Hindawi Applied Bionics and Biomechanics Volume 2021, Article ID 6651671, 7 pages https://doi.org/10.1155/2021/6651671 Research Article Lumbar Intervertebral Disc Degeneration Does Not Affect Muscle Synergy for Rowing Activities 1 2 3 4 5 Chie Sekine , Naoto Matsunaga, Yu Okubo, Mika Hangai, and Koji Kaneoka Department of Physical Therapy, Niigata University of Health and Welfare, 1398 Shimami-cho, Kita-ku, Niigata City, Niigata 950-3198, Japan General Education Core Curriculum Division, Seigakuin University, 1-1 Tosaki, Ageo City, Saitama 362-8585, Japan School of Physical Therapy, Faculty of Health and Medical Care, Saitama Medical University, 1397-1 Yamane, Hidaka City, Saitama 350-1241, Japan Medical Center, Japan Institute of Sports Sciences, 3-15-1 Nishigaoka, Kita-ku, Tokyo 115-0056, Japan Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa City, Saitama 359-1192, Japan Correspondence should be addressed to Chie Sekine; email@example.com Received 9 November 2020; Revised 17 January 2021; Accepted 3 February 2021; Published 15 February 2021 Academic Editor: Wen-Ming Chen Copyright © 2021 Chie Sekine et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Rowers with disc degeneration may have motor control dysfunction during rowing. This study is aimed at clarifying the trunk and lower extremity muscle synergy during rowing and at comparing the muscle synergy between elite rowers with and without lumbar intervertebral disc degeneration. Twelve elite collegiate rowers (with disc degeneration, n =6; without disc degeneration, n =6) were included in this study. Midline sagittal images obtained by lumbar T2-weighted magnetic resonance imaging were used to evaluate disc degeneration. Participants with one or more degenerated discs were classiﬁed into the disc degeneration group. A 2000 m race trial using a rowing ergometer was conducted. Surface electrodes were attached to the right rectus abdominis, external oblique, internal oblique, latissimus dorsi, multiﬁdus, erector spinae, rectus femoris, and biceps femoris. The activity of the muscles was measured during one stroke immediately after 20% and 80% of the rowing trial. Nonnegative matrix factorization was used to extract the muscle synergies from the electromyographic data. To compare the muscle synergies, a scalar product (SP) evaluating synergy coincidence was calculated, and the muscle synergies were considered identical at SP > 75%. Both groups had only one module in the 20% and 80% time points of the trial. At the 20% time point of the 2000 m rowing trial, the SP of the module was 99.8%. At the 80% time point, the SP of the module was 99.9%. The SP results indicate that, at 20% and 80% time points, both groups had the same module. The module showed a high contribution in all muscles. The activation coeﬃcients indicated that the module was always highly activated throughout the rowing stroke in both groups. The trunk and lower extremity muscles are mobilized through the rowing stroke and maintain coordination during rowing. There was no diﬀerence in the muscle synergy between the rowers with and without lumbar intervertebral disc degeneration. 1. Introduction two factors: muscle weighting and activation coeﬃcient. Muscle weighting represents the relative weighting of each The central nervous system controls movement through a muscle within each module, and the activation coeﬃcient combination of a few basic activation patterns known as represents the relative activation of the muscle weighting . motor modules or muscle synergies . A muscle synergy Recently, using NMF analysis, muscle synergy in compet- can be characterized as a low-dimensional organizational itive sports has been analyzed. As a result, it is reported that the number of muscle synergy changes every sports activity structure controlling multiple muscles. The evaluation of muscle coordination was reﬁned