.6) 0.69 (0.6)  Fear 0.05 (0.2) − 0.08* (0.3) 0.03 (2.9) 0.4 (0.2) 0 (0) − 0.4* (0.2) 0.06 (0.2) − 0.06 (0.4) 0.15 (0.3)  Irritation 0.03 (0.2) 0.08 (0.4) 0.22 (0.6) 0.5 (0.2) 0.13 (0.5) 0.13 (0.5) 0 (0) 0 (0.4) 0.38 (0.9)  Disgust 0 (0) 0,13 (0.5) 0 (0.2) 0 (0) 0.14 (0.4) 0 (0) 0 (0) 0.13 (0.6) 0 (0.4) No significant differences are present neither between both videos nor between patients versus healthy subjects *p < 0.05 1 3 Experimental Brain Research immediately after observing other’s painful action. The fact that observing others’ painful motor action alters one’s own motor action is relevant, especially for LBP patients training together always observing others’ painful action. The higher FRP-rs present while observing a painful bend- ing action, in all subjects, indicate relatively more flexion relaxation (less activation) of the erector spinae at full trunk flexion. This is not present after observing a neutral or happy bending condition. From a clinical point of view it is relevant that in all subjects observation of pain alters motor execution of a spontaneous similar action. LBP patients often display pain behavior when bending forward or lifting objects. Meanwhile, LBP patients, especially Graph 1 Mean FRP-rs ± standard deviation (SD) per video in LBP with a chronic condition, are often trained in groups with patients and healthy controls an emphasis on graded activity. Seeing another patients´ pain behavior might interfere with a patients’ own motor control. Clinicians should be aware of this phenomenon. In addition, execution of motor control of healthy spouses or friends of these patients might be influenced as well. Still, we have to be careful in drawing firm conclusions on both pilot studies. Confirmation of these findings in a larger study is necessary for more robust proof. Altered FRP-rs are a new finding which is supplemen- tary to the knowledge we have on the influence of observa- tion others’ pain on motor excitability. It seems that not only motor excitability and reaction times in motor execu- tion alters after observation of a painful stimulus to the hand, but also by seeing others’ painful activity executing the same action (Ferrari 1996; Hodges et al. 2007; Lepage et al. 2010; Vogt and Thomaschke 2007; Wulf and Mornell 2008; Murata et al. 2016; Behrendt et al. 2014; Morrison Graph 2 Mean FRP-rs/standard deviation (SD) per video in healthy subjects with a strict FRP protocol versus spontaneous bending action et al. 2007). Emotional status {Mn 0.23, SD 0.52 [t(60) = 6.83 p = 0.00]} as well as the happy video [Mn 0.31, SD 0.58, t(60) = 4.87, p = 0.00]. The current study has demonstrated that the emotional sta- No significant differences were present in FRP-rs after tus of the observer can significantly be influenced directly observing a happy or a neutral video. The between-sub- by a negative stimulus like observing others’ pain. All jects effects were not significant. No significant effect subjects scored more fear on the emotional questionnaire was present by order of video. after observing a painful video. The findings are in line No significant within-subjects effects were present with results from the literature. Data have been presented of observing a video nor between-subjects effects in the on the influence of observation of pain in humans. Seeing strict protocol condition between in study 2 (see Graph 2). painful or unpleasant stimuli may elicit arousal or aversion (personal distress) reactions (Williams 2002). We have to be careful to draw firm conclusions, since the reliability Discussion of the emotional questionnaire is not tested and the data cannot be confirmed by facial mimicry (EMG of facial Main finding of the current pilot study is that observing an muscles). Furthermore, the number of subjects is small. overt painful motor bending action of the trunk increases fear in the observers and significantly alters the execu- tion of the congruent painful action. It seems, this only takes place when the motor activity is spontaneous and 1 3 Experimental Brain Research fact that research demonstrated that recalled pain as in physi- Influence of observation of others’ pain on motor execution in all subjects cal pain conditions reveals significant activation in mostly similar affective pain processing brain structures, including It has been reported in the literature that the intensity of bilateral anterior insula, anterior cingulate cortex (ACC), and thalamus (Fairhurst et al. 2012), this does not lead to someone else’s pain is negatively correlated to changes in cortical excitability of the observer, in healthy subjects different executions of motor control in LBP patients. Actu- ally, to what extend recall of pain can play a role in motor (Avenanti and Aglioti 2006; Singer et al. 2004). Further- more, it has been reported that negative stimuli prior to the execution is not clear. Further research is necessary to study a possible influence of the pain resonance system in pain observation of transitive hand movements facilitated cortical spinal excitability as well (Enticott et al. 2012; Hill et al. patients on motor execution. 2013). In addition, Hajcak et al. (2007) have been demon- strating increased motor cortex excitability in participants Strengths and limitations who viewed pleasant and unpleasant compared to neutral images. Although we did not study motor cortex excitability Strength of the current study is that this is the first study focusing on motor execution in relation with the model of but motor execution, we could not demonstrated influence of a pleasant (happy) stimulus. Our findings do seem to sup- empathy observing others’ low back pain. Main limitation of the study is that only one trial per port the other above-mentioned studies by demonstrating significant differences in motor execution by observing oth- video has been performed in study 1. Therefore, we tried to test the effect of repeated measurements on motor execution ers’ pain. This is in line with the finding of motor response changes to observing others’ pain in a pain population prior to study 1. Calculating a mean of three trials would have been more robust. However, the effect of observing a (amputees) (Fitzgibbon et al. 2010a, b). Since motor execu- tion changed in all subjects after observing a painful video video on spontaneous motor execution was not present dur- ing repeated measures according to FRP protocol. and this phenomenon did not occur after observing a happy or neutral video, it seems that especially, the negative stimu- Regarding the spontaneous motor execution, the fact that the test–retest reliability in healthy subjects after observing lus of observing others’ pain was the trigger. However, from the current study, we