Accepted Manuscript

Muscle synergies during bench press are reliable across days

Mathias Kristiansen, Afshin Samani, Pascal Madeleine, Ernst Albin Hansen

PII: S1050-6411(16)30052-9
DOI: http://dx.doi.org/10.1016/j.jelekin.2016.06.004
Reference: JJEK 1982

To appear in: Journal of Electromyography and Kinesiology

Received Date: 25 September 2015
Revised Date: 11 May 2016
Accepted Date: 8 June 2016

Please cite this article as: M. Kristiansen, A. Samani, P. Madeleine, E.A. Hansen, Muscle synergies during bench
press are reliable across days, Journal of Electromyography and Kinesiology (2016), doi: http://dx.doi.org/10.1016/
j.jelekin.2016.06.004

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Muscle synergies during bench press are reliable across days

Authors

Mathias Kristiansen1, Afshin Samani1, Pascal Madeleine1, Ernst Albin Hansen1

Institution
1
Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology,
Aalborg University, Aalborg, Denmark

Corresponding Author:
Mathias Kristiansen, MSc, Physical Activity and Human Performance group, Center for
Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg
University, Fredrik Bajers Vej 7 E2, DK-9220, Aalborg, Denmark.
Tel +45 26803461

Fax +45 98154008

E-mail: mvk@hst.aau.dk

Keywords:

Bilateral arm movement, Motor modules, Muscle coordination, Neural adaptations,

Repeatability, Strength training

1

1. Introduction

For successful execution of movement, both timing and pattern of activation of all involved

muscles need to be well coordinated. However, at the moment there are unknown aspects of

how the central nervous system controls the muscles involved in movements. One theory on

how the central nervous system controls human movement, infers that movements to a large

extent are controlled by a combination of a few basic activation patterns, also known as

motor modules or muscle synergies [Bernstein, 1967; Ivanenko et al, 2006; Lacquaniti et al,

2012]. A muscle synergy can be characterized as a low dimensional organizational structure

controlling multiple muscles. These neural coordinative structures are thought to be located at

spinal level, and to be controlled by motor cortical areas and affected by afferent systems

[Bizzi and Cheung, 2013]. Muscle synergies have thus been suggested to provide a simplified

strategy for the nervous system to control movements [Bernstein, 1967; D'Avella and Bizzi,

2005; Hug, 2010; Ivanenko et al, 2006; Torres-Oviedo et al, 2006; Torres-Oviedo and Ting,

2007]. Indeed, a few basic patterns have been shown to adequately describe a number of

various movements in humans such as reaching in the horizontal plane [Muceli et al, 2010;

Muceli et al, 2014] standing [Krishnamoorthy et al, 2003; Torres-Oviedo and Ting, 2007],

walking [Ivanenko et al, 2004; MacLellan et al, 2014; Oliveira et al, 2014], running

[Cappellini et al, 2006], pedaling [Dorel et al, 2009; Hug et al, 2010; Hug et al, 2011], rowing

[Turpin et al, 2011a; Turpin et al, 2011b], bench press [Kristiansen et al, 2015b], and

backward giant swing [Frère and Hug, 2012].

To study inter-muscular coordination during movements, muscle synergies can be

extracted from multiple surface electromyography (EMG) signals using a nonnegative matrix

2

there are to the best of the authors’ knowledge not any reports available on within.0±12. 2011]. 2010].4±25. The extraction of muscle synergies offers unique insight into the combined timing and activation patterns of multiple muscles during movements.2±26.1 kg and 109. Investigations reporting both the absolute and relative reliability are needed to provide evidence that muscle synergy analyses based on nonnegative matrix factorization are clinically and experimentally sound. Materials and methods 2. 2006] and to be robust in human balance control across different biomechanical contexts in humans [Torres-Oviedo and Ting.1. age 24. three repetition maximum (3RM) in bench press at first and second test session 109. Muscle synergies are reported to be consistent across a variety of postural perturbations in cats [Torres-Oviedo et al.5±13. However. all participants had performed full body strength training for 2-3 times per week for at least two years.8 kg.81±0.05. Participants Healthy male individuals (n=21. Considering the consistency and robustness of muscle synergies.07 m.and between-day reliability of the method. The presentation of this reliability study follows the guidelines for reporting reliability and agreement studies [Kottner et al.9 kg) volunteered for participation in the current study. body mass at first and second test session 88. the aim of the study was to evaluate the between-day reliability of applying nonnegative matrix factorization to EMG data collected during bench press. height 1.5±2. At the time of data collection. Consistency has also been reported for pedaling [Hug et al. 3 . we hypothesized that muscle synergies describing bench press would be reliable across days. 2.factorization algorithm.1 kg and 89. 2011]. The number of participants was determined using an α level set to 0.2 years (mean±standard deviation (SD)). Thus.

