Evidence for constancy in the modularity of trunk muscle activity preceding reaching: implications for the role of preparatory postural activity

Abstract

Postural muscle activity precedes voluntary movements of the upper limbs. The traditional view of this activity is that it anticipates perturbations to balance caused by the movement of a limb. However, findings from reach-based paradigms have shown that postural adjustments can initiate center of mass displacement for mobility rather than minimize its displacement for stability. Within this context, altering reaching distance beyond the base of support would place increasing constraints on equilibrium during stance. If the underlying composition of anticipatory postural activity is linked to stability, coordination between muscles (i.e., motor modules) may evolve differently as equilibrium constraints increase. We analyzed the composition of motor modules in functional trunk muscles as participants performed multidirectional reaching movements to targets within and beyond the arm's length. Bilateral trunk and reaching arm muscle activity were recorded. Despite different trunk requirements necessary for successful movement, and the changing biomechanical (i.e., postural) constraints that accompany alterations in reach distance, nonnegative matrix factorization identified functional motor modules derived from preparatory trunk muscle activity that shared common features. Relative similarity in modular weightings (i.e., composition) and spatial activation profiles that reflect movement goals across tasks necessitating differing levels of trunk involvement provides evidence that preparatory postural adjustments are linked to the same task priorities (i.e., movement generation rather than stability).NEW & NOTEWORTHY Reaching within and beyond arm's length places different task constraints upon the required trunk motion necessary for successful movement execution. The identification of constant modular features, including functional muscle weightings and spatial tuning, lend support to the notion that preparatory postural adjustments of the trunk are tied to the same task priorities driving mobility, regardless of the future postural constraints.

Keywords: coordination; motor module/synergy; postural adjustment; reach; trunk muscles.

Graphical abstract

Figure 1.

A: schema of predicted module weightings (W_i) and module tuning (C_i) as a function of mobility, stability, or changing task demands as trunk involvement increases across reach distance. In the current study, targets necessitated reaching movements to 70%, 100%, or 130% of total arm length (see methods) to produce movements within and beyond arm’s length. For movement to targets requiring right rotation (e.g., 0°–30° represented by the gray bar in C_i), increases in weightings for muscles driving movement (i.e., greater contributions in W_i of muscles producing right rotation, Rr, see solid color) would show greater module tuning in the same direction as the movement goals. If reflective of a postural control strategy for mobility (i.e., pPA = Movement Goals), extracted module weightings and coefficient tuning would remain similar irrespective of reach distance, such that W_{i 70%} ∼ W_{i 130%} and C_{i 70%} ∼ C_{i 130%}. B: schema of experimental setup for reach paradigm. Ant., anterior; Lr, muscles producing leftward (counterclockwise) rotation; Post., posterior; pPA, preparatory postural adjustment; Pred., prediction; rot., rotation; Rr, muscles producing rightward (clockwise) rotation.

Figure 2.

Mean trunk excursion (A) and center of mass (CoM) metrics (B–D) for all participants across reaching direction and reaching distance. As reaching distance moved beyond arm’s length, trunk contribution to movement increased in both the anteroposterior (AP) and mediolateral (ML) planes and was associated with similar changes in CoM excursion. Tangential CoM velocity and acceleration profiles for each direction were aligned to movement onset and offset (see methods). See legend for direction color scheme and representation of significant differences in AP and ML measures. Acc, acceleration; sig. diff, significant difference; Vel., velocity.

Figure 3.

Mean surface electromyography (sEMG) activity (A) and representative muscle tuning curves (B) for 2 arm and 12 trunk muscles of a typical participant (S03) over 5 directions (0°, 45°, 90°, 135°, and 180°) for reaching to targets across reach distances (70%, 100%, and 130% total reach distance). A: traces show a period of 500-ms preceding and proceeding movement onset. The shaded area represents the preparatory postural adjustment period, occurring before finger movement onset (black solid line), where data pertaining to the motor module analysis is derived. B: tuning curves highlighting the evolution of activation for muscles of the arm and trunk across the final 3 epochs of the preparatory postural adjustment period (pPA, 3–5) for reaching to 70% (light gray), 100% (dark gray), and 130% (black) of total reaching distance. Epochs consist of mean muscle activity + SD, for 15 trials, recorded over a 50-ms window for each muscle (filled circles). ADelr, right anterior deltoid muscle; EOl, left external oblique muscle; EOr, right external oblique muscle; IOTrAl, left combined internal oblique and transversus abdominis muscle; IOTrAr, right combined internal oblique and transversus abdominis muscle; Latl, left latissimus dorsi muscle; Latr, right latissimus dorsi muscle; LumESl, left lumbar erector spinae muscle; LumESr, right lumbar erector spinae muscle; Multl, left multifidus muscle; Multr, right multifidus muscle; PDelr, right posterior deltoid muscle; RAl, left rectus abdominis muscle; RAr, right rectus abdominis muscle.