cannot conclude which processes take a neutral video was sufficient supports the reliability of the data despite the fact that only one trial per video per subject place within the brain. The overall emotional status of more fear in all subjects and/or empathy for pain and/ or ‘mirror- was performed. Still, the findings are not very robust. This is why we recommend a repetition of the study in a larger matching’ simulation of others’ state (Gallese 2003; Mor- rison 2004; Singer et al. 2004) or even other pain processes sample size. In the current study, we have chosen to measure the FRP-r can play a role. The fact that in the healthy subjects in study 2, no significant change in evoked emotion was present and during a normal activity like picking up a wallet. Reason for this was the fact that a video of a flexion of the lumbar spine that also no effect was present in change in motor execution could indicate that emotions can play a role. Further research during a preprogrammed time schedule would interfere with the execution of the same spontaneous action as in the video. is necessary to demonstrate which pain processing take place during observation of someone else’s pain and execution of Furthermore, research does underpin the notion that mirror neurons are more sensitive to “object- and goal-orientated” motor control. movement (Enticott et al. 2011). Therefore, picking up a wallet is more appropriate in stimulating mirror neurons, but No differences between healthy subjects and low is different from the preprogrammed timed flexion–relaxa- back pain patients tion phenomenon described in the literature, which was car- ried out in study 2 (Ahern et al. 1988; Alschuler et al. 2009; We anticipated for differences to occur after observing oth- Ambroz et al. 2000; Geisser 2007; McGorry and Lin 2012; ers’ pain between LBP patients and healthy subjects both in Watson et al. 1997). Indeed, study 2 did not result in any evoked emotion as in motor execution. However, no signifi- positive findings. The scores of study 1 are not compara- cant differences were present. Valeriani et al. (2008) sug- ble to the outcome on FRP-rs in the literature. Although gested that being in pain might bias the empathic relation we have chosen the most optimal analysis of FRP-r with with others (Valeriani et al. 2008). Since no differences at regard to association with clinical outcomes in LBP patients group level are present in emotional status after observing (Alschuler et al. 2009; McGorry and Lin 2012), we won- others’ pain, we cannot confirm this suggestion. der whether these associations also count for the FRP-rs Furthermore, no significant differences were present in described in the current study. Still, the current data analysis execution of motor control during flexion of the spine, since of FRP-rs in normal spontaneous action seems promising in all subjects, the FRP-rs altered significantly. Despite the and is reliable in the test–retest. Recommendation is made to 1 3 Experimental Brain Research test the spontaneous FRP for differences in LBP patients and Conclusion healthy subjects in larger groups and to test for associations with clinical outcomes in future research. Observing others’ painful action increases fear and can alter Another limitation of the study was that validation of spontaneous motor control during execution of the same emotion by facial mimicry during observation of each activity in LBP patients as well as in healthy subjects. This video was not possible due to the artifacts in the facial mus- only occurs immediately after observing the painful video cles EMG recordings. It might be that crosstalk is present and is not present during strict protocolled movements. between the EMG electrodes: the phenomenon that elec- trical activity generated by a specific muscle spreads to Compliance with ethical standards adjacent areas through volume conduction (Boxtel 2001). Conflict of interest All authors declare that there is no conflict of in- Another impeding factor might have been that emotional terest. experiences under natural circumstances often consist of a mixture of elementary emotions, which in addition, may Open Access This article is distributed under the terms of the Crea- rapidly change so that EMG response patterns may thus be a tive Commons Attribution 4.0 International License (http://creat iveco function of such undetermined or dynamic emotional states mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- tion, and reproduction in any medium, provided you give appropriate (Boxtel van 2010). Furthermore, the human face does not credit to the original author(s) and the source, provide a link to the only display affective responses, but also produces a large Creative Commons license, and indicate if changes were made. variety of activities unrelated to emotional processes like speech, mental effort or mental fatigue, task involvement, startle reflexes, etc. (Boxtel van 2010). Hence, it was not possible to test the Emotional Questionnaire thoroughly for References its external validity. Additional research is necessary to vali- Ahern DK, Follick MJ, Council JR, Laser-Wolston N, Litchman H date the questionnaire. (1988) Comparison of lumbar paravertebral EMG patterns in Limitation of the current study is the small sample size. chronic low back pain patients and non-patient controls. Pain Further research in larger cohorts is necessary to confirm the 34(2):153–160 findings of the current study. 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Changes in spontaneous overt motor execution immediately after observing others’ painful action: two pilot studies

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Biomedicine; Neurosciences; Neurology
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Abstract