p0 to 0. the participants performed the following: warm up. 1998]. back and upper body. bench press is a demanding and complex bilateral arm movement. Oliveira et al.7.2±2. It was necessary to apply a submaximal intensity level during the bench press that was used for investigation of reliability as a minimum of 20-40 cycles are required during cyclic tasks to obtain representative EMG data [Hug. while handling a heavy load. laboratory environment and test equipment. As there are no conclusive recommendations on how to normalize EMG data. p0 and p1 denotes the minimally acceptable level of reliability and the expected level of reliability. we used a task-specific submaximal 4 . and n to 2 [Walter et al. For trained individuals. α level and β level denotes the probability of making a type 1 and type 2 error. respectively. Approximately one week after the familiarization session. one set of 3 repetitions at 75% of the 3RM load for normalization. respectively. Table 1 near here 2. The purpose of the first session was to familiarize the participants with the test protocol. a 3RM test in bench press.β level to 0. as well as to minimize learning effects in the two subsequent sessions.9 days.20. all participants performed two test sessions for investigation of between-day reliability of muscle synergies during bench press. and then three sets of eight repetitions at 60% of the 3RM load for investigation of reliability. Proper execution requires the coordinated activation of all major muscle groups in the legs. we applied the common exercise of bench press. Experimental procedure As a means to study the reliability of extracting muscle synergies during a strength training movement. In the test sessions. 2014]. All participants gave their written informed consent after having been explained the experimental methods and risks. 2010.2.9. The study consisted of three sessions. The time interval between the first and the second test session was on average 8. The study was approved by the local ethics committee of North Denmark Region (N-20120036). p1 to 0.

anterior deltoideus (AD). rectus femoris (RF). triceps brachii. latissimus dorsi (LD). surface EMG electrodes (Ambu Neuroline 720 01-K/12. lateral head (TBL). 2015b].dynamic normalization procedure. For PM and LD. the task-specific submaximal dynamic normalization procedure consisted of recording the maximal surface EMG envelope on the below mentioned muscles during the execution of a submaximal bench press at 75% of 3RM. medial head (TBM). the electrodes were mounted four fingerbreadths below the clavicle. participants performed a progressive warm up regimen by lifting increasingly heavier loads in bench press. which we have previously used in a similar experimental setup [Kristiansen et al. until 3RM was found. respectively. Ambu A/S. parallel to the lateral border of scapula [Lehman et al. soleus (SOL). Bench press was performed using an ER-Equipment power rack (ER Equipment. erector spinae (ES). biceps brachii (BB). Denmark). medial to the anterior axillary border and 3 fingerbreadths distal to and along the posterior axillary fold. triceps brachii.3. 2006]. A reference electrode was mounted on the ankle. Briefly. inter electrode distance 20 mm. 2000]. 2. Ballerup. Then. On 5 . which are not listed by SENIAM. biceps femoris (BF). and vastus medialis (VM). Albertslund. gastrocnemius lateral head (GML). Ag/AgCl. For the 3RM test. vastus lateralis (VL). Test sessions First. Denmark) were placed on the skin over the following muscles on the right side of the body: pectoralis major (PM). the load was increased by 2. the involved skin areas were shaved and cleaned with alcohol. All electrodes were mounted by the same researcher in both test sessions.5-10 kg per set of 3 repetitions. Most of the electrodes were mounted according to the SENIAM recommendations [Hermens et al. The obtained value in this procedure was then used as a normalization factor. at the lateral malleolus. After the placement of the electrodes. The electrodes were mounted along the muscle fiber direction in a bipolar configuration.

Finally.4. a notch filter (4th order Butterworth band stop with rejection width of 1 Hz centered at the first three harmonics of the power line frequency of 50 Hz) was used to remove line interference. To avoid any initial transition. the first bench press cycle of each set was removed from the data resulting in the concatenation of 21 cycles per participant. After successful completion of the 3RM test. Participants were instructed to perform the eccentric phase in approx. 1 s and the concentric phase as fast as possible for the 3RM test and the normalization set. LISiN . 1 s eccentric phase and 1 s concentric phase.OT Bioelectronica. Italy) where they were amplified using an individual-specific gain factor (100-500) and band-pass filtered [10-750 Hz] before being sampled at 2048 Hz. A bench press cycle was defined as the period between two successive top positions. Hadsund. This resulted in a total of 24 repetitions with a cyclic pattern consisting of approx. Data recording and processing The surface EMG signals were recorded using a 128-channel surface EMG amplifier (EMG- USB. Four min rest was applied between all sets. NTT Nordic Transducer. The EMG data obtained during these repetitions was used for normalization purpose. Denmark) was connected to the middle of the barbell for measurement of the vertical position. the load was further decreased to 60% of the 3RM load. The linear envelopes of the EMG measurements 6 . and the last 3 sets of 8 repetitions were completed. the exact same procedure was applied. The data recorded during these repetitions were used to study the between–day reliability of muscle coordination. the load was decreased to 75% of the 3RM load and 3 repetitions were performed. Furthermore.average 4 sets were required for the determination of the 3RM. A potentiometer (model KS60. Table 2 near here 2. Turin. In the second test session.

