Increasing cognitive load attenuates right arm swing in healthy human walking

Abstract

Human arm swing looks and feels highly automated, yet it is increasingly apparent that higher centres, including the cortex, are involved in many aspects of locomotor control. The addition of a cognitive task increases arm swing asymmetry during walking, but the characteristics and mechanism of this asymmetry are unclear. We hypothesized that this effect is lateralized and a Stroop word-colour naming task-primarily involving left hemisphere structures-would reduce right arm swing only. We recorded gait in 83 healthy subjects aged 18-80 walking normally on a treadmill and while performing a congruent and incongruent Stroop task. The primary measure of arm swing asymmetry-an index based on both three-dimensional wrist trajectories in which positive values indicate proportionally smaller movements on the right-increased significantly under dual-task conditions in those aged 40-59 and further still in the over-60s, driven by reduced right arm flexion. Right arm swing attenuation appears to be the norm in humans performing a locomotor-cognitive dual-task, confirming a prominent role of the brain in locomotor behaviour. Women under 60 are surprisingly resistant to this effect, revealing unexpected gender differences atop the hierarchical chain of locomotor control.

Keywords: arm swing; central pattern generator; cognitive control; dual-task; gender; motor control.

Figures

Figure 1.

Experimental set-up. For the normal walking condition (a), subjects walked on an instrumented treadmill while fixating a black cross. They then performed two Stroop colour-naming task (see Material and methods) of differing difficulty. Image (b) shows the simpler task in which word and colour stimuli are congruent. In the more difficult, incongruent task (c) word and colour are discordant.

Figure 2.

Performance in congruent and incongruent Stroop tasks; (a) males, (b) females. Relative frequency of Stroop trial error rate trichotomized into no errors, one to five errors or more than five errors. (c) Correlation (Spearman's ρ) between arm swing asymmetry index and error rate during the incongruent Stroop task.

Figure 3.

Arm swing asymmetry under increasing cognitive load. Wrist trajectory asymmetry index is calculated using the left and right three-dimensional wrist centre trajectories, with left dominance resulting in a positive value and vice versa. ASI is given as the mean value per gait cycle over a trial of 45 s (approx. 42 gait cycles at 4 km h−1). s.e.m., Standard error of the mean. Statistical significance was determined using a linear mixed model with post hoc t-tests. The p-values are corrected for multiple pairwise within-age group comparisons using the Bonferroni method.

Figure 4.

Absolute wrist trajectory length. Three-dimensional wrist joint centre trajectories for younger, middle-aged and older adults during normal walking and during a congruent and an incongruent Stroop dual-task. GC, gait cycle. Error bars indicate 1 s.e.m. Statistical significance was determined using a linear mixed model with post hoc t-tests. The p-values are corrected for multiple pairwise within-age group comparisons using the Bonferroni method.

Figure 5.

(a) Sagittal gait cycle mean joint angle maxima and minima based on the approach used by Roggendorf et al. [25]. (b) Sagittal shoulder angle changes during normal walking and under increased cognitive load (incongruent Stroop task) in older adults walking on a treadmill. Diagrams represent the right (green) and left (red) mean sagittal shoulder angle maxima and minima (thick lines) per gait cycle with associated single standard deviations (thin dark lines). A significant decrease in shoulder flexion in the incongruent Stroop task is indicated by asterisk (*). Elbow flexion was also reduced under increased cognitive load, with preserved extension (not shown; see Results section).

Figure 6.

Arm swing asymmetry under increasing cognitive load—gender effects. Wrist trajectory asymmetry index is calculated using the left and right three-dimensional wrist centre trajectories, with left dominance resulting in a positive value and vice versa. ASI is given as the mean value per gait cycle over a trial of 45 s (approx. 42 gait cycles at 4 km h−1), s.e.m.; standard error of the mean. Statistical significance was determined using a linear mixed model with post hoc t-tests. The p-values are corrected for pairwise within-group comparisons using the Bonferroni method.