Our previously published articles on this dataset describe our analysis of the kinematic and kinetic data [21, 24]. Here, we introduce all the steps regarding the EMG analysis.
Participants
Twenty young and healthy volunteers (10 women, 10 men; 25.5 ± 3.8 years, 1.71 ± 0.08 m height, 67.6 ± 10.9 kg mass) gave written informed consent and participated in the study. The participant shown in Fig. 1 gave informed consent to publish the image. The Ethics Committee of the Medical Department of Heidelberg University (S-105/2021) approved the study, which was then performed according to the Declaration of Helsinki.
Experimental protocol
The participants sat still and, after hearing “stand up” by the experimenter, they stood up at their own pace. Then, the experimenter said, “stand still”. After standing still for at least two seconds, the experimenter said, “sit down,” and the participants sat down at their own pace. The seat height was set to the height of the participant’s lateral epicondyle of the femur, and a custom-built robot rollator simulator was used to provide rollator support (Fig. 1). Following recommendations in the health care literature [60–62], the handle height was set at the participant’s standing wrist height. According to the support condition, they did not use the rollator handles at all (unassisted, UA), only with a light touch of the hand (light touch, LT) or with a power grip (full support, FS). These support conditions were combined with two floor conditions: the standard lab floor and a more "challenging ground", which was created by positioning a circular rubber balance pad with a compliant surface (Dynair® Ballkissen®, diameter 33 cm, height 8 cm, TOGU GmbH, Prien-Bachham, Germany) under each foot. Participants familiarized themselves with the task by performing two repetitions in each condition combination (support: unassisted, light touch, full support; floor: non-challenging, challenging). No further instructions on the movement execution were given, allowing the participants to stand up and sit down as naturally as possible. All participants performed three valid, non-consecutive repetitions in each condition combination, resulting in a total of 18 trials per participant. The order of the support and floor conditions was randomized across participants.
<Please insert Fig. 1.pdf here>
Figure 1: Experimental setup and data analysis. A: The participant stands up from an instrumented chair with the custom-made robot rollator simulator. Full-body passive markers for motion tracking and EMG electrodes were placed on the body. Two movements were studied: sit-to-stand and stand-to-sit. Two floor conditions were used (middle): non-challenging (lab floor) and challenging (balance pads). Three different support conditions were used (right): unassisted (handles not used), light touch (palm on the handles), and full support (power grip). B: Participants used different movement strategies and switched between them, as exemplarily shown for the non-challenging sit-to-stand task. The bottom plot shows the distribution of the trials among strategies. One dot represents one trial. The row indicates to which movement strategy it belongs. The column shows to which participant it belongs. The support conditions are color-coded as indicated by the legend. The labels on the right y-axis show how many trials were associated with the strategy written on the left y-axis. The figure is adapted from [24]. C: EMG data from the trials of the same movement strategy were arranged into a matrix (for example, Mvertical rise). Temporal muscle synergies were extracted from each matrix with NMF [63–65], resulting in trial-independent activation profiles and trial-dependent muscle activation vectors. The activation profiles were matched across the movement strategies and ordered chronologically using k-means + + clustering, ensuring a correlation coefficient above 0.9. Bottom: The duration of each activation profile was assessed as full-width at half-maximum. Linear mixed models were used to investigate how rollator support affects the muscle activation vectors. Abbreviations: P1: participant 1, UA1: first unassisted trial, LT1: first light touch trial, FS1: first full support trial, ES: M. erector spinae, RA: M. rectus abdominis, NMF: non-negative matrix factorization [63, 64].
Data collection
Full-body 3D kinematics were obtained using the IOR full-body marker model [66, 67] and ten cameras (150 Hz; Type 5+, Qualisys, Gothenburg, Sweden). Ground reaction forces (GRF; 1000Hz; Bertec Corp., Columbus, OH, USA) and forces on the seating surface (142 Hz; Phidgets Inc., Calgary, AB, Canada) were measured.
Thirty surface EMG electrodes (two 16-channel systems at 1500 and 4000 Hz; Noraxon USA, Scottsdale, AZ, USA) captured full-body muscle activity of the following muscles bilaterally: pectoralis major (Pec), latissimus dorsi (Lat), trapezius (Tra), deltoideus (Del), biceps brachii (Bic), triceps brachii (Tri), gluteus medius (GM), tensor fasciae latae (TF), rectus femoris (RF), vastus medialis (VM), biceps femoris (BF), tibialis anterior (TA), peroneus longus (PL), and gastrocnemius (GA). Additionally, erector spinae (ES) and rectus abdominis (RA) activities were recorded. The participants’ skin was prepared by shaving, abrasion, and cleansing with alcohol to ensure good electrode-skin contact before the Al/AgCl electrodes were attached according to SENIAM guidelines [68] and [69].