and represents the synergy activation coefficient. 2007]. In line with previous work [Kristiansen et al. 2011. Nonnegative matrix factorization decomposes the initial matrix E into two multiplication matrices (W and C). Functional sorting is necessary as the order of the muscle synergies 7 .across each of the bench press cycles were obtained by low pass filtering (zero-lag Butterworth. 2014] using the Lee and Seung algorithm [Lee and Seung. Kristiansen et al. 2007. The maximum of these averaged values was then used as a normalization factor for the matching EMG measurement [Kristiansen et al. a nonnegative matrix factorization was applied to the concatenation of the 21 bench press cycles [Oliveira et al. 2011a]. 2015b. During the normalization set performed at 75% of 3RM. 2015b]. the first and last half second of the EMG measurements were excluded. the muscle synergies extracted from each participant were functionally sorted [Torres- Oviedo and Ting. The number of synergies chosen for further analysis is dependent on the variance accounted for (VAF). The linear envelopes of the EMG measurements for normalization purposes were then computed and averaged across 100 ms non-overlapping intervals. and consists of the muscle synergy vectors. the smallest number of synergies that provided a total VAF ≥90% for all participants was accepted. C is an s-by-n matrix. 2015b. Torres-Oviedo and Ting. Turpin et al. where p is the number of muscles (13) and n is the number of time points (2100). Each of the EMG envelopes was then interpolated into 100 time points. 2nd order. Synergy activation coefficients represent the recruitment of the muscle synergy over time. After finding the smallest number of muscle synergies that described ≥90% of the VAF. n is calculated as 21 bench press cycles times 100 time points per bench press cycle. For the extraction of muscle synergies. Muscle synergy vectors represent the relative weighting of each muscle within each synergy. 4 Hz) of the rectified EMG. 1999] in line with previous studies [Hug et al. Torres-Oviedo and Ting. E is a p-by-n matrix of the normalized EMG envelopes. 2007]. W is a p-by-s matrix (s is number of synergies).

To evaluate the between-day reliability of the extracted muscle synergy vectors and synergy activation coefficients. [2] The new recomputed synergy activation coefficients were then compared with their original versions in each day. A similar procedure was then performed to re-compute the muscle synergy vectors extracted in the second test session using the fixed synergy activation coefficients from the first test session. as they were recomputed. continues until the reconstruction error converges. T is the matrix transpose. n is the iteration counter. [1] when C is fixed. and were initially randomized in equation [1] and [2]. 2012] and Muceli et al [Muceli et al. was carried out for the synergy activation coefficients. using the fixed muscle synergy vector from the opposite day. respectively. The magnitude of the correlation coefficients across the procedures was considered for evaluation 8 . This iteration process.may be swapped among participants following the application of the non-negative matrix factorization. 2010]. the muscle synergy vectors extracted in the first test session were recomputed. In this iterative procedure [1]. not to be confused with the one previously described for sorting of muscle synergies. using the fixed synergy activation coefficients from the second test session. we performed a cross-validation analysis similar to that performed by Frère and Hug [Frère and Hug. The new recomputed muscle synergy vectors were then compared to their original versions in each day using correlation analysis. A similar procedure [2] as described above. For this purpose the cross-correlation function was used. and i and j are indices corresponding to the row and column elements of the matrices. W is being recomputed.

of the between-day reliability of muscle synergy vectors and synergy activation coefficients. and the maximum of the cross-correlation function (rmax) for synergy activation coefficients of each subject. The same procedure was carried out for VAF of each of the 13 individual muscles (termed VAFMuscle). We then tested the r-values for systematic bias across test sessions. This yielded a total of four r-values per subject. r-values were calculated between the recomputed component of the first test session and the original component of the first test session and between the recomputed component of the second test session and the original component of the second test session for each subject. The relative reliability was evaluated by calculating a 2-way fixed ICC3. Figure 1 near here 2. The total VAF of each test session was then recomputed using the procedure described above. the use of a conventional intraclass correlation coefficient (ICC) or standard error of the measurement (SEM) to evaluate reliability was not directly applicable. Statistical analysis As muscle synergy vectors and synergy activation coefficients are not single scalar quantities. In order to be able to compare components across test sessions.5. within-subjects repeated measures analysis of variance (RM-ANOVA). by fixing either the muscle synergy vector (termed VAFFix_W) or the synergy activation coefficient (termed VAFFix_C) of the opposite day. As a measure of the 9 . To evaluate the between-day reliability of total VAF. we therefore calculated Pearson’s correlation coefficient (r) for muscle synergy vectors. we first determined total VAF for the first and second test session. the relative and absolute reliability across test sessions of the r-values obtained when comparing the original and the recomputed components were then evaluated using ICC and SEM. To compare original components and recomputed components. using a single-factor. Further. A substantial drop in total VAF would indicate low reliability across test sessions. by calculating the effect of trials.1 and the absolute reliability was evaluated by calculating SEM.