by nonnegative matrix and that muscle synergy diﬀers by the performance level factorization (NMF) analyses based on Bernstein’s concept and existence of injury. For example, in the research which . This analysis divides electromyographic (EMG) data into evaluated the muscle synergy during sidestepping, it was 2 Applied Bionics and Biomechanics One rowing cycle shown that groin pain causes motor control dysfunction of Catch Next catch the trunk and lower extremity muscle groups . Motor con- trol of the upper and lower extremities and the trunk is very important in rowing. Therefore, it may be connected with injury prevention and performance improvement by clarifying the muscle synergy in rowing. Muscle synergy during rowing has been analyzed in experienced rowers and untrained sub- jects. In research comparing the muscle synergy between expe- Figure 1: One rowing cycle. The catch position was deﬁned as the rienced rowers and untrained subjects during rowing at high time at which the x-coordinate of the handle marker showed the stroke rates, three synergies were identiﬁed in both groups, minimum value. The time between the catch position and the conﬁrming the similarity in muscle synergy between groups next stroke’s catch position was referred to as the stroke (one [4, 5]. In the study of collegiate rowers and recreational rowing cycle). athletes with no rowing experience, three synergies were identiﬁed in both groups during rowing . duration of rowing career: 6:5±2:0 years). All participants In terms of injuries to rowers, the lumbar spine is the belonged to the same university team. Their training most common site of injury [7–9]. Therefore, a number of involved mainly rowing for approximately 11 sessions a week studies on the factors contributing to low back pain (LBP) for approximately 2 hours per session, which included weight have been performed, and LBP history  and ergometer training approximately twice a week. The experiment was training [9, 11] have been reported as signiﬁcant risk carried out according to the tenets of the Declaration of factors for LBP in rowers . In addition, signs of disc Helsinki. This study was approved by the institutional ethics degeneration are associated with LBP . A longitudinal review committee (approval number: 2012-223). All partici- study that investigated the relationship between LBP and pants provided informed consent to participate in this study. intervertebral disc degeneration in collegiate rowers also reported that lumbar intervertebral disc degeneration is 2.2. Experimental Protocol. A 2000 m rowing trial was related to LBP . Therefore, in this study, we focused conducted using a Concept 2 Model D rowing ergometer on lumbar intervertebral disc degeneration associated with (Concept Inc., Morrisville, VT, USA). The warm-up was per- LBP in rowers. A previous study involving combat sports formed on land and included ergometer rowing, with similar athletes reported that the relative size of the cross- intensity and duration among the participants. After warm- sectional areas of the trunk muscles to their body weight ing up, electrodes and a wireless EMG system were attached in the lumbar intervertebral disc degeneration group was to the participants. As in previous studies that investigated signiﬁcantly smaller than that in the nonlumbar interverte- the kinematics and kinetics of rowing [16, 17], participants bral disc degeneration group . Accordingly, it was were asked to row at a race pace. thought that the trunk muscles are related to lumbar inter- vertebral disc degeneration. As described above, motor 2.3. Assessment of Disc Degeneration. Lumbar T2-weighted control of the upper and lower extremities and the trunk sagittal magnetic resonance (MR) images (repetition time: is very important in rowing. Therefore, we hypothesized 2800 ms; echo time: 90 ms) were obtained using a 