Data processing
To reconstruct the 3D coordinates of the markers, raw kinematic data were processed offline with Qualisys Track Manager (v 2018.1). Subsequently, force and kinematic data were filtered with a 4th -order zero-lag low-pass Butterworth filter at 10 Hz. Using Visual3D (v6, C-Motion Inc., Germantown, MD, USA), full-body kinematics and the center of mass (CoM) were then calculated. Further data analyses were done in Matlab (R2023b, Natick, MA, USA). Raw EMG data were bandpass (20–500 Hz) and notch (50 Hz) filtered with a 4th -order zero-lag Butterworth filter [49]. ECG artefacts apparent in the trunk muscle recordings were removed with a template-matching procedure [70]. For robustness, we created a muscle- and participant-specific template of ECG artefacts using the data from the sit-to-stand and stand-to-sit recordings and an additional 9 minutes of still-standing recordings. Subsequently, filtered EMG data were full-wave rectified and smoothed with a 4th -order zero-lag low-pass Butterworth filter at 10 Hz [49]. Movement start, seat-off/on, and movement end were identified using a k-means + + algorithm on the GRF and CoM data [71]. As muscles need to be active before a visible movement starts, data from 200 ms before the detected start of the movement were included [72, 73]. Afterward, data were segmented and time-normalized to 101 time points (100%) using a spline interpolation. Finally, EMG data were amplitude-normalized per muscle and participant to their maximum activity across the 18 trials [64]. Of the 720 trials, 24 were not included in the analyses as some recordings of a few muscles were corrupt (Supplementary Table 1, Additional File 1).
Movement strategies
Our previous investigation found that participants switched movement strategies when introduced to a rollator [24]. In particular, three movement strategies were identified for the sit-to-stand non-challenging task (“forward leaning”, “hybrid, and “vertical rise”) and two for the challenging task (“exaggerated forward leaning” and “forward leaning”). Likewise, three and two movement strategies were identified respectively in the stand-to-sit tasks (“vertical lowering”, “hybrid”, and “backward lowering”; and “exaggerated forward leaning” and “forward leaning”). The naming of these strategies was inferred by visual inspection of their movement progression, the different hip, knee, and ankle sagittal angle courses, and the relative movements between the CoM and the heel. The grouping of trials into the movement strategies was used in the current analysis to extract muscle synergies specific to the movement strategies. Supplementary Fig. 1, Additional File 1 shows the distribution of trials among strategies.
Data analysis
3.1.1 Muscle synergy analysis
We extracted muscle synergies with respect to our previous findings that participants switched their movement strategies when introduced to a rollator ([24]; Fig. 1). As stated in the introduction, the two models (spatial and temporal muscle synergies) describe different aspects of movement coordination [42, 74–77]. Temporal muscle synergies allow us to follow the underlying assumption that the CNS uses a fixed temporal sequence (trial-independent activation profiles) for the different movement strategies and that muscle weightings vary (trial-dependent muscle activation vectors) across the support conditions. Therefore, the EMG signals (30 channels) of all trials belonging to the same strategy (strat) were horizontally concatenated into a data matrix \(\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t}}\in\:{\mathbb{R}}_{\ge\:0}^{101\:\times\:\:30\bullet\:\text{t}\text{r}}\). NMF decomposed Mstrat into a set of Nstrat trial-independent activation profiles \(\:{\text{C}}_{\text{s}\text{t}\text{r}\text{a}\text{t},\text{n}}\in\:{\mathbb{R}}_{\ge\:0}^{101\:\times\:\:1}\), and trial-dependent muscle activation vectors\(\:\:{\mathbf{W}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\:\mathbf{n}}^{\mathbf{s}}\in\:{\mathbb{R}}_{\ge\:0}^{30\:\times\:\:1}\) [63–65]. Thus, EMG data from a single trial (s is the trial index) \(\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t}}^{\mathbf{s}}\left(\text{t}\right)\) were decomposed with:
$$\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t}}^{\mathbf{s}}\left(\text{t}\right)\approx\:{\sum\:}_{\text{n}\in\:{\text{N}}_{\text{s}\text{t}\text{r}\text{a}\text{t}}}{\text{C}}_{\text{s}\text{t}\text{r}\text{a}\text{t},\:\text{n}}\left(\text{t}\right)\:\cdot\:{\mathbf{W}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\mathbf{n}}^{\mathbf{s}}$$
To investigate hypothesis 1 (that temporal muscle synergies represent sit-to-stand and stand-to-sit EMG patterns more compactly than spatial muscle synergies), we also extracted spatial muscle synergies. Therefore, the EMG signals (30 channels) of all trials belonging to the same strategy (strat) were horizontally concatenated into a data matrix \(\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\:\:\:\mathbf{s}\mathbf{p}\mathbf{a}\mathbf{t}\mathbf{i}\mathbf{a}\mathbf{l}}\in\:{\mathbb{R}}_{\ge\:0}^{30\:\times\:\:101\bullet\:\text{t}\text{r}}\). NMF decomposed Mstrat, spatial into a set of Nstrat, spatial trial-independent muscle activation vectors \(\:{\mathbf{W}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\mathbf{n},\:\mathbf{s}\mathbf{p}\mathbf{a}\mathbf{t}\mathbf{i}\mathbf{a}\mathbf{l}}\in\:{\mathbb{R}}_{\ge\:0}^{30\:\times\:\:1}\), and trial-dependent activation profiles \(\:{\text{C}}_{\text{s}\text{t}\text{r}\text{a}\text{t},\:\text{n},\text{s}\text{p}\text{a}\text{t}\text{i}\text{a}\text{l}}^{\text{s}}\in\:{\mathbb{R}}_{\ge\:0}^{1\:\times\:\:101}\) [63–65]. Thus, EMG data from a single trial (s is the trial index) \(\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\:\mathbf{s}\mathbf{p}\mathbf{a}\mathbf{t}\mathbf{i}\mathbf{a}\mathbf{l}}^{\mathbf{s}}\left(\text{t}\right)\) were decomposed with:
$$\:{\mathbf{M}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\mathbf{s}\mathbf{p}\mathbf{a}\mathbf{t}\mathbf{i}\mathbf{a}\mathbf{l}}^{\mathbf{s}}\left(\text{t}\right)\approx\:{\sum\:}_{\text{n}\in\:{\text{N}}_{\text{s}\text{t}\text{r}\text{a}\text{t},\text{s}\text{p}\text{a}\text{t}\text{i}\text{a}\text{l}}}{\mathbf{W}}_{\mathbf{s}\mathbf{t}\mathbf{r}\mathbf{a}\mathbf{t},\mathbf{n},\mathbf{s}\mathbf{p}\mathbf{a}\mathbf{t}\mathbf{i}\mathbf{a}\mathbf{l}}\cdot\:{\text{C}}_{\text{s}\text{t}\text{r}\text{a}\text{t},\text{n},\text{s}\text{p}\text{a}\text{t}\text{i}\text{a}\text{l}}^{\text{s}}\left(\text{t}\right)$$
NMF’s iterative decomposition was limited to 3000 iterations and started 50 times to avoid convergence to a local minimum [48, 78].
A 5-fold cross-validation procedure was used to increase the confidence that the extracted muscle synergies were robust and generalizable rather than due to characteristics of single trials. In line with the literature, a training/test split of 80:20 was employed [32, 79]. Muscle synergies were extracted from a random 80% portion of the trials. Then, the trial-independent parts were fixed and fitted to the remaining 20% of the trials. Finally, the reconstruction quality R²CV of the fits to the test sets was used to identify the number of synergies. R² is a multivariate measure allowing assessment of the reconstruction quality: R² = 1 − SSE/SST, with SSE being the sum of the squared residuals and SST the sum of the squared residuals from the mean vector [80]. The numbers of synergies Nstrat and Nstrat,spatial were chosen at the R² knee point, after which the R² curve remained approximately straight [80]. Therefore, a series of linear regressions were fitted to the R² curve, starting with the interval [N1, N30] and iteratively removing the smallest N from the interval. Then, the regressions’ mean squared residual errors (MSE) were calculated, and Nstrat and Nstrat,spatial were selected for the first number N with an MSE smaller than 10− 4. The number of synergies to extract must be chosen carefully to obtain a good low-dimensional representation of the data with minimum noise [81, 82], and numerous criteria have been proposed [83]. To avoid the results being specific to the choice of Nstrat, rather than reflecting physiological patterns, an additional criterion was used to compare the results. Therefore, Nstrat* was chosen to be the minimum number fulfilling both a global (\(\:{R}_{{N}_{strat}}^{2}\ge\:0.9\)) and a local criterion (\(\:{R}_{n}^{2}-{R}_{n-1}^{2}<0.05;\:n=1...{N}_{strat}\)).