20 is considered poor. Results Two muscle synergies caused the total VAF to be ˃90% for all participants (Figure 1). Armonk. unless otherwise indicated. for both muscle synergy vectors.00 is very strong [Martínez-Valencia et al.62) for muscle synergy vectors and very strong (0. 0. USA) was used for all statistical analyses. 2013].0 statistics software (IBM Corp.05. The muscle synergy vector and synergy activation coefficient for these subjects in the first and second test session are depicted in Figure 3.10-0. 1977].30 is considered weak.00 is almost perfect [Landis and Koch. The same statistics were applied to VAFFix_W.00-0. 0.60 is moderate. However. and 0. in both test sessions.40 is fair.41-0.61-0.84 and 0.31-0.81-1.21-0. ICC3. however.58 and 0. 0.70 is strong. 10 . VAFFix_C. and VAFMuscle. two subjects displayed negative correlation values.minimal difference needed to be considered real. Results are presented as mean±SD. one muscle synergy was sufficient for the VAF to be ˃90%. NY. and VAFMuscle to be ˃75%. SPSS Version 22. The correlations between the first and second test session were strong (0.1-values were interpreted using the categories proposed previously in which an ICC3.80 is substantial. and 0. 0.1 of 0.89) for synergy activation coefficients (Table 1).71-1. Muscle synergy 1 mainly involved the eccentric phase of the bench press cycle while muscle synergy 2 mainly involved the concentric phase. The synergy activation coefficients together with the muscle synergy vectors for the first and second test session are depicted in Figure 2. r-values were interpreted using categories previously suggested in which an r-value of 0. Figure 2 near here 3. we calculated a 95% confidence interval (CI).50 is considered moderate. 0. Statistical significance was accepted at p ≤ 0. For seven subjects.51-0.

ICC3. and SEM calculated on the r-values were 0. respectively. 11 . this may indicate that the relative weighting of each of the muscles within each synergy is subject to small variations between the first and second test session. For synergy activation coefficients.1-values ranged from poor (0.9 and 92.2 for the first and second test session. and SEM calculated on the rmax–values were 0.4±1. The SEM was in all cases low (0-0. The between-day reliability of muscle synergy vectors and synergy activation coefficients were strong and very strong. muscle synergy vectors and synergy activation coefficients showed a very strong correlation in all instances (0. respectively. As muscle synergy vectors were slightly less reliable. For a few muscles (AD.9±10. and SOLFix_C). For muscle synergy vectors.7±2. we evaluated between-day reliability of muscle synergies. VAFFix_C was 92.03%).59) and almost perfect (0.74-0.06 in both cases (Table 2).70) and almost perfect (0.90). the VAFMuscle exhibited systematic bias (p≤0. When fixing the synergy activation coefficient.1-values were almost perfect (0. ICC3.7 for the first and second test session. we found that the extracted muscle synergies which described bench press. respectively.95).1-values of VAFFix_C and VAFFix_W were moderate (0. When fixing the muscle synergy vector.1-values were substantial (0.05) between the first and second test session. Discussion In the present study.07%.88) (Table 2). extracted by applying a nonnegative matrix factorization algorithm to EMG data collected during bench press. were stable and reliable across days.06) to almost perfect (0. Comparing the original components to the recomputed components for the first and second test session. VAFFix_W was 84.0 and 86. The ICC3. TBMFix_C.10 and 0.85 and 0.86). respectively.16 (Table 2). The ICC3. Figure 3 near here 4. In line with our hypothesis.87) while the SEM was in general low and ranged from 0-3.8±7.