Research has demonstrated that motor control is directly influenced by observation of others’ action, stimulating the mir - ror neuron system. In addition, there is evidence that both emotion and empathy after observing a painful stimulus affects motor cortical excitability and reaction times. Aim of the present two pilot studies is a) to test for significant influence of observing other’s painful bending of the trunk on execution of the same activity in a self-directed bending action (study 1) and to compare these results with a bending action according to a strict bending protocol (study 2). In addition to study 1, differences between Low Back Pain (LBP) patients versus healthy subjects are tested. Video footage of a (1) neutral, (2) painful, and (3) happy bending action was presented in random order. Changes in flexion–relaxation phenomenon (FRP) of back muscles were studied directly after watching the videos with surface EMG, in study 1 during a self-directed bending action in LBP patients and healthy subjects, in study 2 according to a strict bending protocol. FRP ratios were calculated by a custom-made analysis scheme tested for sufficient reliability prior to both studies. Evoked emotions were measured with an Emotional Questionnaire after each video. A Mixed Model ANOVA was used to test for the effect video and the difference between LBP and healthy subjects on the FRP-rs. Differences in evoked emotion will be tested with a Wilcoxon Signed Rank Test. In study 1, 24 healthy controls and 16 LBP patients FRP-rs were significantly influenced after observing a painful video in all subjects versus a happy and neutral video (p = 0.00). No differences were present between LBP and healthy controls. All subjects experienced more fear after observation of the painful video (p 0.05). In study 2, 6 healthy subjects followed the strict FRP bending protocol for three times after observing each video. No significant changes occurred in FRPs per video compared to FRPs of six healthy subjects carrying out the spontaneous bending activity. Observing a painful action in another person changes motor performance and increases fear in both people with and without back pain, during self-directed trunk flexion, but not during a protocolled trunk flexion. Keywords Low back pain · Motor control · Action observation · Empathy · Mirror neuron system * Annelies Pool-Goudzwaard Introduction a.l.pool-goudzwaard@vu.nl Rehabilitation strategies in low back pain (LBP) patients Amsterdam Movement Sciences, Faculty of Behaviour and Movement Sciences, Vrije Universiteit Amsterdam, Van often focus on training trunk coordination, strengthening, der Boechorststraat 7, 1081BT Amsterdam, The Netherlands and endurance training of muscles of the trunk (Delitto Somt University of Physiotherapy, Amersfoort, et al. 2012). Theoretical basis for this intervention is alter- The Netherlands ations in motor control of lumbar spinal muscles demon- Department of Neuroscience, Faculty of Health Sciences strated to be present in this specific patient group (D’hooge and Medicine, ErasmusMC University, Rotterdam, et al. 2013a, b; Dickx et al. 2008; Geisser 2007; Hodges The Netherlands et al. 2001, 2003; Kalichman et al. 2010; MacDonald et al. Menzies Health Institute Queensland, Griffith University, 2010; Tsao et  al. 2010; Etemadi et  al. 2016; Sánchez- Gold Coast, Australia Zuriaga et al. 2015). Typical for altered motor control is Faculty of Psychology and Educational Sciences, Open the change in paraspinal muscle activity during forward University of the Netherlands, Heerlen, The Netherlands bending in these patients, the so-called flexion–relaxa- School of Health and Rehabilitation Sciences, The University tion phenomenon (Ahern et  al. 1988; Alschuler et  al. of Queensland, Brisbane, Australia Vol.:(0123456789) 1 3 Experimental Brain Research 2009; Ambroz et al. 2000; Geisser et al. 2000; Watson Even more, mirror neurons are also directly influenced et al. 1997; Sanchez-Zuriaga et al. 2015). Among normal by emotions (Enticott et  al. 2008, 2011, 2012; Gazzola healthy subjects, activity of the lumbar paraspinal mus- et al. 2006; Budell et al. 2015). A study revealed the effect cles during flexion initially increases, and then decreases of observation of emotion in others on motor cortex excit- as the ligaments begin to support the trunk as the angle ability, providing support that direct emotion perception is of flexion increases (Alschuler et al. 2009). However, in closely linked to action systems (Borgomaneri et al. 2012). people with LBP, this paraspinal relaxation in maximum This is in line with several studies, indicating that empathy voluntary flexion tends to be absent or decreased (Ahern for people in pain may be based on ‘mirror-matching’ simu- et al. 1988; Alschuler et al. 2009; Ambroz et al. 2000; Col- lation of others’ state (Gallese 2003; Morrison 2004; Singer loca and Hinrichs 2005; Descarreaux et al. 2008; Geisser et al. 2004; Budell et al. 2015). Avenanti and Aglioti (2006) 2007; Maher et al. 2005; Mayer et al. 2009; Watson et al. demonstrated that not only the affective nodes in the pain 1997; Schinkel-Ivy et  al. 2013; Sanchez-Zuriaga et  al. network are concerned with empathy for pain, but also the 2015). The assumption is that this altered motor control is sensomotoric side (Avenanti and Aglioti 2006). Avenanti due to anticipation of the presence of LBP (Hodges et al. et al. (2009a, b) demonstrated that an onlooker to a needle 2003; Moseley and Hodges 2005) leading to a “smudg- penetration of a models hand leads to diminished cortical ing of the brain” on the sensory motor cortex and pos- excitability specific for the muscle and hand observed to be sibly an altered neural drive of muscles (Tsao et al. 2010; penetrated. In contrast, observing a needle penetration in one Chiou et al. 2014). Motor control deficits as demonstrated other’s hand leads to a generalized corticospinal excitability by alteration of the flexion–relaxation phenomenon are of the opposite hand, leading to a possible freezing response indeed associated with the clinical status of people with (Avenanti et al. 2009a, b). However, the participants in these LBP (Schinkel-Ivy et al. 2013). A significant association studies were not active nor any action was required. One exists between the flexion–relaxation phenomenon ratio might discuss whether motor action preparation and activ- (FRP-r) (i.e., the ratio between activity at maximal flexion ity could have an effect on these results. Indeed, Morrison and during extension) and measures of perceived disabil- et al. (2007) demonstrated altered reaction times such as ity, a measure of clinical pain, pain-related fear as well speeding withdrawal response and slowing approach move- as range of motion during flexion and elicitation of pain ments with the hand/finger pressing keys when observing a during straight leg raise (Alschuler et  al. 2009). Based needle pricking a finger (Morrison et al. 2007). Gallang et al. on these findings, it seems logical to train motor control (2017) stated that these responses contrast muscle specific deficits in LBP patients. inhibition after pain observation often found in transcranial Since rehabilitation in people with LBP often take magnetic stimulation (TMS) studies. Furthermore, Gal- place in groups, especially in a multidisciplinary setting lang et al. (2017) demonstrated that participants actually another important factor can influence motor control in responded faster (increased excitability) after observation of these patients. Motor control of muscles is also influenced a painful stimulus to the hand than a non-painful stimulus, by observation of others. Observing