1.5-T MR that the rowers developing intervertebral disc degeneration device (Signa HDxt XV; GE Healthcare, Tokyo, Japan) with might have diﬀerent muscle coordination of the trunk and a four-channel spine coil. The slice thickness was 4.0 mm, lower extremities while rowing, as compared to those who and the ﬁeld of view was 300 × 300 mm. The midsagittal did not develop any intervertebral disc degeneration. image was used for the evaluation. Using the Pﬁrrmann classi- Rowers with disc degeneration may have motor control ﬁcation , the L1–L2 to L5–S1 discs were classiﬁed into ﬁve dysfunction during rowing, but muscle synergy during grades according to the degree of degeneration. Participants rowing has not been compared in rowers with and without with one or more degenerated discs were classiﬁed into the lumbar intervertebral disc degeneration. disc degeneration group. Degeneration was assessed by two Therefore, this study is aimed at clarifying the trunk and experienced orthopedic surgeons. MR images were obtained lower extremity muscle synergy during rowing and at approximately 4 months before the rowing ergometer task comparing the muscle synergy between elite rowers with because disc degeneration was assessed retrospectively. and without lumbar intervertebral disc degeneration. 2.4. Data Measurements. Muscle activity was measured using a wireless EMG system (EMG-025; Harada Electronic Indus- 2. Materials and Methods try Ltd., Sapporo, Japan) at a sampling frequency of 2.1. Participants. The study participants were 12 elite colle- 983.217 Hz. Before the surface electrodes were attached, skin giate rowers with career durations of >3 years, including six abrasives and alcohol were applied to the skin to achieve an rowers with lumbar intervertebral disc degeneration (sex: electrical resistance of ≤2kΩ, and pairs of disposable male, n =4; female, n =2; age: 19:8±0:8 years; body mass Ag/AgCl surface electrodes (BlueSensor N-00-S; Ambu, Ballerup, Denmark) were attached parallel to the muscle index: 21:7± 1:3 kg/m ; and duration of rowing career: 5:1±2:2 years) and six rowers without lumbar interverte- ﬁbers, with a center-to-center distance of 2 cm. Surface bral disc degeneration (sex: male, n =4; female, n =2; age: EMG data were collected from the right rectus abdominis 21:2±0:8 years; body mass index: 23:3±1:5 kg/m ; and (3 cm lateral to the umbilicus) [19, 20], external oblique Applied Bionics and Biomechanics 3 Table 1: Results of the performance data. DD group non-DD group p value Rowing stroke ratings (20%) (strokes per minute) 29:4±2:429:1±2:3 0.81 29:6±1:529:8±2:0 Rowing stroke ratings (80%) (strokes per minute) 0.84 440:9±29:4 432:2±33:3 2000 m rowing time (seconds) 0.64 The DD group is the group with disc degeneration. The non-DD group is the group without disc degeneration. The performance data did not show any signiﬁcant diﬀerences between the two groups. DD: disc degeneration. (15 cm lateral to the umbilicus) , internal oblique (the where E is a p × n initial matrix (p is the number of muscles, abdominal muscle corresponding to two ﬁngerbreadths and n is the number of time points) that represents the EMG medial to the anterior superior iliac spine), multiﬁdus (2 cm matrix. The initial matrix E consisted of a cycle for each of lateral to the L5 spinous process) , erector spinae (3 cm the eight muscles; therefore, E was a matrix with 8 rows and lateral to the L3 spinous process) [19, 20], latissimus dorsi 101 columns. W is a p × s matrix (s is the number of synergies) (the belly muscle corresponding to three ﬁngerbreadths infe- that represents the muscle weighting. C is an s × n matrix that rior to the posterior axillary fold) , rectus femoris (the represents the activation coeﬃcient, and e is a p × n matrix point corresponding to 50% of the distance between the ante- that represents the residual error matrix. Equation (2) indi- rior superior iliac spine and the upper margin of the patella) cates that matrix e, calculated using Equation (1), reaches a , and biceps femoris (the point corresponding to 50% of minimum. For each participant, we iterated the analysis by the distance between the head of the ﬁbula and the ischial varying the number of synergies between 1 and 8. We selected tuberosity) . A reference electrode was placed over the least number of synergies that accounted for >90% of the the sternum. To divide the rowing cycle, a digital video global variance accounted for (VAF) [2, 25, 26] and >75% of camera (Exilim EX-FH25; Casio Computer Co., Ltd., the local VAF . Based on these studies, global and local Tokyo, Japan) synchronized with the EMG system was VAFs were calculated as follows: used to make a recording at 29.97 frames per second. p 2 Reﬂective markers with a diameter of 19 mm (QPM190; ∑ ∑ e i=1 j=1 i,j Global VAF = 1 − ×100 % , ð3Þ ðÞ Qualisys, Gothenburg, Sweden) were attached to the left p 2 ∑ ∑ E i=1 j=1 i,j side of the handle and the seat. 2.5. Data Analysis. Thetimepoint at whichthe x-coordinate of ∑ e j=1 m,j the sheet marker increased was referred to as the trial starting Local VAF m =1 − ×100 % , ð4Þ ½ ðÞ ∑ E point. The x-coordinate determined where the point was in a j=1 m,j left-right direction. The catch position was deﬁned as the time where i ranges from 1 to p and j ranges from 1 to n.Thus,in at which the x-coordinate of the handle marker showed the this study, i ranged from 1 to 8 and j ranged from 1 to 101. minimum value. The time between the catch position and the In Equation (4), m represents the muscle “m.” next stroke’s catch position was referred to as the stroke (one rowing cycle, Figure 1). The marker coordinates were deﬁned 2.6. Statistical Analysis. A scalar product (SP), calculated using DIPP-Motion Pro (Ditect Co., Ltd., Tokyo, Japan). according to the formula described by Cheung et al. , A custom MATLAB (MATLAB R2016; MathWorks, compared the synergies between the groups with and without Inc., Natick, MA, USA) code was used on the linear envelope disc degeneration. We deﬁned the module as the same if the and NMF. EMG data (raw data) corresponding to one row- SP was >75%. ing cycle were extracted. The EMG data were normalized to ! ! the maximum value of the EMG amplitudes over all condi- W ·W degeneration normal tions within the same participant for each muscle. Thus, the SP = × 100 % , ð5Þ ðÞ ! ! EMG scales ranged from 0 to 1. The rectiﬁed EMG signals W W degeneration normal were transformed into the linear envelope. One stroke at the 20% time point and another at the 80% time point of where each W is the averaged vector among the participants the 2000 m rowing trial were analyzed. To normalize time, ! ! the rowing cycle was interpolated to 101 time points. NMF in each group and W and W are the W of the degeneration normal was then performed to extract muscle synergies as described groups with and without degeneration, respectively. SP were by Lee and Seung , using the following formulas: performed using a custom MATLAB (MATLAB R2016; MathWorks, Inc., Natick, MA, USA). Other statistics were ð1Þ performed using SPSS version 27.0 (IBM Corp., Armonk, E = WC + e, NY, USA), and statistical signiﬁcance was set at p =0:05. Unpaired t-tests were conducted for the two groups (with minjj jj E − WC , disc degeneration vs. without disc degeneration) for rowing FRO W>0 ð2Þ stroke ratings at the 20% and 80% time points and 2000 m C>0 rowing time. The Kolmogorov-Smirnov test was conducted 4 Applied Bionics and Biomechanics DD Rectus abdominis DD Multifidus non-DD Rectus abdominis non-DD Multifidus 1 1 1 1 0.5 0.5 0.5 0.5 0 0 0 0 0 100010001000100 Time (%) Time (%) Time (%) Time (%) DD External oblique DD Erector spinae non-DD External oblique non-DD Erector spinae 1 1 1 1 0.5 0.5 0.5 0.5 0 0 0 0 0 100 0 100 0 100 0 