Muscle Synergies in Children Walking and Running on a Treadmill

Abstract

Muscle synergies reflect the presence of a common neural input to multiple muscles. Steering small sets of synergies is commonly believed to simplify the control of complex motor tasks like walking and running. When these locomotor patterns emerge, it is likely that synergies emerge as well. We hence hypothesized that in children learning to run the number of accompanying synergies increases and that some of the synergies' activities display a temporal shift related to a reduced stance phase as observed in adults. We investigated the development of locomotion in 23 children aged 2-9 years of age and compared them with seven young adults. Muscle activity of 15 bilateral leg, trunk, and arm muscles, ground reaction forces, and kinematics were recorded during comfortable treadmill walking and running, followed by a muscle synergy analysis. We found that toddlers (2-3.5 years) and preschoolers (3.5-6.5 years) utilize a "walk-run strategy" when learning to run: they managed the fastest speeds on the treadmill by combining double support (DS) and flight phases (FPs). In particular the activity duration of the medial gastrocnemius muscle was weakly correlated with age. The number of synergies across groups and conditions needed to cover sufficient data variation ranged between four and eight. The number of synergies tended to be smaller in toddlers than it did in preschoolers and school-age children but the adults had the lowest number for both conditions. Against our expectations, the age groups did not differ significantly in the timing or duration of synergies. We believe that the increase in the number of muscle synergies in older children relates to motor learning and exploration. The ability to run with a FP is clearly associated with an increase in the number of muscle synergies.

Keywords: children; development; locomotion; muscle synergies; running; treadmill.

FIGURE 1

Temporal gait parameters. (A) Percentage double support and flight phase during walking (blue) and running (red). Flight phase is depicted with negative numbers. Vertical dotted lines separate the different groups: Toddlers, Preschoolers, School-age, and Adults, (B) Stride duration for walking and running, (C) Stance duration for walking and running, and (D) Froude number for walking and running. DS, double support; FP, flight phase; s, seconds; T, toddlers; P, preschoolers; S, school-age; A, adults; V, velocity, g, gravitational constant; L, leg length. *p < 0.01 and **p < 0.001.

FIGURE 2

Characteristics of EMG signals. (A) Grand averages of 15 EMG activity patterns for walking (blue) and running (red) for all four groups, data are plotted vs. normalized gait cycle, relative duration of stance varied across groups, a bar indicates an amount of variability in the stance phase duration across groups. (B) Phase shift between the peak activation of medial gastrocnemius (MG) for walking and running for each group, positive value indicates a lag of walking signal relative to running signal. (C,D) Full-width half-maximum (FWHM) of the MG activity as a function of age for walking (C) and running (D). Continuous lines represent exponential fittings, note the decrease in values with age. (E) FWHM of all muscles (means + SD) for the four groups. TA, tibialis anterior; MG, medial gastrocnemius; BF, biceps femoris; VMO, vastus medialis oblique; RF, rectus femoris; TFL, tensor fascia latae; GM, gluteus maximus; ES, erector spinae; LD, latissimus dorsi; AD, anterior deltoid; PD, posterior deltoid; TRAP, trapezius; TB, triceps brachii; BB, biceps brachii; BR, brachioradialis; T, toddlers; P, preschoolers; S, school-age; A, adults; FWHM, full-width half-maximum. *p < 0.01, **p < 0.001, and ***p < 0.0001.

FIGURE 3

Number of synergies and accuracy. (A) Number of synergies needed to account for the cycle-to-cycle variability of EMG activity during walking and running for each group as determined by principal component analysis PCA (>80% of variance). (B) The corresponding reconstruction accuracy (RA) after rank-reduction with PCA followed by NMF. (C) The RA (mean SD) for each muscle and condition (blue = walking, red = running). TA, tibialis anterior; MG, medial gastrocnemius; BF, biceps femoris; VMO, vastus medialis oblique; RF, rectus femoris; TFL, tensor fascia latae; GM, gluteus maximus; ES, erector spinae; LD, latissimus dorsi; AD, anterior deltoid; PD, posterior deltoid; TRAP, trapezius; TB, triceps brachii; BB, biceps brachii; BR, brachioradialis; T, toddlers; P, preschoolers; S, school-age; A, adults.

FIGURE 4

Muscle synergy structure for the four groups for walking (left; in blue) and running (right; in red). Vertical dotted line in activation timing plots represents the end of the stance phase. Each colored line represents a participant side, leading to one line for right side and one line for left side for each participant resulting in a total of (n = 10) for the toddler group, (n = 12) for the preschoolers, (n = 24) for the school-age group, and (n = 14) for the adult group. Black lines represent the mean. Y-axis is in arbitrary units. In the weighting plots, each colored bar represents the weighting coefficient for one participant side, the weightings are ordered based on their size. The black outlines represent the mean for the group. TA, tibialis anterior; MG, gastrocnemius medialis; BF, biceps femoris; VMO, vastus medialis oblique; RF, rectus femoris; TFL, tensor fascia latae; GM, gluteus maximus; ES, erector spinae; LD, latissimus dorsi; AD, anterior deltoid; PD, posterior deltoid; TRAP, trapezius; TB, triceps brachii; BB, biceps brachii; and BR, brachioradialis.

FIGURE 5

FWHM of consistent activation waveforms and phase shift between walking and running activation waveforms. (A) FWHM of all waveforms as a function of the percentage of the gait cycle for each group. Color-coding refer to the groups. (B) Phase shift as a function of the gait cycle, determined using the cross-covariance between the waveforms for walking and running. Means and standard deviations are given per group. FWHM, full-width half-maximum. *p < 0.01.