This may have caused some inter-trial variation in the motor patterns. In the present experimental setup. thus being controlled by the afferent systems and the motor cortical areas [Bizzi and Cheung. Further. as the cross correlation of synergy activation coefficients are calculated from 100 samples. 2006]. This is further advocating the higher reliability of the synergy activation coefficients over the muscle synergy vectors. 2010]. From a neurophysiological point of view. In addition. in line with a previous study [Torres-Oviedo and Ting. while only 13 samples are used for muscle synergy vectors. 2013]. 2004]. a metronome guided the tempo of the execution of the task. a larger estimation variance is expected in muscle synergy vectors compared to synergy activation coefficients [Mak. some believe that muscle activity is the result of a few temporal activation components distributed to various muscles [Ivanenko et al. 2002]. Another possible explanation. 2015]. which may explain the very strong correlation between synergy activation coefficients. muscle synergies are thought to be of neural origin located at the spinal level. whereby a movement can be performed using different muscle recruitment options [Latash et al. muscle redundancy could also explain why negative correlation values were obtained in two out of 21 cases for muscle synergy vector 1 (Table 1). The strong to very strong correlations of muscle synergy vectors and synergy 12 . Within this framework. might be related purely to computation. the reliability of the muscle synergy vectors were still strong and indicated good between-day reliability and the synergy activation coefficients displayed very strong correlations between the first and second test session. Due to this difference. it is possible that small variations in the placement of EMG electrodes among sessions could in part explain why muscle synergy vectors were slightly less reliable. This can also be explained by the experimental task since biomechanically constrained task have been recently reported to reduce the accuracy of estimated synergies [Steele et al. Despite this.This could be explained by the redundancy or abundancy of the musculoskeletal system.

meaning that if different muscle coordination is used in the first and second test session.1 values and the low SEM values further indicates that the within-subject reliability of the extracted muscle synergies across test sessions was high. mean values decreased to just below the 90% threshold (86. ICC3. the control of bench press is stable. For VAFFix_W.1 values were almost perfect for VAFFix_W. the correlation of the recomputed component would be weak.1 values 13 . ICC3. the very strong correlation of the r-values.activation coefficients suggest that the same basic motor output patterns were responsible for the muscle coordination in the first and second test session. as these data for the first time provide information on the robustness of the low dimensional structure of muscle coordination across days. This procedure was done to verify the within-subject reliability of the extracted muscle synergies. This has important implications for the use of nonnegative matrix factorization as an assessment tool.7% and 92. However. In addition to evaluating the reliability of muscle synergy vectors and synergy activation coefficients using Pearsons r.8% and 84. the high ICC3. When comparing first and second test session with respect to values of VAFFix_W and VAFFix_C.4%). the mean values of VAF Fix_C for both test sessions were still above the 90% threshold (92. When we recomputed VAF by fixing either the muscle synergy vectors or the synergy activation coefficients of the opposite day. It therefore seems that at least for trained individuals.03%. we also performed a cross validation analysis of the extracted muscle synergies in which we recomputed each of the muscle synergy vectors and synergy activation coefficients. This indicates that extracting muscle synergies from EMG data using nonnegative matrix factorization is a reliable method for studying muscle coordination during bench press. combined with a very low SEM-value of 0. This decrease may be the result of the muscle synergy vectors being slightly less reliable than synergy activation coefficients. indicating that only a minor part of the variability was not accounted for.9%).

we found a very small drop in VAFFix_W (9. SOL.7%) [Weir.9% and 2.2% and 3.0% and 11. with the exception of ADFix_C. As we were aware that some of the subjects displayed VAF-values above 90%.1 only ranged from poor to moderate. using just one synergy component. and RFFix_C (5 out of 39 versions of VAFMuscle). 2007]. And even when fixing either the muscle synergy vector or the synergy activation coefficient of the opposite test session. a moderate to almost perfect ICC3. PMFix_C.were merely moderate for VAFFix_C. a very large portion of the variability in the dataset is still accounted for following recomputation. This may in fact be the case for VAFFix_C based on the almost identical mean values (92. This further confirmed the high between-day reliability of muscle synergy vectors and synergy activation coefficients. LDFix_C.4% and 92.00%. 2005]. in addition to the fact that versions of VAFMuscle in most cases were above the 75% threshold. This indicates that by using a fixed synergy component from another test session. When calculating VAFMuscle. ADFix_C.7%) and the very low SD values (1. This was the case for almost all versions of VAFMuscle. the VAF Muscle would in most cases still satisfy the 75% threshold for adequate reconstruction. PM.3%) and VAFFix_C (3. with very low SD and SEM values. 14 . In summary. 75% of the variability must be accounted for to adequately reconstruct muscle data vectors [Torres-Oviedo and Ting. This implies that the reconstruction of single muscle data vectors was in most cases adequate. GML. TBMFix_C. and VM all display identical mean VAFMuscle values in the first and second test session. BBFix_C. This point is further underlined when looking at VAF for individual muscles. VL. even the ones that were recalculated. The reason for the latter could be that the ICC value may be small in case of low between-subject variability.9%) compared to mean total VAF. Thus. we applied the commonly used criteria for VAF Muscle in which a VAFMuscle above 75% is required for adequate reconstruction [Torres-Oviedo and Ting.1 and very low SEM-values for VAFFix_W and VAFFix_C. despite the negligible SEM value of ≤ 0. TBLFix_C. Yet. the ICC3.