100 Time (%) Time (%) Time (%) Time (%) DD Internal oblique DD Rectus femoris non-DD Internal oblique non-DD Rectus femoris 1 1 1 1 0.5 0.5 0.5 0.5 0 0 0 0 0 100 0 100 0 100 0 100 Time (%) Time (%) Time (%) Time (%) DD Latissimus dorsi DD Biceps femoris non-DD Latissimus dorsi non-DD Biceps femoris 1 1 1 1 0.5 0.5 0.5 0.5 0 0 0 0 0 100 0 100 0 100 0 100 Time (%) Time (%) Time (%) Time (%) Figure 2: EMG data of the mean of the two groups during a rowing stroke. The DD group is the group with disc degeneration. The non-DD group is the group without disc degeneration. The EMG scales ranged from 0 to 1. Solid line: 20% time point of the 2000 m rowing trial; dashed line: 80% time point of the 2000 m rowing trial. DD: disc degeneration; EMG: electromyographic. to conﬁrm the normality of the data. As a result of the normality test, parametric testing was selected. Table 2: Results of the nonnegative matrix factorization analysis (number of modules = 1). 3. Results 20% time point 80% time point 98:1±2:698:6±1:7 Global VAF (%) Table 1 shows the results of the performance data. The row- ing stroke ratings at the 20% time point were 29:4±2:4 83:2±11:279:0±20:5 RA strokes per minute and 29:1±2:3 strokes per minute for 83:6±10:980:3±20:2 EO the disc degeneration group and nondisc degeneration 82:3±12:278:1±20:8 group, respectively (p =0:81). The rowing stroke ratings at IO the 80% time point were 29:6±1:5 strokes per minute and 84:9±10:380:4±20:1 MF Local VAF (%) 29:8±2:0 strokes per minute for the disc degeneration group 84:4±10:679:5±21:0 LD and nondisc degeneration group, respectively (p =0:84). 84:2±10:781:1±20:4 ES The 2000 m rowing times were 440:9±29:4 seconds and 432:2± 33:3 seconds for the disc degeneration group and 83:2±11:879:2±21:3 RF nondisc degeneration group, respectively (p =0:64). The 83:9±10:580:2±20:4 BF rowing stroke ratings and 2000 m rowing time did not VAF: variance accounted for; RA: rectus abdominis; EO: external oblique; show any signiﬁcant diﬀerences between the two groups. IO: internal oblique; MF: multiﬁdus; LD: latissimus dorsi; ES: erector Figure 2 shows the EMG data of the mean of the two spinae; RF: rectus femoris; BF: biceps femoris. VAF corresponding to the groups during a rowing stroke. Table 2 and Figure 3 show number of modules. The number of modules is decided when the global the results of the NMF analysis. At both the 20% and 80% VAF exceeds 90% and the local VAF exceeds 75% for the ﬁrst time. time points of the 2000 m rowing trial, when there was one module, the global and local VAFs exceeded 90% and 75%, the SP of the module was 99.9%. The SP results indicate that, respectively, for the ﬁrst time (Table 2). Therefore, one mod- at 20% and 80% time points, both groups had the same mod- ule was extracted in each group (Figure 3). All participants ule. In both the 20% and 80% time points, the data from the had one module. At the 20% time point of the 2000 m rowing module mainly reﬂected that all muscles have high degrees of trial, the SP of the module was 99.8%. At the 80% time point, contribution. The activation coeﬃcients indicated that the Applied Bionics and Biomechanics 5 SP = 99.8% 1 0.5 0.5 0 0 RA EO IO MF LD ES RF BF 0 25 50 75 100 Time (%) Disc degeneration Normal Disc degeneration Normal SP = 99.9% 1 0.5 0.5 0 0 RA EO IO MF LD ES RF BF 0 25 50 75 100 Time (%) Disc degeneration Normal Disc degeneration Normal Figure 3: Extracted module during the 2000 m rowing trial. SP indicates the similarity between the groups with and without disc degeneration. RA: rectus abdominis; EO: external oblique; IO: internal oblique; MF: multiﬁdus; LD: latissimus dorsi; ES: erector spinae; RF: rectus femoris; BF: biceps femoris; SP: scalar product. module in both groups was always highly activated through- hand, it has been reported that antagonistic muscle prefati- out the rowing stroke, even during the