someone performing irrelevant if the participants responded with the foot or the an action is known to influence motor execution and even hand. Even more, the delay (500 ms) of a Go/No go signal motor skills (Ferrari 1996; Hodges et al. 2007; Lepage even increased the speed of the response. It seems that sen- et al. 2010; Vogt and Thomaschke 2007; Wulf and Mornell sorimotor contagion of emotion leads to altered excitability, 2008; Murata et al. 2016; Behrendt et al. 2014; Morrison studied by reaction times to a Go/No go task after observing et  al. 2007). The neuronal mechanism of this influence a painful stimulus. However, these studies cannot answer the may rely on the mirror neuron system. Mirror neurons are question whether people with LBP in a rehabilitation group neurons that are activated not only during the execution might be influenced in their overt motor activity by observ - of an action, but also during the observation of the same ing others in pain. After all, these people with LBP do not action performed by someone else (Di Pellegrino et al. observe “a painful damaging stimulus” but a painful activ- 1992; Fadiga and Craighero 2003; Gallese et al. 1996; Gal- ity in others, nor have to respond in a predefined activity to lese 2003). Results from experimental studies demonstrate this stimulus as quickly as possible. Still, these patients will facilitation of movement execution (Villiger et al. 2011), observe others moving with pain while performing the same specifically of the initiation and optimization of move- functional activities. ment, when observing congruent action in others (Ménoret The aim of the first pilot study was (a) to demonstrate et al. 2013). Murata et al. (2016) state that control of one’s differences in an overt bending motor action measured with own action and the mirror neuron system are shared with EMG, after watching a painful bending activity versus a the “who” system, which is related to the recognition of bending activity in a neutral and happy condition and (b) action. whether this is different for people with LBP and healthy controls. The aim of the second study was to demonstrate 1 3 Experimental Brain Research the differences between following a strict bending protocol of a few seconds bending forward, a few seconds maximal versus a self-directed bending action after observing the flexion and a few seconds extension of the lumbar spine same videos. (Ahern et al. 1988; Alschuler et al. 2009; Ambroz et al. 2000; Geisser et al. 2000; McGorry and Lin 2012; Watson et al. 1997). We hypothesized that after watching a painful Materials and methods bending action, the motor excitability of the trunk muscles would be increased and that the relaxation of the erector Design spinae muscles would not occur while bending, even more evident in LBP patients. Two fundamental experimental pilot studies have been per- For the first experiment, we decided that the official flex- formed. Medical ethical approval was obtained by the Open ion relaxation protocol being a predefined time framed pro- University of The Netherlands. tocol of flexion and extension of the trunk did not reflect normal movement patterns as bending forwards in healthy Study 1 subjects nor in LBP patients during rehabilitation programs. We decided to focus on a spontaneous change in the flex- Participants ion relaxation phenomenon evoked by observing a similar bending activity in others. Therefore, we adapted the flexion For the first study, healthy subjects (n = 24) are recr uited relaxation protocol to a more spontaneous activity as pick- from the Department of Neuroscience at the ErasmusMC ing up an object, like a wallet from the ground. At first, we University, Rotterdam. People with LBP (n = 16) are established a mean standardized time frame by measuring recruited from primary care physiotherapy clinic. All sub- the speed of picking up a wallet from the ground multiple jects voluntary participated in the study after reading an times prior to the research. A mean standardized time frame information flyer and signed an informed consent. Inclusion could be calculated of 0.1-s maximal voluntary flexion after criteria were age between 20 and 60 year old en being able to bending forward picking up the wallet and 0.3 s coming up read and understand Dutch. Exclusion criteria were specific straight. During the experiment, continuous SEMG meas- LBP due to malignant processes and systematic disease as urements were performed of the erector spinae muscles high well as inability to bend forward. (height L1) and low (height L4) (see Fig.  1a). All EMG electrodes were connected to a portable EMG registration Questionnaires system (TMS porti: Twente Medical Systems International, Oldenzaal, The Netherlands). EMG signals were band pass Prior to the measurements, all subjects filled in a question- filtered (10–1000 Hz). A Notch filter of 50.2–49.8 Hz sup- naire containing the Roland Disability Questionnaire (RDQ), pressed possible power-line interference of 50 Hz. a pain Numeric Rating Scale (NRS) and additional questions For study 1, we measured not only erector spinae activity on socio-demographic data. The Roland disability question- with SEMG, but also facial muscles: the frontalis, corrugator naire has proven sufficient to good reliability and validity supercilii, orbicularis oculi, and zygomaticus major on the to measure disability due to LBP (Smeets et al. 2011). The left and right sides (Lapatki et al. 2010) (see Fig. 1b). NRS is a scale between 0 (no pain) and 10 (excruciating Increased activity in facial muscles can be used in two pain). The psychometric qualities of both instruments are ways. At first, increased activity of facial muscles can be good (Ostelo and de Vet 2005; Soer et al. 2012; van der used as a reference for maximal bending forward, since Roer et al. 2006). With a positive score on the RDQ > 0 and activity in facial muscles increases during extension after NRS > 0, a subject entered the LBP group. Prior and during bending forward. An intensity graph of SEMG of the facial the measurements, an “Emotional Questionnaire” was used. muscles plotting the amplitude in color versus time demon- This is a small questionnaire scoring six separate emotions strated the highest activity in facial muscles related to bend- (surprise, happiness, fear, irritation, disgust, and sadness) ing forward and maximal flexion (see Fig.  2). SEMG data on a five-point Likert scale from not at all present (0) to during the mean standardized time frame of 0.1 s of maximal very strong (5). flexion and 0.3 s extension with the highest facial activity were used for analysis. Second, increased activity of facial Bending motor action–flexion relaxation phenomenon muscles can