Only 8 participants out of 21 (=38%) met this criterion using one synergy component. we tried to establish a link between these particular subjects and variables such as absolute strength.2007]. For the rest of the subjects. 2010]. One possible explanation is that the subjects are consistently coping against the weight in both the eccentric as well as the concentric phase. however. the muscle synergy vector and synergy activation coefficient may reflect a merge of the two originally extracted muscle synergies as shown in Figure 3. is the result of these subjects not being capable of differentially activating the two muscle synergies. For the seven subjects requiring only one muscle synergy. this made us consider that two synergy components would mainly be required for an adequate description of the task. For 7 of these 8 subjects. It has previously been shown. body mass and training experience. it seems that muscle activation is predominantly applied at a later stage of the eccentric phase. and we are not sure of the reason causing discrepancy in number of muscle 15 . thus leaving the control and stabilization of the weight to the very last moment of the eccentric phase. This can be seen by the well-defined peak of activation occurring just before the 50th time point in synergy activation coefficient 1 in Figure 2. In combination. This peak most likely represents the shift between the eccentric and the concentric phase. relative strength. This could point towards a more confident strategy in which the muscle activation is minimized. that muscle synergies extracted during walking in patients with post-stroke hemiparesis were merged together. However. resulting in impaired walking performance [Clark et al. in which the difference between maximum and minimum activation is small. age. In addition to this. This consistent application of muscle activation is illustrated by the synergy activation coefficient in Figure 3. this was not possible. In an attempt to explain why 7 out of 21 subjects exhibit only one muscle synergy. the criterion was met at both the first and second test session. It is possible that the merge of two muscle synergy components into one. the extraction of two synergy components fits nicely with the functional role of the muscles and the phases of the task.

we opted for a VAF-criterion that could accommodate all the subjects and thus we did not separate the subjects in two groups with one and two muscle synergies for the main analysis. rather than bilateral. there is an ongoing debate as to whether muscle synergies are functional entities produced by the nervous system or simply a result of the biomechanical constraints of the motor task [Steele et al.1 values ranged from substantial to almost perfect combined with low SEM values. 2015a]. A perspective of the present study is that it appears sound to use nonnegative matrix factorization algorithm for quantification of changes in muscle coordination over time. to support the study conclusions. One explanation is that altered supraspinal drive and sensory- motor control may have affected the modular control in some of the subjects. 16 .g. Further. the between-day reliability of muscle synergies was evaluated for the first time in bench press.Limitations of this study include that ipsilateral. training intervention studies [Kristiansen et al. In conclusion.synergies among subjects. Further. Moreover. The present findings suggest that the same general structure of the muscle coordination was present across days. 2015]. the reliability of the application of nonnegative matrix factorization to derive synergy components during a functional task remains important. 2010]. and further analysis indicated that ICC3. biomechanical studies including 3D kinematics may help to delineate the relationship between the number of muscle synergies and the movement kinematics. EMG data was obtained. This demonstrates the consistency of the strategy used by the nervous system to control movements like bench press. Bilateral recording of EMG data would have yielded further data. as previously discussed [Clark et al. Regardless. The correlations of muscle synergy vectors and synergy activation coefficients between two test sessions were strong to very strong. The design of the present study does not allow for any speculations on this matter. e.

00099.21(1):1-12. References Bernstein N. Development of recommendations for SEMG sensors and sensor placement procedures. Proceedings of the National Academy of Sciences of the United States of America. Clark DJ. 17 . institutional or other conflicts of interests. Hermens HJ. Rau G. The neural origin of muscle synergies. Cheung VCK. 1967. Journal of neurophysiology. Dorel S. Cappellini G. Between-subject variability of muscle synergies during a complex motor skill. 2006.95(6):3426-3437. 2010.00051. 2000. New York: Pergamon Press. Can muscle coordination be precisely studied by surface electromyography? Journal of Electromyography and Kinesiology. consultant. Neptune RR. Drouet J. Changes of pedaling technique and muscle coordination during an exhaustive exercise.2012. 2009. Poppele RE.Acknowledgements The study was partly supported by grants from the Ministry of Culture Committee on Sports Research in Denmark and the Danish Rheumatism Association. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. Journal of Electromyography and Kinesiology. Hug F.10(5):361-374. Frontiers in Computational Neuroscience. Bizzi E.103:844-857. Hug F.3389/fncom.2013. Bizzi E. Hug F.7(Article 51):DOI: 10. 2010. 2012. Lacquaniti F. Conflict of interest The authors declare no competing financial.6:99(Article 99):DOI: 10. Champoux Y. Motor patterns in human walking and running. Ting LH. Freriks B. Ivanenko YP. Disselhorst-Klug C. The Coordination and Regulation of Movements. ER Equipment is thanked for loan of the lifting equipment.41(6):1277-1286. Medicine and science in sports and exercise. Couturier A.3389/fncom. 2013. Frère J. Frontiers in Computational Neuroscience. Journal of neurophysiology.102(8):3076-3081. Zajac FE. D'Avella A. Shared and specific muscle synergies in natural motor behaviors. 2005. Kautz SA.

