Visuomotor Entrainment and the Frequency-Dependent Response of Walking Balance to Perturbations

Abstract

Visuomotor entrainment, or the synchronization of motor responses to visual stimuli, is a naturally emergent phenomenon in human standing. Our purpose was to investigate the prevalence and resolution of visuomotor entrainment in walking and the frequency-dependent response of walking balance to perturbations. We used a virtual reality environment to manipulate optical flow in ten healthy young adults during treadmill walking. A motion capture system recorded trunk, sacrum, and heel marker trajectories during a series of 3-min conditions in which we perturbed a virtual hallway mediolaterally with systematic changes in the driving frequencies of perceived motion. We quantified visuomotor entrainment using spectral analyses and changes in balance control using trunk sway, gait variability, and detrended fluctuation analyses (DFA). ML kinematics were highly sensitive to visual perturbations, and instinctively synchronized (i.e., entrained) to a broad range of driving frequencies of perceived ML motion. However, the influence of visual perturbations on metrics of walking balance was frequency-dependent and governed by their proximity to stride frequency. Specifically, we found that a driving frequency nearest to subjects' average stride frequency uniquely compromised trunk sway, gait variability, and step-to-step correlations. We conclude that visuomotor entrainment is a robust and naturally emerging phenomenon during human walking, involving coordinated and frequency-dependent adjustments in trunk sway and foot placement to maintain balance at the whole-body level. These findings provide mechanistic insight into how the visuomotor control of walking balance is disrupted by visual perturbations and important reference values for the emergence of balance deficits due to age, injury, or disease.

Can optical flow perturbations detect walking balance impairment in people with multiple sclerosis?

“…Indeed, individuals may normally prefer to walk more slowly to accommodate balance perturbations. Additionally, we chose constant perturbation frequencies of 0.125, 0.25 and 0.442 Hz to be consistent with optical flow perturbations that altered gait variability in prior studies [17], but entrainment to perturbation frequency is affected by the participant's stride frequency, which varies between participants [54]. Future work should investigate how differences in stride frequency affect susceptibility to optical flow perturbations.…”

Neuroimaging of Human Balance Control: A Systematic Review

“…Walking balance control is especially dynamic, involving coordinated adjustments in posture (i.e., head and trunk stabilization) and foot placement from step to step (Bauby and Kuo, 2000; Kay and Warren, 2001; Donelan et al, 2004; Rankin et al, 2014). Particularly in unpredictable and challenging environmental conditions, these adjustments depend on the integration of reliable sensory feedback and the planning and execution of appropriate motor responses (O'Connor and Kuo, 2009; O'Connor et al, 2012; Francis et al, 2015; Franz et al, 2015, 2016; Goodworth et al, 2015). Accordingly, sensory and mechanical perturbations are increasingly used to study corrective motor responses in standing and walking and the onset and progression of balance deficits.…”

“…Accordingly, sensory and mechanical perturbations are increasingly used to study corrective motor responses in standing and walking and the onset and progression of balance deficits. Sensory perturbations may include those of visual (e.g., optical flow) (O'Connor and Kuo, 2009; O'Connor et al, 2012; Francis et al, 2015; Franz et al, 2015, 2016), somatosensory (e.g., tendon vibration) (Gurfinkel et al, 1976; Hay et al, 1996; Bove et al, 2003; Mullie and Duclos, 2014), or vestibular feedback (e.g., galvanic stimulation) (Day et al, 1993; Fitzpatrick et al, 1994; Bent et al, 2002; Dakin et al, 2007; Dalton et al, 2014), whereas mechanical perturbations most frequently incorporate support surface translations (Sinitksi et al, 2012; Aprigliano et al, 2016). Cortical activity and high-order cognitive processes are highly involved in the planning and execution of these motor responses.…”

Postural Stability When Walking and Exposed to Mediolateral Oscillatory Motion: Effect of Oscillation Waveform

“…Studies of perturbed walking have identified perturbation-induced changes in specific measures of walking stability. Trunk sway and gait variability measures of mediolateral kinematics while walking have been found to be frequency-dependent and sensitive to visual stimuli 21 . Foot placement as quantified by step width and step length variability and variability in postural sway were greater during perturbation than during normal walking 21 .…”

“…Trunk sway and gait variability measures of mediolateral kinematics while walking have been found to be frequency-dependent and sensitive to visual stimuli 21 . Foot placement as quantified by step width and step length variability and variability in postural sway were greater during perturbation than during normal walking 21 . The 'margin of stability' as a metric to identify postural stability has been defined as the distance between a velocity adjusted or 'extrapolated' position of the COM (center of mass) and the edge of an individual's BOS (base of support) at any given instant in time 22 .…”