reveal the subjects’ affective state evoked by the videos (de Wied et al. 2006; Ekman et al. 1981; Lapatki In the literature, the flexion–relaxation phenomenon (FRP) et al. 2010; Larsen et al. 2003). These positive and negative is described as relaxation of the paraspinal Erector Spinae affective states can be reliably distinguished by facial EMG muscle in full flexion. This can be measured by Surface (Larsen et al. 2003). Electro-MyoGraphy (SEMG) during a predefined protocol 1 3 Experimental Brain Research Fig. 1 Electrode position of the back muscles (a) and on the face (b) we tested the test–retest reliability in ten healthy subjects Experimental setup and protocol executing 3 × 3 bending actions (ICC 0.67 during flexion and 0.78 during extension). Since ICC was sufficient, we All subjects were measured in a separate area, created by room dividers, to avoid emotional contagion and EMG decided that one measurement could be used per video in study 1. During study 1, the bending action was carried out activity by the presence of the researchers (see Fig. 3). All subjects sat on a chair behind a table on which two printed by placing a wallet on a mark on the ground beside the table. After each video, the subject was instructed to pick up the emotional questionnaires were placed. All subjects watched three separate custom-made videos: (a) a video with a per- wallet and to sit down on the chair and fill in one emotional questionnaire. After completion, the subject was instructed son picking up a wallet from the floor extending to erect posture and walking on (neutral video); (b) picking up the to return the wallet to the marking on the ground. All sepa- rate actions (start video, emotion evoking moment during same wallet hardly able to raise himself to erect posture due to excruciating acute LBP (painful video); and (c) picking the video, ending of the video, standing up, bending for- ward, return to chair, etc.) were marked with a marker on the up the same wallet coming to erect posture with someone else responding enthusiastic and glad that their wallet was 16th channel of the SEMG-recording system. After the final video, the subjects were asked to stand erect for 3 s, while found (happy video). The videos were displayed in random order on a projection screen in front of them, one ‘condi- three consecutive SEMG “rest activity” measurements were performed of the erector spinae muscles to make it possible tion’ video (3 conditions neutral, happy and painful) per subject. We choose not to repeat any videos to mimic ‘nor- to normalize SEMG data by dividing the SEMG value dur- ing the flexion and extension by the mean average SEMG mal life observing other subjects bending and raising again as well as LBP patients in a rehabilitation clinic since view- during standing of the same erector spinae muscle. ing another LBP patient hurting his or her back, hardly able to raise again. It is not natural for such a patient to repeat this movement over and over. This indicated that we could only execute one bending action per video. Prior to study 1, 1 3 Experimental Brain Research Fig. 2 Three seconds of SEMG data registered after the marker signalling picking up a wallet. The upper part shows the inten- sity graph of facial muscles, the lower part shows the 4 channels of the erector spinae muscles (9, left erector spinae high; 10, right erector spinae high; 11, left erector spinae low; 12, right erector spinae low). The 0.1 s of maximal flexion and 0.3 s of extension as a fixed time frame are selected at the location of most increased facial activity Data analysis when calculating normalized values for maximal voluntary flexion and 0.78 for normalized extension. In study 1, data analysis was performed in a custom-made Affective facial EMG responses were calculated using the smoothed, rectified maximum EMG output during a LabVIEW 8.2 application-DaqSys 16 player. Three com- plete seconds of data after markers 3 and 9 (indicating short interval of 100 ms after each marker related to the emotion evoking moment in the pain and happy videos. picking up the wallet from the floor directly after watching the videos) were used. The FRP was localized by study- These max. EMG values per muscles and side were stand- ardized as a proportion of 3  s of baseline EMG ampli- ing SEMG activity of the erector spinae muscles (four channels) (see Fig.  1). At first, SEMG data during the tudes per subject (Boxtel van 2010). Higher proportions of zygomaticus major and orbicularis oculi muscle activity flexion relaxation phenomenon of all erector spinae chan - nels were normalized by dividing the maximum SEMG are expected during an elementary positive emotion of happiness, while frontalis and corrugator supercilii mus- during extension and the average SEMG during maximal flexion by the mean SEMG of 3 s of rest activity in stand- cle activity is expected during a pain-related or negative emotion like fear, anger, or sadness (Boxtel van 2010). ing. According to the strict analyses protocol to define the Flexion–Relaxation Phenomenon ratio (FRP-r) with the Statistical analysis highest association with clinical measures in LBP patients as pain and disability (Alschuler et al. 2009), the FRP-r To demonstrate changes in emotional status after observa- was calculated by dividing the normalized maximum SEMG during extension (0.3  s) to the average normal- tion of a painful, happy, or neutral video, at first, all scores were calculated for change from the initial values on the ized SEMG during maximal voluntary flexion (0.1 s) (Als- chuler et al. 2009), see Fig. 4 for the signal processing flow emotional questionnaire to eliminate confounding effect of higher scores on emotional status prior to the measurement. of the SEMG. Reproducibility of this procedure in obser- vation of a pain-free video was tested with 3 × 3 repetitions These delta scores per video were tested for significant dif- ferences overall and per group (LBP versus healthy subjects) per video in ten healthy subjects, prior to this research and demonstrated an intra-class correlation coefficient of 0.67 1 3 Experimental Brain Research Fig. 3 Experimental setup using a Wilcoxon signed rank test and a Mann–Whitney U Study 2 test, respectively. Differences in affective state (positive versus negative Subjects facial EMG muscle activity) evoked by the videos were tested for significant difference between positive and nega- For the second study, students and employees of the VU tive facial mimicry using a Paired T test. University in Amsterdam were asked to participate. With A Mixed Model ANOVA was used to test for the effect a difference in FRP-rs of 1.1 between the healthy sub- of the observed video and the difference between LBP jects