Age-related changes in the neuromuscular control of forward and backward locomotion

Abstract

Previous studies found significant modification in spatiotemporal parameters of backward walking in healthy older adults, but the age-related changes in the neuromuscular control have been considered to a lesser extent. The present study compared the intersegmental coordination, muscle activity and corresponding modifications of spinal montoneuronal output during both forward and backward walking in young and older adults. Ten older and ten young adults walked forward and backward on a treadmill at different speeds. Gait kinematics and EMG activity of 14 unilateral lower-limb muscles were recorded. As compared to young adults, the older ones used shorter steps, a more in-phase shank and foot motion, and the activity profiles of muscles innervated from the sacral segments were significantly wider in each walking condition. These findings highlight age-related changes in the neuromuscular control of both forward and backward walking. A striking feature of backward walking was the differential organization of the spinal output as compared to forward gait. In addition, the resulting spatiotemporal map patterns also characterized age-related changes of gait. Finally, modifications of the intersegmental coordination with aging were greater during backward walking. On the whole, the assessment of backward walk in addition to routine forward walk may help identifying or unmasking neuromuscular adjustments of gait to aging.

Fig 1. Elevation angles of lower-limb segments and general gait parameters during forward (FW) and backward (BW) walking in young and older adults.

A—Elevation angles of the trunk, thigh, shank and foot over a stride. All the curves of each subject walking at a given walking condition were first averaged (mean-curve). The curves presented here are the average of the mean-curves of all the young (grey lines) and older (black lines) adults. The grey zone represents±1 SD for the older adults. B—Average range of motion of the thigh, shank and foot over one stride. C—Average, stride period, relative stance phase and mean trunk inclination over one stride. In panel B and C, the bars represent the grand mean of all the young (grey) and the older (black) adults. Thin lines represent one standard deviation. The * indicates a significant effect of age.

Fig 2. Planar covariation of elevation angles.

A–Covariation of the ensemble-average limb-segment elevation angles during forward (right—1.11 m s⁻¹) and backward (left– 3 km h^-1) walking in young (up) and older adults (bottom). Note that when the elevation angles of thigh, shank and foot are plotted one versus the other in a x-y-z space, they co-vary along a loop constrained on a plane (x–y). Grids show the best-fitting plane. B–Average percentage of variance accounted for by the first (left—PV₁), second (middle—PV₂) and third (right–PV₃) eigenvector of the principal component analysis and the direction cosines of the normal to the covariation plane with the positive semi-axis of the thigh angular coordinates (u3t). C–Average amplitude ratios between the range of motion of adjacent segments and phase lags between time curves of elevation angles of adjacent segments. In panel A and B, grey bars correspond to young adults, whereas black bars correspond to older adults. The * indicates a significant effect of age.

Fig 3. Ensemble-averaged electromyogram (EMG) patterns during forward and backward walking in young and older adults.

A–ensemble-averaged EMG patterns over one stride. ES, erector spinae; GM, gluteus maximus; Gmed, gluteus medius; SART, sartorius; TFL, tensor fascia latae; ADD, adductor longus; VM, vastus medialis; VL, vastus lateralis; RF, rectus femoris; BF, biceps femoris; ST, semitendinous; TA, tibialis anterior; MG, gastrocnemius medialis; LG, lateral gastrocnemius; SOL, soleus; PERL, peroneus longus. The curves presented here are the average of the mean-curves of all the young (grey lines) and older (black lines) adults. The grey zone represents±1 SD for the older adults. B–Full Width Half Maximum (FWHM) of the 14 lower-limb muscles at each walking condition. The bars represent the grand mean of all the young (grey) and the older (black) adults. Thin lines represent one standard deviation. The * indicates a significant effect of age.

Fig 4

Spatiotemporal spinal motor outputs computed from normalized EMGs (A) and average full width half maximum and mean activation of the lumbar (top) and sacral (bottom) segments (B) during forward and backward walking. For each individual, EMG signals from each muscle were normalized to unit variance across all trials [60]. The bars represent the grand mean of all the young (grey) and the older (black) adults. Thin lines represent one standard deviation. The * indicates a significant effect of age.