recovery. There was gue led to signiﬁcantly lower gamma-band corticomuscular no signiﬁcant diﬀerence between the groups with and coherence during an isometric elbow extension, and muscle without disc degeneration. fatigue may reduce coherence . In this study, we did not examine the diﬀerence in muscle fatigue between the 20% and 80% time points, but corticomuscular coherence 4. Discussion may have been reduced at the 80% time point. The number This study investigated eight muscles functioning during a of modules in various athletic movements has been investi- 2000 m rowing trial and compared their activities between gated, and it has been reported that Japanese archery has the rowers with and without disc degeneration. The main two modules , and running has four modules . ﬁndings of this study were that only one module was active Muscle synergies have also been investigated in swimming; at the 20% and 80% time points of the 2000 m rowing trial, underwater undulatory swimming and breaststroke swim- and there was no signiﬁcant diﬀerence between the groups ming have three modules [32, 33]. Unlike other sports that with and without disc degeneration. The module showed a consist of multiple modules, the results of this study suggest high contribution in all muscles, and the activation coeﬃ- that rowing does not require multiple modules. On the other cients indicated that the module was highly activated hand, previous studies investigating muscle synergy during throughout the rowing stroke in the groups with and without rowing have detected three synergies [4–6]. In previous disc degeneration. Therefore, it is suggested that the trunk studies, 16 to 23 muscles, including upper extremity muscles, and lower extremity muscle groups are mobilized through were analyzed, but in this study, only 8 muscles were the rowing stroke and maintain coordination during the included in the analysis. The small number of test muscles rowing motion. compared to that in the previous study may have inﬂuenced Turpin et al.  analyzed the muscle synergy during the result of only one synergy in this study. rowing in nine male participants who had no prior experi- In our study, we focused on the lumbar intervertebral ence in rowing and reported that there was no change in disc degeneration in elite rowers and found no diﬀerence in the muscle coordination between the groups with and the number of synergies during the fatiguing rowing test. In their study, subjects performed the fatiguing rowing test for without disc degeneration. It is possible that there was no sig- up to 6 minutes, and the amount of power required increased niﬁcant diﬀerence in muscle synergy between the two groups every 2 minutes. In our study, there was no diﬀerence in the because the presence of LBP in both groups was not consid- number of synergies during the 2000 m rowing trial, and the ered in this study. Since disc degeneration becomes a factor of LBP, rowers with disc degeneration may experience LBP result was similar to that of the previous study. On the other Module (80% time point) Module (20% time point) 6 Applied Bionics and Biomechanics untrained subjects,” The Journal of Sports Medicine and Phys- during rowing, which may aﬀect their coordination. How- ical Fitness, vol. 56, no. 9, pp. 980–989, 2016. ever, it is not clear whether the subjects with disc degenera- tion had LBP at the time of the rowing trial, and thus, there  M. D. Devereaux and S. M. Lachmann, “Athletes attending a sports injury clinic, a review,” British Journal of Sports Medi- may have been no diﬀerence in muscle synergy between the cine, vol. 17, no. 4, pp. 137–142, 1983. two groups. In addition, in our study, the disc degeneration grade was a grade 3 or 4 with no participants having the most  T. Smoljanovic, I. Bojanic, J. A. Hannaﬁn, D. Hren, D. Delimar, and M. Pecina, “Traumatic and overuse injuries advanced