watching a painful (2.6 ± 0.9) versus a neutral video and healthy subjects on the FRP-rs, with the three video (1.55 ± 0.7) and the expectation that this similar difference conditions (Painful, Happy, and Neutral) as a within-sub- will be present between a flexion relaxation phenomenon jects factor and participant type (LBP and Healthy) as the according to a strict protocol and a non-strict protocol with between-subjects factor. Possible confounding effect of order an alpha of 0.05 and a power of 0.8, we need a sample size of videos was taken into account. All data were tested for of n = 12 (n = 6 for the strict protocol and n = 6 for the spon- normal distribution. Logistic transformation of all skewed taneous action). The last group will be derived from study 1 data was carried out prior to statistical analysis. by an ad random selection of every fourth healthy subject. The same Mixed Model ANOVA was used to test for the Another six healthy subjects participated in study 2. effect in the second study. Protocol The protocol described by McGorry and Lin (2012) was followed to measure the FRP in study 2 with standing still for 4 s, bending forwards in 4 s, remaining fully flexed for 1 3 Experimental Brain Research Fig. 4 Signal flow and process- ing 4 s and extending for 4 s. For study 2, we recorded and cal- Statistical analyses culated the movements of the spine using an optical tracking system Optotrak, reading two markers on the dorsal side of Another Mixed Model ANOVA was used to test for the the spine at the height of L1 and L5. A marker signal was effect of the observed video with the three video conditions used to synchronize the data of the EMG with the output of (Painful, Happy, and Neutral) as a within-subjects factor. As Optotrak. between-subjects factor the effect of either or not following, Data analyses were performed in a custom-made Matlab a strict FRP protocol was used. R2014b application. Again, all SEMG data during the flex- ion relaxation phenomenon of all erector spinae channels were normalized. During four seconds of maximal flexion Results measured by Optotrak, mean SEMFG of a same time frame as in study 1 of 0.1 s was calculated as well as 0.3 s during As described, 40 subjects participated in study 1 16 LBP the extension. According to the same pre-described protocol, patients and 24 healthy controls and 6 healthy subjects in FRP-rs were calculated as in study 1. study 2. Socio-demographic data are shown in Table 1. No 1 3 Experimental Brain Research significant differences are present between LBP patients and present throughout all videos in all facial muscles. Since healthy controls on socio-demographic data and initial val- low-frequency artifacts such as eye blinking and/or other ues on the EQ. Cronbach’s alpha for internal consistency for movements like activity of neighboring muscles, swallow- positive labeled emotions on the EQ (surprise and happi- ing, etcetera were interfering with the facial data we ques- ness) was 0.67. The Cronbach’s alpha of the negative labeled tioned these data for reliability and did not perform statisti- emotions (fear, irritation, disgust, and sadness) was 0.88. cal analysis on this data. Evoked emotion Influence of observation of pain on FRP‑rs All median scores on changes in emotional status after Differences between FRP-rs per video are displayed in observation of the videos are 0 (see Table 2 for study 1). In Graph 1. Higher FRP-rs are present in the painful condi- the overall group, there is a significant difference of feeling tion versus the neutral and happy condition, indicating more fear (p < 0.05) after observation of a painful action in relatively more f lexion relaxation (less activation) of the both groups with respect to the neutral and happy video in erector spinae at full trunk f lexion. study 1. This, however, is not present in study 2. In study 1, Since sphericity was not present (χ = 1.2, p > 0.05, df significant less fear is present in healthy controls after watch- 1.98 was corrected by Greenhouse–Geisser. The mixed ing a happy video with respect to the pain patients. model ANOVA demonstrates a significant effect of video In contrast with our expectation, EMG facial activity in as a within subject effect F = 3.26, p < 0.05. Follow-up the 100 ms interval after the marker related to emotion evok- paired t tests demonstrated a significant difference in (log ing moment did not show a single peak of muscle activity transformed) FRP-rs after observing the painful video after a “still” period. Multiple peaks in muscle activity were (Mn 0.72, SD 0.37) and after observing the neutral video Table 1 Socio-demographic Subjects All (n = 40) HC (n = 24) LBP patients (n = 16) HC study 2 data and initial values on the EQ Gender (F/M) 19/21 11/13 8/8 4/2 Age (years) 35 (SD ± 12.1) 34 (SD ± 12.3) 37 (SD ± 11.9) 27 (SD ± 11.9) Outcome questionnaires  NRS (mean SD, min, max) 0 4 (SD ± 2.5) min 2, max 7 0  RDQ 0 5.2 (SD ± 4, min 0, max 19) 0 EQ  Surprise 1 (SD ± 0.6) 1 (SD ± 1.1) 0 (SD ± 0.3)  Happiness 2 (SD ± 0.7) 1.5 (SD ± 1.0) 0 (SD ± 0.6)  Fear 0 (SD ± 0.2) 0 (SD ± 0.4) 0 (SD ± 0.1)  Irritation 0 (SD ± 0.2) 0 (SD ± 0.7) 0 (SD ± 0.2)  Disgust 0 (SD ± 0.1) 0 (SD ± 0.3) 0 (SD ± 0.1)  Sadness 0 (SD ± 0.3) 0 (SD ± 0.5) 0 (SD ± 0.1) LBP low back pain, SD standard deviation, F/M female/male, NRS numeric rating scale, RDQ Roland dis- ability questionnaire, EQ emotional questionnaire Table 2 Mean changes in scores per emotion on the emotional questionnaire after observation of a painful (P), neutral (N) and a happy (H) video, overall and per subgroup in study 1 Subjects All (n = 40) HC (n = 24) LBP patients (n = 16) EQ (± SD) N P H N P H N P H  Surprise 0.33 (0.7) 0.23 (0.7) − 0.03 (0.9) 0.30 (0.7) 0.22 (0.6) 0.0 (0.9) 0.38 (0.7) 0.25 (0.9) − 0.8 (0.8)  Happiness 0.08 (0.6) − 0.03 (0.7) − 0.67 (0.7) − 0.04 (0.5) − 0.13 (0.7) 0.65 (0.7) 0.25 (0.7) 0.13 (0.6) 0.69 (0.6)  Fear 0.05 (0.2) − 0.08* (0.3) 0.03 (2.9) 0.4 (0.2) 0 (0) − 0.4* (0.2) 0.06 (0.2) − 0.06 (0.4) 0.15 (0.3)  Irritation 0.03 (0.2) 0.08 (0.4) 0.22 (0.6) 0.5 (0.2) 0.13 (0.5) 0.13 (0.5) 0 (0) 0 (0.4) 0.38 (0.9)  Disgust 0 (0) 0,13 (0.5) 0 (0.2) 0 (0) 0.14 (0.4) 0 (0) 0 (0) 0.13 (0.6) 0 (0.4) No significant differences are present neither between both videos nor between patients versus healthy subjects *p < 0.05 1 3 Experimental Brain Research immediately after observing other’s painful action. The fact that observing others’ painful motor action alters one’s own motor action is relevant, especially for LBP patients training together always observing others’ painful action. The higher FRP-rs present while observing a painful bend- ing action, in all subjects, indicate relatively more flexion relaxation (less activation) of the erector spinae