Figure 4.

Comparison of similarity in mean muscle activation tuning curves across reaching distance data for the final epoch before movement onset (i.e., pPA5) using principal component analysis. The contribution of a single muscle tuning curve from each reaching distance (see color scheme in legend) to the primary extracted principal component (PC1, in black) is reflected by the variance accounted for (i.e., VAF). Greater values of VAF reflect higher similarity in activation coefficients across within (70%), at (100%), and beyond (130%) arm-reaching distances. ADelr, right anterior deltoid muscle; EO, external oblique muscle; IOTrA, internal oblique and transversus abdominis muscle; Lat, latissimus dorsi muscle; LumES, lumbar erector spinae muscle; Mult, multifidus muscle; PDelr, right posterior deltoid muscle; pPA, preparatory postural adjustment; RA, rectus abdominis muscle.

Figure 5.

Validation of the number of motor modules using both global (A) and local (B) criteria of the variability accounted for (VAF) during reconstruction of S02, and total number of motor modules (C) and percentage of shared motor modules (D) extracted across reaching distances. A: 95% confidence limits were estimated for the reconstruction of the original data set and compared with limits calculated with a shuffled data (see methods). The gray bar shows the number of motor modules identified by all VAF criteria. B: local criteria relating to the VAF for each respective muscle over all trials and under each time condition (i.e. epoch). Additional modules were added until a minimum threshold of 75% VAF was satisfied for both local conditions. C: the mean number of extracted motor modules (red bar) did not change as movements shifted from within to beyond arm’s length. Connected circles (gray) represent the number of motor modules for an individual participant. D: for each participant (gray circle), the percentage of shared motor modules was similar. Although the percentage shared was reduced when all conditions were considered (i.e., All), when subdivided, much greater similarity was seen. Graphs consist of mean + SD (purple bar). ADelr, right anterior deltoid muscle; EOr, right external oblique muscle; IOTrAl, left combined internal oblique and transversus abdominis muscle; IOTrAr, right combined internal oblique and transversus abdominis muscle; Latl, left latissimus dorsi muscle; Latr, right latissimus dorsi muscle; LumESl, left lumbar erector spinae muscle; LumESr, right lumbar erector spinae muscle; Multl, left multifidus muscle; Multr, right multifidus muscle; PDelr, right posterior deltoid muscle; pPA, preparatory postural adjustment; RAl, left rectus abdominis muscle; RAr, right rectus abdominis muscle.

Figure 6.

Motor modules extracted from all participants (n = 5) and across each reaching distance (70%, 100%, 130%). Modules are color coded based on their similarity in module weightings (i.e., composition) or module coefficients (see methods for criteria). Individual bars represent the relative weighting of a single muscle to the motor module. Modules that did not meet the criteria for similarity across all reach distance conditions were then grouped based on the spatial tuning reflected in the module tuning for the final epoch (pPA5) using PCA. Such modules are highlighted in light gray for dissimilar weightings comparisons for 70% vs. 130% and dark gray for dissimilar comparisons between 70% and 100% vs. 130%. ADelr, right anterior deltoid muscle; EOr, right external oblique muscle; IOTrAl, left combined internal oblique and transversus abdominis muscle; IOTrAr, right combined internal oblique and transversus abdominis muscle; Latl, left latissimus dorsi muscle; Latr, right latissimus dorsi muscle; LumESl, left lumbar erector spinae muscle; LumESr, right lumbar erector spinae muscle; Multl, left multifidus muscle; Multr, right multifidus muscle; PDelr, right posterior deltoid muscle; PCA, principal component analysis; pPA, preparatory postural adjustment; RAl, left rectus abdominis muscle; RAr, right rectus abdominis muscle; VAF, variability accounted for.