To justify the choice of temporal muscle synergies beyond the assumption that the CNS uses a fixed temporal sequence (trial-independent activation profiles) for the different movement strategies and that muscle weightings vary (trial-dependent muscle activation vectors) across the support conditions (degree of handle support), we extracted spatial synergies and evaluated the dimensionality reduction (R²-knee criterion) against the dimensionality reduction of the temporal extraction (Nstrat and Nstrat, spatial). Furthermore, the number of trial-dependent parameters (temporal: synergies ∙ muscles, spatial: time samples ∙ synergies) and the number of trial-independent parameters (temporal: time samples ∙ synergies, spatial: synergies ∙ muscles) were compared between the temporal and spatial extraction, with the number of synergies selected at the respective R² knee [41]. All steps regarding muscle synergy analyses were done separately for the two movements and floor conditions.
3.1.2 Matching of similar synergies across the movement strategies
To investigate hypothesis 2, that the activation profiles of the temporal muscle synergies differ across movement strategies, the activation profiles were matched with k-means + + clustering (Fig. 1; [84]). A correlation coefficient [84] of at least 0.9 per match was ensured. Only one activation profile per strategy was included within each cluster. The clustering was repeated ten times to confirm the robustness of the cluster assignments [85].
3.1.3 Statistics
Timing and duration of temporal synergies
To investigate hypothesis 2 that the activation profiles of the temporal muscle synergies differ across movement strategies beyond their similarity (see 3.5.2), we assessed the duration of activation by measuring the full-width at half-maximum of the main peak (FWHM; Matlab findpeaks; [84]. Therefore, the time difference between the two points at half-height on either side of the main peak was calculated. As sit-to-stand and stand-to-sit are sequential movements, we cannot assume that the boundary synergies (synergies with the peaks close to the movement start and end) are symmetrical. In the case of boundary synergies, we measured the difference between the movement start and the point of half-height of the descending synergy or the difference between the point of half-height and the movement end.
Linear mixed model to assess differences in the activation vectors
To investigate hypothesis 3, i.e., to identify the changes in the muscle weightings between the support conditions (unassisted, light touch, full support), a linear mixed model (LMM) was used (Matlab fitlme). The LMM considers that repeated measures of a single participant are likely correlated [86, 87] allowing us to manage the distribution of participants’ trials over several movement strategies. To account for the simultaneous changes in multiple muscle activations (trial-dependent muscle activation vectors) with support condition, a multivariate LMM approach was used [88].
Single trials (level 1) were nested into participants (level 2). The support conditions were included as dummy variables using reference coding (LT or FS set to 1, or both to 0 for the unassisted condition). The first multivariate LMM was calculated with UA as the reference group, and the second multivariate LMM with LT as the reference group, allowing investigation of all pairwise comparisons within the support conditions. Each muscle activation vector belongs to one temporal synergy, i.e., the reference frames in which the muscle activation vectors lie are different across the temporal synergies, so one multivariate LMM was used for each muscle vector. For example, for the non-challenging sit-to-stand task using the forward leaning strategy, seven synergies led to 14 multivariate LMM tests within this task (seven synergies tested once with UA and once with LT as reference group). Sex was added as a within-participant control variable at level 1 but was not included in the final model as it did not improve the model based on the change in the − 2 log-likelihood or the Akaike's information criterion (Matlab’s linearmixedmodel.compare function; [89, 90]). The residual plots were inspected to assess linearity and homoscedasticity as prerequisites for LMM, and no gross violations were found [91].