at full trunk flexion. This is not present after observing a neutral or happy bending condition. From a clinical point of view it is relevant that in all subjects observation of pain alters motor execution of a spontaneous similar action. LBP patients often display pain behavior when bending forward or lifting objects. Meanwhile, LBP patients, especially Graph 1 Mean FRP-rs ± standard deviation (SD) per video in LBP with a chronic condition, are often trained in groups with patients and healthy controls an emphasis on graded activity. Seeing another patients´ pain behavior might interfere with a patients’ own motor control. Clinicians should be aware of this phenomenon. In addition, execution of motor control of healthy spouses or friends of these patients might be influenced as well. Still, we have to be careful in drawing firm conclusions on both pilot studies. Confirmation of these findings in a larger study is necessary for more robust proof. Altered FRP-rs are a new finding which is supplemen- tary to the knowledge we have on the influence of observa- tion others’ pain on motor excitability. It seems that not only motor excitability and reaction times in motor execu- tion alters after observation of a painful stimulus to the hand, but also by seeing others’ painful activity executing the same action (Ferrari 1996; Hodges et al. 2007; Lepage et al. 2010; Vogt and Thomaschke 2007; Wulf and Mornell 2008; Murata et al. 2016; Behrendt et al. 2014; Morrison Graph 2 Mean FRP-rs/standard deviation (SD) per video in healthy subjects with a strict FRP protocol versus spontaneous bending action et al. 2007). Emotional status {Mn 0.23, SD 0.52 [t(60) = 6.83 p = 0.00]} as well as the happy video [Mn 0.31, SD 0.58, t(60) = 4.87, p = 0.00]. The current study has demonstrated that the emotional sta- No significant differences were present in FRP-rs after tus of the observer can significantly be influenced directly observing a happy or a neutral video. The between-sub- by a negative stimulus like observing others’ pain. All jects effects were not significant. No significant effect subjects scored more fear on the emotional questionnaire was present by order of video. after observing a painful video. The findings are in line No significant within-subjects effects were present with results from the literature. Data have been presented of observing a video nor between-subjects effects in the on the influence of observation of pain in humans. Seeing strict protocol condition between in study 2 (see Graph 2). painful or unpleasant stimuli may elicit arousal or aversion (personal distress) reactions (Williams 2002). We have to be careful to draw firm conclusions, since the reliability Discussion of the emotional questionnaire is not tested and the data cannot be confirmed by facial mimicry (EMG of facial Main finding of the current pilot study is that observing an muscles). Furthermore, the number of subjects is small. overt painful motor bending action of the trunk increases fear in the observers and significantly alters the execu- tion of the congruent painful action. It seems, this only takes place when the motor activity is spontaneous and 1 3 Experimental Brain Research fact that research demonstrated that recalled pain as in physi- Influence of observation of others’ pain on motor execution in all subjects cal pain conditions reveals significant activation in mostly similar affective pain processing brain structures, including It has been reported in the literature that the intensity of bilateral anterior insula, anterior cingulate cortex (ACC), and thalamus (Fairhurst et al. 2012), this does not lead to someone else’s pain is negatively correlated to changes in cortical excitability of the observer, in healthy subjects different executions of motor control in LBP patients. Actu- ally, to what extend recall of pain can play a role in motor (Avenanti and Aglioti 2006; Singer et al. 2004). Further- more, it has been reported that negative stimuli prior to the execution is not clear. Further research is necessary to study a possible influence of the pain resonance system in pain observation of transitive hand movements facilitated cortical spinal excitability as well (Enticott et al. 2012; Hill et al. patients on motor execution. 2013). In addition, Hajcak et al. (2007) have been demon- strating increased motor cortex excitability in participants Strengths and limitations who viewed pleasant and unpleasant compared to neutral images. Although we did not study motor cortex excitability Strength of the current study is that this is the first study focusing on motor execution in relation with the model of but motor execution, we could not demonstrated influence of a pleasant (happy) stimulus. Our findings do seem to sup- empathy observing others’ low back pain. Main limitation of the study is that only one trial per port the other above-mentioned studies by demonstrating significant differences in motor execution by observing oth- video has been performed in study 1. Therefore, we tried to test the effect of repeated measurements on motor execution ers’ pain. This is in line with the finding of motor response changes to observing others’ pain in a pain population prior to study 1. Calculating a mean of three trials would have been more robust. However, the effect of observing a (amputees) (Fitzgibbon et al. 2010a, b). Since motor execu- tion changed in all subjects after observing a painful video video on spontaneous motor execution was not present dur- ing repeated measures according to FRP protocol. and this phenomenon did not occur after observing a happy or neutral video, it seems that especially, the negative stimu- Regarding the spontaneous motor execution, the fact that the test–retest reliability in healthy subjects after observing lus of observing others’ pain was the trigger. However, from the current study, we cannot conclude which processes take a neutral video was sufficient supports the reliability of the data despite the fact that only one trial per video per subject place within the brain. The overall emotional status of more fear in all subjects and/or empathy for pain and/ or ‘mirror- was performed. Still, the findings are not very robust. This is why we recommend a repetition of the study in a larger matching’ simulation of others’ state (Gallese 2003; Mor- rison 2004; Singer et al. 2004) or even other pain processes sample size. In the current study, we have chosen to measure the FRP-r can play a role. The fact that in the healthy subjects in study 2, no significant change in evoked emotion was present and during a normal activity like picking up a wallet. Reason for this was the fact that a video of a flexion of the lumbar spine that also no effect