Seeing Gravity: Gait Adaptations to Visual and Physical Inclines – A Virtual Reality Study

Abstract

Using advanced virtual reality technology, we demonstrate that exposure to virtual inclinations visually simulating inclined walking induces gait modulations in a manner consistent with expected gravitational forces (i.e., acting upon a free body), suggesting vision-based perception of gravity. The force of gravity critically impacts the regulation of our movements. However, how humans perceive and incorporate gravity into locomotion is not well understood. In this study, we introduce a novel paradigm for exposing humans to incongruent sensory information under conditions constrained by distinct gravitational effects, facilitating analysis of the consistency of human locomotion with expected gravitational forces. Young healthy adults walked under conditions of actual physical inclinations as well as virtual inclinations. We identify and describe 'braking' and 'exertion' effects-locomotor adaptations accommodating gravito-inertial forces associated with physical inclines. We show that purely visual cues (from virtual inclinations) induce consistent locomotor adaptations to counter expected gravitybased changes, consistent with indirect prediction mechanisms. Specifically, downhill visual cues activate the braking effect in anticipation of a gravitational boost, whereas uphill visual cues promote an exertion effect in anticipation of gravitational deceleration. Although participants initially rely upon vision to accommodate environmental changes, a sensory reweighting mechanism gradually reprioritizes body-based cues over visual ones. A high-level neural model outlines a putative pathway subserving the observed effects. Our findings may be pivotal in designing virtual reality-based paradigms for understanding perception and action in complex environments with potential translational benefits.

Patterns of whole-body muscle activations following vertical perturbations during standing and walking

“…We hypothesized that muscle activation patterns in response to vertical perturbations will differ from those in response to horizontal perturbations, because vertical perturbations generate unique challenges to equilibrium [6,13,21,27,28] (for a detailed rationale of a priori predictions and hypotheses, see Supplementary File #1). We further hypothesized that the role of vision would differ for vertical versus horizontal perturbations due to the critical role of vision in maintaining equilibrium [29][30][31], and because visual perturbations can signal gravitational changes as well as positional changes [32,33]. Specifically, since vertical visual scenes influence the apparent direction of gravity [33] and anteroposterior visual scenes act in advance of induced falls, we expect that visual conditions will modulate postural responses by adjusting the body against expected gravitational forces following vertical perturbations, and by activating muscles opposing a potential fall following horizontal perturbations.…”

“…We observed that magnitude of muscle activation, for instance, was progressive: smallest after visual perturbations, followed by (physical perturbations) dynamic-camera, static-camera, and finally, eyes-closed conditions that usually led to largest magnitudes. Visual sensory cues have been suggested to be suitable for balance-control regulation [59,60], and for locomotion modulation related to surface inclination changes [32]. Understanding the multisensory integration determining muscle activation patterns for postural control can have translational benefits for patients with sensory-integration dysfunctions, either to entrain compensations or to identify sources of sensory impairment.…”

Visuomotor Interactions and Perceptual Judgments in Virtual Reality Simulating Different Levels of Gravity

“…The evidence for motor actions is uncontroversial. Thus, it is well established that humans take gravity effects into account to control reaching movements optimally (Gaveau et al, 2011(Gaveau et al, , 2016, to guide locomotion on an inclined plane (Cano Porras et al, 2019), and to interact effectively with objects moving under Earth gravity (Zago et al, 2009;Lacquaniti et al, 2013). For instance, healthy participants easily intercept a target dropped vertically from above or rolling down an inclined plane, even with sparse visual information (e.g., Lee et al, 1983;Lacquaniti and Maioli, 1989a;Michaels et al, 2001;Zago et al, 2004;La Scaleia et al, 2014a).…”

Vision affects gait speed but not patterns of muscle activation during inclined walking – a virtual reality study

“…In order to maintain stability during bipedal locomotion, the muscle system continuously adapts to changing walking conditions via a complex motor process that relays on multisensory integration (Wall-Scheffler CM, Chumanov E and B, 2011) that involves whole body adaptations (Kimel-Naor et al, 2017;Cano Porras et al, 2020). Particularly, walking on inclined surfaces lead to significantly different patterns and magnitudes of activation in lower limb muscles, as compared to leveled walking.…”

“…Inclined walking involves adjustment to gravitational forces. The exertion effect (uphill walking) and the braking effect (downhill walking) have been previously described and quantified (Cano Porras et al, 2020). Briefly, during uphill walking, the exertion effect counteracts the gravitational deceleration and allows the walker to maintain roughly stable gait speed pace, which is lower than natural speed during leveled walking (Sun et al, 1996;Sinitski et al, 2015;Kimel-Naor et al, 2017).…”