disc degeneration (grade 5). The subjects had one among international elite junior rowers,” The American Jour- or two degenerated discs. If the subjects had many degener- nal of Sports Medicine, vol. 37, no. 6, pp. 1193–1199, 2009. ated discs or the degree of degeneration was more severe,  F. Wilson, C. Gissane, J. Gormley, and C. Simms, “A12-month there might have been diﬀerences in muscle synergy between prospective cohort study of injury in international rowers,” Brit- the two groups. ish Journal of Sports Medicine,vol. 44,no.3,pp.207–214, 2010. The limitations of this study were that the upper extrem-  J. W. O’Kane, C. C. Teitz, and B. K. Lind, “Eﬀect of preexisting ity muscles were not measured and that the number of ana- back pain on the incidence and severity of back pain in inter- lyzed muscles may be insuﬃcient. Therefore, the upper collegiate rowers,” The American Journal of Sports Medicine, extremity muscles should be included in future investiga- vol. 31, no. 1, pp. 80–82, 2003. tions. In addition, the existence of LBP was not considered  C. C. Teitz, J. O'Kane, B. K. Lind, and J. A. Hannaﬁn, “Back in this study. Therefore, further investigations considering pain in intercollegiate rowers,” The American Journal of Sports the existence of LBP are necessary for the future. Medicine, vol. 30, no. 5, pp. 674–679, 2002.  F. Wilson, C. Gissane, and A. McGregor, “Ergometer training 5. Conclusions volume and previous injury predict back pain in rowing; strat- egies for injury prevention and rehabilitation,” British Journal In conclusion, all the muscles have high contributions in the of Sports Medicine, vol. 48, no. 21, pp. 1534–1537, 2014. single model during rowing. The activation coeﬃcients indi-  K. Luoma, H. Riihimäki, R. Luukkonen, R. Raininko, cate that the module is highly activated throughout the row- E. Viikari-Juntura, and A. Lamminen, “Low back pain in rela- ing stroke, and there is no diﬀerence in the muscle synergy tion to lumbar disc degeneration,” The Spine Journal, vol. 25, between rowers with and without lumbar intervertebral disc no. 4, pp. 487–492, 2000. degeneration.  C. Sekine, K. Hirayama, O. Yanagisawa et al., “Lumbar inter- vertebral disc degeneration in collegiate rowers,” The Journal of Physical Fitness and Sports Medicine, vol. 3, no. 5, Data Availability pp. 525–530, 2014.  K. Iwai, K. Koyama, T. Okada et al., “Asymmetrical and The datasets analyzed during the current study are available smaller size of trunk muscles in combat sports athletes with from the corresponding author on reasonable request. lumbar intervertebral disc degeneration,” Springer Plus, vol. 5, article 1474, 2016. Conflicts of Interest  J. S. Caldwell, P. J. McNair, and M. Williams, “The eﬀects of repetitive motion on lumbar ﬂexion and erector spinae muscle The authors declare that there is no conﬂict of interests. activity in rowers,” Clinical biomechanics, vol. 18, no. 8, pp. 704–711, 2003.  C. L. Pollock, I. C. Jones, T. R. Jenkyn, T. D. Ivanova, and S. J. References Garland, “Changes in kinematics and trunk electromyography during a 2000 m race simulation in elite female rowers,”  N. A. Bernstein, The Co-ordination and Regulation of Move- Scandinavian Journal of Medicine & Science in Sports, ments, Pergamon Press, London, UK, 1967. vol. 22, no. 4, pp. 478–487, 2012.  F. Hug, N. A. Turpin, A. Guével, and S. Dorel, “Is interindivid-  C. W. A. Pﬁrrmann, A. Metzdorf, M. Zanetti, J. Hodler, and ual variability of EMG patterns in trained cyclists related to diﬀerent muscle synergies?,” Journal of Applied Physiology, N. Boos, “Magnetic resonance classiﬁcation of lumbar inter- vertebral disc degeneration,” Spine, vol. 26, no. 17, pp. 1873– vol. 108, no. 6, pp. 1727–1736, 2010. 1878, 2001.  