was present in change in motor execution could indicate that emotions can play a role. Further research during a preprogrammed time schedule would interfere with the execution of the same spontaneous action as in the video. is necessary to demonstrate which pain processing take place during observation of someone else’s pain and execution of Furthermore, research does underpin the notion that mirror neurons are more sensitive to “object- and goal-orientated” motor control. movement (Enticott et al. 2011). Therefore, picking up a wallet is more appropriate in stimulating mirror neurons, but No differences between healthy subjects and low is different from the preprogrammed timed flexion–relaxa- back pain patients tion phenomenon described in the literature, which was car- ried out in study 2 (Ahern et al. 1988; Alschuler et al. 2009; We anticipated for differences to occur after observing oth- Ambroz et al. 2000; Geisser 2007; McGorry and Lin 2012; ers’ pain between LBP patients and healthy subjects both in Watson et al. 1997). Indeed, study 2 did not result in any evoked emotion as in motor execution. However, no signifi- positive findings. The scores of study 1 are not compara- cant differences were present. Valeriani et al. (2008) sug- ble to the outcome on FRP-rs in the literature. Although gested that being in pain might bias the empathic relation we have chosen the most optimal analysis of FRP-r with with others (Valeriani et al. 2008). Since no differences at regard to association with clinical outcomes in LBP patients group level are present in emotional status after observing (Alschuler et al. 2009; McGorry and Lin 2012), we won- others’ pain, we cannot confirm this suggestion. der whether these associations also count for the FRP-rs Furthermore, no significant differences were present in described in the current study. Still, the current data analysis execution of motor control during flexion of the spine, since of FRP-rs in normal spontaneous action seems promising in all subjects, the FRP-rs altered significantly. Despite the and is reliable in the test–retest. Recommendation is made to 1 3 Experimental Brain Research test the spontaneous FRP for differences in LBP patients and Conclusion healthy subjects in larger groups and to test for associations with clinical outcomes in future research. Observing others’ painful action increases fear and can alter Another limitation of the study was that validation of spontaneous motor control during execution of the same emotion by facial mimicry during observation of each activity in LBP patients as well as in healthy subjects. This video was not possible due to the artifacts in the facial mus- only occurs immediately after observing the painful video cles EMG recordings. It might be that crosstalk is present and is not present during strict protocolled movements. between the EMG electrodes: the phenomenon that elec- trical activity generated by a specific muscle spreads to Compliance with ethical standards adjacent areas through volume conduction (Boxtel 2001). Conflict of interest All authors declare that there is no conflict of in- Another impeding factor might have been that emotional terest. experiences under natural circumstances often consist of a mixture of elementary emotions, which in addition, may Open Access This article is distributed under the terms of the Crea- rapidly change so that EMG response patterns may thus be a tive Commons Attribution 4.0 International License (http://creat iveco function of such undetermined or dynamic emotional states mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- tion, and reproduction in any medium, provided you give appropriate (Boxtel van 2010). Furthermore, the human face does not credit to the original author(s) and the source, provide a link to the only display affective responses, but also produces a large Creative Commons license, and indicate if changes were made. variety of activities unrelated to emotional processes like speech, mental effort or mental fatigue, task involvement, startle reflexes, etc. (Boxtel van 2010). Hence, it was not possible to test the Emotional Questionnaire thoroughly for References its external validity. Additional research is necessary to vali- Ahern DK, Follick MJ, Council JR, Laser-Wolston N, Litchman H date the questionnaire. (1988) Comparison of lumbar paravertebral EMG patterns in Limitation of the current study is the small sample size. chronic low back pain patients and non-patient controls. Pain Further research in larger cohorts is necessary to confirm the 34(2):153–160 findings of the current study. Furthermore, the data might Alschuler KN, Neblett R, Wiggert E, Haig AJ, Geisser ME (2009) Flexion-relaxation and clinical features associated with chronic be disturbed by selection bias. All healthy subjects were low back pain: A comparison of different methods of quantifying volunteers from the department of Neuroscience. Yet, none flexion-relaxation. Clin J Pain 25(9):760–766 of them knew the research questions and hypothesis, so the Ambroz C, Scott A, Ambroz A, Talbott EO (2000) Chronic low back influence on selection bias is not large. pain assessment using surface electromyography. J Occup Environ Med 42(6):660–669 Another limitation of this study was that per condition Avenanti A, Aglioti SM (2006) The sensorimotor side of empathy for (Happy, Neutral, Painful) only one video was viewed to all pain. Psychoanalysis and neuroscience (pp 235–256) Springer, subjects. This is in contrast with (Avenanti and Aglioti 2006; Berlin Avenantie et al. 2009; Gallese 2000), Morrison et al. (2007), Avenanti A, Minio-Paluello I, Bufalari I, Aglioti S (2009a) The pain of a model in the personality of an onlooker: Influence of state- and Galang et al. (2017) who repeatedly > 18 times showed reactivity and personality traits on embodied empathy for pain. the painful stimulus video. In our view, since our experiment NueroImage 44:275–283 tends to relate the findings to the clinic, we could not show Avenanti A, Minio-Paluello I, Sforza A, Aglioti S (2009b) Freezing or the painful video over and over again. After all, it is unusual escaping? Opposite modulations of empathic reactivity to the pain of others. Cortex 45:1072–1077 in the clinic when an LBP patient is hurting his or her back Behrendt F, de Lussanet MH, Wagner H (2014) Observing a move- during bending and is hardly able to rise anymore that he or ment correction during walking affects evoked responses but not her will repeat this action. We acknowledge by only dem- unperturbed walking. 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Experimental Brain ResearchSpringer Journals

Published: Jun 7, 2018

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