64(1):96-106. Ivanenko YP. Dynamic Medicine. The measurement of observer agreement for categorical data. Is interindividual variability of EMG patterns in trained cyclists related to different muscle synergies? Journal of applied physiology. MacMillan B. Roberts C.33(1):159-174. Journal of neurophysiology. Scholz JP. Latash ML. Neuroscientist. 1999. Brorson S.22:822-828. 2012. Muscle synergies during shifts of the center of pressure by standing persons. 2015b. Experimental Brain Research. Samani A. Biometrics. 2003.152(3):281- 292. Muscle activation patterns are bilaterally linked during split-belt treadmill walking in humans. MacIntyre I. Motor control programs and walking. Development of human locomotion. 2006. Zatsiorsky VM. Gajewski BJ. The Journal of physiology. Journal of Strength & Conditioning Research. Turpin NA. Kristiansen M. Shoukri M.111:1541-1552. Learning the parts of objects by non-negative matrix factorization. Exercise and sport sciences reviews. 2014. Hróbjartsson A. 2015a. Landis JR. Lehman GJ. 2010. Nature. Journal of neurophysiology. Scholz JP. Lacquaniti F.556(1):267-282. Zago M. Krishnamoorthy V. Guidelines for reporting reliability and agreement studies (GRRAS) were proposed. 7):DOI: 10.5:7(art. Dorel S. Lacquaniti F. Streiner DL. Poppele RE. Ivanenko YP. Chivers M.0000000000001282. Duysens J. Seung HS. Lee DD. Hug F.30(1):26-31. Guével A. Hansen EA. Current opinion in neurobiology. Hansen EA.401(6755):788-791. 1977. Shoulder muscle EMG activity during push up variations on and off a Swiss ball. 2004. Samani A. Turpin NA. Ivanenko YP. Scandinavian Journal of Medicine and Science in Sports. Poppele RE. Latash ML. 2011. Motor control strategies revealed in the structure of motor variability. Consistency of muscle synergies during pedaling across different mechanical constraints. Bruijn SM. Journal of Clinical Epidemiology. Effects of five weeks of bench press training on muscle synergies .A randomized controlled study.12(4):339-348. Lacquaniti F.106(1):91-103. Dorel S. 2006.1519/JSC. Inter-subject variability of muscle synergies during bench press in power lifters and untrained individuals. no.108(6):1727-1736.25(1):89-97.DOI Number: 10. Ivanenko YP. 18 . Madeleine P. Madeleine P. Audigé L. Five basic muscle activation patterns account for muscle activity during human locomotion. Kristiansen M. Lacquaniti F. MacLellan MJ. 2002.1186/1476-5918-5-7. Fluter M. 2011.Hug F. Koch GG. Kottner J. Couturier A. Donner A. Schöner G. Massaad F.

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and VM=vastus medialis. For explanation of black and gray bars and lines. N = 21. For synergy activation coefficients. the thick black line represents the group mean. %) depicted as a function of the number of the original extracted muscle synergies for the first and second test session. PM=pectoralis major. VL=vastus lateralis. The percentage of variance accounted for (VAF. Synergy activation coefficient and muscle synergy vector of the first (A) and second (B) test session for the seven subjects who achieved a VAF value above 90% using only one muscle synergy. SOL=soleus. Figure 3. see Figure 2 caption. ES=erector spinae. GML=gastrocnemius lateral head. RF=rectus femoris. while the thin gray lines represent individual synergy activation coefficients. The muscle synergy vector and synergy activation coefficient reflect a merge of the two muscle synergy components shown in Figure 2. TBL=triceps brachii lateral head. BF=biceps femoris. AD=anterior deltoideus. N = 7. Synergy activation coefficients and muscle synergy vectors of the first (A) and second test session (B). TBM=triceps brachii medial head. Muscle synergy 1 mainly involved the eccentric phase (1. while muscle synergy 2 mainly involved the concentric phase (2. half) of the bench press cycle. The thin gray bars represent individual muscle synergy vectors. Values are presented as mean±25th and 75th percentiles.Figure captions Figure 1. the black bars represent group mean (with SD bars). LD=latissimus dorsi. 20 . Figure 2. half) of the bench press cycle. and muscle acronyms. BB=biceps brachii. For muscle synergy vectors.