N. Matsunaga, K. Aoki, and K. Kaneoka, “Comparison of modular control during sidestepping with versus without  G. M. Souza, L. L. Baker, and C. M. Powers, “Electromyo- groin pain,” International Journal of Sport and Health Science, graphic activity of selected trunk muscles during dynamic vol. 17, pp. 114–118, 2019. spine stabilization exercises,” Archives of Physical Medicine and Rehabilitation, vol. 82, no. 11, pp. 1551–1557, 2001.  N. A. Turpin, A. Guével, S. Durand, and F. Hug, “No evidence of expertise-related changes in muscle synergies during row-  Y. Okubo, K. Kaneoka, A. Imai et al., “Electromyographic ing,” Journal of Electromyography and Kinesiology, vol. 21, analysis of transversus abdominis and lumbar multiﬁdus using no. 6, pp. 1030–1040, 2011. wire electrodes during lumbar stabilization exercises,” The Journal of Orthopaedic and Sports Physical Therapy, vol. 40,  N. A. Turpin, A. Guével, S. Durand, and F. Hug, “Eﬀect of power output on muscle coordination during rowing,” no. 11, pp. 743–750, 2010. European Journal of Applied Physiology, vol. 111, no. 12,  V. K. Stevens, K. G. Bouche, N. N. Mahieu, P. L. Coorevits, pp. 3017–3029, 2011. G. G. Vanderstraeten, and L. A. Danneels, “Trunk muscle  S. Shaharudin and S. K. Agrawal, “Muscle synergies during activity in healthy subjects during bridging stabilization exer- incremental rowing VO2max test of collegiate rowers and cises,” BMC Musculoskeletal Disorders, vol. 7, no. 1, p. 75, 2006. Applied Bionics and Biomechanics 7  J. P. Arokoski, T. Valta, O. Airaksinen, and M. Kankaanpää, “Back and abdominal muscle function during stabilization exercises,” Archives of Physical Medicine and Rehabilitation, vol. 82, no. 8, pp. 1089–1098, 2001.  A. O. Perotto and R. Kayamori, Anatomical Guide for the Elec- tromyographer: The Limbs and Trunk, Nishimura Shoten, Tokyo, Japan, third edition edition, 2007.  D. D. Lee and H. S. Seung, “Algorithms for non-negative matrix factorization,” in Advances in Neural Information Pro- cessing Systems, pp. 556–562, Neural Information Processing Systems Foundation, San Diego, CA, USA, 2001.  G. Torres-Oviedo, J. M. Macpherson, and L. H. Ting, “Muscle synergy organization is robust across a variety of postural perturbations,” Journal of Neurophysiology, vol. 96, no. 3, pp. 1530–1546, 2006.  F. Hug, “Can muscle coordination be precisely studied by sur- face electromyography?,” Journal of Electromyography and Kinesiology, vol. 21, no. 1, pp. 1–12, 2011.  V. C. K. Cheung, A. Turolla, M. Agostini et al., “Muscle synergy patterns as physiological markers of motor cortical damage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 36, pp. 14652– 14656, 2012.  N. A. Turpin, A. Guevel, S. Durand, and F. Hug, “Fatigue- related adaptations in muscle coordination during a cyclic exercise in humans,” The Journal of Experimental Biology, vol. 214, no. 19, pp. 3305–3314, 2011.  L. Wang, Z. Xie, A. Lu et al., “Antagonistic muscle prefatigue weakens the functional corticomuscular coupling during iso- metric elbow extension contraction,” Neuro Report, vol. 31, no. 5, pp. 372–380, 2020.  N. Matsunaga, A. Imai, and K. Kaneoka, “Comparison of modular control of trunk muscle by Japanese archery compet- itive level: a pilot study,” Int J Sport Health Sci, vol. 15, pp. 160– 167, 2017.  N. Matsunaga, A. Imai, and K. Kaneoka, “Comparison of mus- cle synergies before and after 10 minutes of running,” Journal of Physical Therapy Science, vol. 29, no. 7, pp. 1242–1246,  Y. Matsuura, N. Matsunaga, S. Iizuka, H. Akuzawa, and K. Kaneoka, “Muscle synergy of the underwater undulatory swimming in elite male swimmers,” Frontiers in Sports and Active Living, vol. 2, pp. 1–9, 2020.  J. R. Vaz, B. H. Olstad, J. Cabri, P.-L. Kjendlie, P. Pezarat- Correia, and F. Hug, “Muscle coordination during breast- stroke swimming: comparison between elite swimmers and beginners,” Journal of Sports Sciences, vol. 34, no. 20, pp. 1941–1948, 2016.
Applied Bionics and Biomechanics – Hindawi Publishing Corporation
Published: Feb 15, 2021