The multivariate LMM regression formula was:
Level 1: \(\:\text{A}\text{c}\text{t}\text{i}\text{v}\text{a}\text{t}\text{i}\text{o}{\text{n}}_{\text{t}\text{p}}={{\beta\:}}_{0\text{p}}+{{\beta\:}}_{1\text{p}}\text{L}{\text{T}}_{\text{t}\text{p}}+{{\beta\:}}_{2\text{p}}\text{F}{\text{S}}_{\text{t}\text{p}}+{\text{ϵ}}_{\text{t}\text{p}}\)
Level 2: \(\:{{\beta\:}}_{0\text{p}}={{\gamma\:}}_{00}+{\text{u}}_{0\text{p}}\)
$$\:{{\beta\:}}_{1\text{p}}={{\gamma\:}}_{10}$$
$$\:{{\beta\:}}_{2\text{p}}={{\gamma\:}}_{20}$$
\(\:\text{A}\text{c}\text{t}\text{i}\text{v}\text{a}\text{t}\text{i}\text{o}{\text{n}}_{\text{t}\text{p}}\) represents the mean activation across the left and right limb of each bilaterally assessed muscle and the single muscle activation of M. erector spinae and M. rectus abdominis of a given synergy on the tth trial for the pth participant. The \(\:{{\beta\:}}_{0\text{p}}\) represents the intercept, \(\:{{\beta\:}}_{1\text{p}}\) and \(\:{{\beta\:}}_{2\text{p}}\) the fixed effects for the support conditions, and \(\:{\text{ϵ}}_{\text{t}\text{p}}\) represents the trial- and participant-specific residual. The variable \(\:{\text{u}}_{0\text{p}}\) is a support-specific random component of \(\:{{\beta\:}}_{0\text{p}}\) and the \(\:{\gamma\:}\) fixed effect parameters. Accordingly, the following formula was used for the function specification of the fitlme function: ‘Activation ~ LT + FS + (1 | Participant)’. To account for the multivariate nature, muscle activities were vertically concatenated into \(\:\text{A}\text{c}\text{t}\text{i}\text{v}\text{a}\text{t}\text{i}\text{o}{\text{n}}_{\text{t}\text{p}}\). For the second multivariate LMM test, ‘LT’ was exchanged with ’UA’ to have LT as the reference group. The t-statistic on the ß coefficients was used for hypothesis testing with the significance set a priori at a two-sided α = 0.05 [90]. To reduce the probability of type I errors, the level of significance was adjusted according to the number of tests within one movement strategy (e.g., for the seven synergies in the non-challenging, sit-to-stand forward leaning strategy, the level of significance was adjusted for 14 tests with Bonferroni correction).
If the multivariate LMM showed significance regarding the support groups [88], MscName (a categorical variable representing the muscle names) was used in the second step as a dummy variable of the LMM analyses using effect coding. Therefore, the interaction between the muscles and the support condition was added to the LMM. This revealed the muscles in which the support condition affects their activation with respect to the mean of the group mean of the reference muscle (M. Rectus abdominis) and support group (effect coding). Consequently, the following model was used:
Level 1: \(\:\text{A}\text{c}\text{t}\text{i}\text{v}\text{a}\text{t}\text{i}\text{o}{\text{n}}_{\text{t}\text{p}}={{\beta\:}}_{0\text{p}}+{{\beta\:}}_{1\text{p}}\text{L}{\text{T}}_{\text{t}\text{p}}+{{\beta\:}}_{2\text{p}}\text{F}{\text{S}}_{\text{t}\text{p}}+{\varvec{\beta\:}}_{3\mathbf{p}}^{\mathbf{T}}{\mathbf{M}\mathbf{s}\mathbf{c}\mathbf{N}\mathbf{a}\mathbf{m}\mathbf{e}}_{\mathbf{p}}+\:{\varvec{\beta\:}}_{4\mathbf{p}}^{\mathbf{T}}\text{L}{\text{T}}_{\text{t}\text{p}}{\mathbf{M}\mathbf{s}\mathbf{c}\mathbf{N}\mathbf{a}\mathbf{m}\mathbf{e}}_{\mathbf{p}}+{\varvec{\beta\:}}_{5\mathbf{p}}^{\mathbf{T}}\text{F}{\text{S}}_{\text{t}\text{p}}{\mathbf{M}\mathbf{s}\mathbf{c}\mathbf{N}\mathbf{a}\mathbf{m}\mathbf{e}}_{\mathbf{p}}+\:{\text{ϵ}}_{\text{t}\text{p}}\)
Level 2: \(\:{{\beta\:}}_{0\text{p}}={{\gamma\:}}_{00}+{\text{u}}_{0\text{p}}\)
$$\:{{\beta\:}}_{1\text{p}}={{\gamma\:}}_{10}$$
$$\:{{\beta\:}}_{2\text{p}}={{\gamma\:}}_{20}$$
$$\:{\varvec{\beta\:}}_{3\mathbf{p}}={\varvec{\gamma\:}}_{30}$$
$$\:{\varvec{\beta\:}}_{4\mathbf{p}}={\varvec{\gamma\:}}_{40}$$
$$\:{\varvec{\beta\:}}_{5\mathbf{p}}={\varvec{\gamma\:}}_{50}$$
Matlab model function: Activation ~ (LT + FS) * MscName + (1 | Participant)
To reduce the probability of type I errors, the significance level (α = 0.05) was adjusted to the number of tests with the second model, at maximum three if a significant effect was found for each pairwise comparison of UA, LT, and FS. The LMM was implemented using the maximum likelihood method.