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22 .

58±0. ________________________________________________________________________________________________________________ Muscle synergy vector 1 Muscle synergy vector 2 _____________________ ______________________ First vs second test session (r) 0.62±0.99] 0.41 [-0. Comparison of muscle synergies across test sessions.32 – 0.62 – 0.89±0.13 [0.Table 1.97] 0.84±0.22 [0.56 – 0.42 [-0. Values are presented as means ± SD [min-max].99] ________________________________________________________________________________________________________________ Correlation coefficients (r) of muscle synergy vectors and cross-correlation coefficients (rmax) of synergy activation coefficients.95] ________________________________________________________________________________________________________________ Synergy activation coefficient 1 Synergy activation coefficient 2 _____________________________ _____________________________ First vs second test session (rmax) 0. 23 .59 – 0.

Comparison of original and recomputed components of muscle synergies consisting of muscle synergy vectors and synergy activation coefficients.75±0.22 [0.75±0.797 0.06 0.18 ±0.41 [-0.00] 0.90 0.38 .1.-values are presented as means ± SD [min-max].46 [-0.359 0.1.00] Second test session (rmax) 0.99] 0.88±0. CI = Confidence interval.36 [-0.41 ________________________________________________________________________________________________________________ Synergy activation coefficient 1 Synergy activation coefficient 2 ___________________________ ___________________________ Recomputed component vs original component First test session (rmax) 0.338 ICC3.00] 0.00] Second test session (r) 0.22 – 1.82±0.1 0.10 0.00] Effect of trials (p-value) 0.19 [0.46 [-0.75±0.85 SEM (r) 0. SEM = Standard error of measurement.06 CI95% ±0.46 [-0.1 = 2-way fixed intraclass correlation coefficient.16 ________________________________________________________________________________________________________________ r and rmax.28 .74±0. 24 .22 – 1.36 [-0.82±0.16 CI95% ±0.67 – 1.1.00] 0.1 0. _______________________________________________________________________________________________________ _________ Muscle synergy vector 1 Muscle synergy vector 2 ____________________ ____________________ Recomputed component vs original component First test session (r) 0.Table 2.70 SEM (rmax) 0.51 – 0.59 .86±0.25 ±0.00] Effect of trials (p-value) 0.163 ICC3.95 0.67 – 1. ICC3.

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Denmark. France. Afshin Samani Afshin Samani received his PhD in Biomedical Engineering and Science in 2010 from Aalborg University. in 1969. He is head of the research interest group within Physical Activity and Human Performance and co- director of the laboratory for Ergonomics and Work-related Disorders. His research areas include human rhythmic motor behaviour and control as well as strength training and sports performance. Department of Health Science and Technology. Denmark. He has published more 160 peer reviewed scientific journal publications and book chapters. His main area of research interests are the development and application of novel methods and technologies in Ergonomics and Sports. Denmark. His main areas of research are neural adaptations to resistance training. He is currently director of Motor Behaviour and Performance Laboratory as well as member of the Research Interest Group of Physical Activity and Human Performance. Pascal Madeleine Pascal Madeleine was born in was born in Toulouse. Department of Health Science and Technology at Aalborg University.Author biography Mathias Kristiansen Mathias Kristiansen earned a MS degree in sports science at Aalborg University in 2012 and received his PhD in Sports Science in 2015 from Aalborg University. He has been associate professor at SMI®. . His scientific production currently includes more than 40 articles published in peer- reviewed journals. Denmark. Denmark. Denmark. He is currently employed as an associate professor in sports science and ergonomics at the Department of Health Science and Technology at Aalborg University. He earned a MS degree in sports science at University of Copenhagen in 1997 and a PhD degree entitled “Is the freely chosen pedal rate optimal during cycling?” at University of Southern Denmark in 2003. He is currently employed as a Professor in Sports and Ergonomics at SMI®. Ernst Albin Hansen Ernst Albin Hansen was born in Roskilde. Denmark. He is co-director of the laboratory for Ergonomics and Work-related Disorders. His specific research field is focused on methods of quantification of work exposures and risk factors for the development of musculoskeletal disorders and interactions between muscle pain and motor control in computer users. on 6 November 1969. He is currently employed at the Department of Health Science and Technology at Aalborg University. Aalborg University since 2010 and defended a DSc degree in 2015 entitled ”On voluntary rhythmic leg movement behaviour and control during pedalling”. He received his DrSc degree and PhD from Aalborg University. He is board member of the Danish Biomechanical Society and the Danish University Extension.