Head motion predictability explains activity-dependent suppression of vestibular balance control

Abstract

Vestibular balance control is dynamically weighted during locomotion. this might result from a selective suppression of vestibular inputs in favor of a feed-forward balance regulation based on locomotor efference copies. The feasibility of such a feed-forward mechanism should however critically depend on the predictability of head movements (HMP) during locomotion. To test this, we studied in 10 healthy subjects the differential impact of a stochastic vestibular stimulation (SVS) on body sway (center-of-pressure, COP) during standing and walking at different speeds and compared it to activity-dependent changes in HMp. SVS-cop coupling was determined by correlation analysis in frequency and time domains. HMP was quantified as the proportion of head motion variance that can be explained by the average head trajectory across the locomotor cycle. SVS-COP coupling decreased from standing to walking and further dropped with faster locomotion. Correspondingly, HMP increased with faster locomotion. Furthermore, SVS-COP coupling depended on the gait-cycle-phase with peaks corresponding to periods of least HMP. These findings support the assumption that during stereotyped human self-motion, locomotor efference copies selectively replace vestibular cues, similar to what was previously observed in animal models.The vestibular system encodes head orientation and motion to facilitate balance reflexes that ensure postural equilibrium during passive as well as self-initiated movements 1 . During locomotion, i.e., stereotyped self-motion, vestibular influences on balance control appear to be dynamically up-or down-regulated in dependence on the phase and speed of the locomotor pattern. Accordingly, vestibulospinal reflexes exhibit phasic modulations across the locomotor cycle 2,3 with the result that balance is particularly sensitive to vestibular perturbations at specific phases of the gait cycle 4 . Furthermore, vestibular influences appear to be down-weighted during faster locomotion. Accordingly, the destabilizing impact of a vestibular loss or perturbation on the gait pattern decreases with increasing locomotion speeds 5-9 .It was previously assumed that activity-dependent modulations of vestibular balance reflexes might reflect an up-or down-regulation of a concurrent intrinsic feed-forward control of posture 10-13 . Accordingly, balance adjustments during self-motion might not solely rely on sensory feedback about how the body has moved, but also on predictions of resultant movements derived from efference copies of the motor command 14 . Physiological evidence for such a direct feed-forward control mode has recently been shown for animal locomotion. During Xenopus laevis tadpole swimming, intrinsic efference copies of the locomotor command deriving from spinal central pattern generators (CPG) were shown to directly trigger ocular adjustments for gaze stabilization and selectively cancel out any afferent (ex-and reafferent) vestibular inputs 10,15 . Thus, also during human stereotyped locomotion, efference copies might pro...

Quantitative Evaluation of a New Posturo-Locomotor Phenotype in a Rodent Model of Acute Unilateral Vestibulopathy

“…If vestibular patients do not run, it is because they consider that their condition probably does not allow them to; it is an avoidance strategy. Indeed, the vestibular contribution to gait variability, which is a predictive marker for falls, declines with faster walking and running (41). Therefore, their balance would be better when running because dynamic balance strategies are different at low and high speeds (41)(42)(43)(44)(45).…”

Bilateral vestibulopathy: beyond imbalance and oscillopsia

“…After all, a higher walking speed can increase stability due to automatic locomotor patterns by spinal cord mechanisms. However, BV patients still report paying more attention to walking, since they lack the fast vestibular mediated reflexes that can prevent them from falling (increasing risk for falls), e.g., when walking on uneven ground or when tripping [51][52][53][54]. This demonstrates that dual tasking can be impaired.…”

Absence of Nonlinear Coupling Between Electric Vestibular Stimulation and Evoked Forces During Standing Balance

“…In recent years, it has become more common to use bandwidth limited white noise stimuli to probe the contribution of the vestibular system to motor control ( Dakin et al, 2007 ; Mian and Day, 2009 ; Mackenzie and Reynolds, 2018 ; Tisserand et al, 2018 ; Dietrich et al, 2020 ). Often these studies assume a linear relationship between the frequencies in the input stimulus and those in the response.…”

“…Recently, the use of random waveform electrical vestibular stimuli, rather than the traditional step or square-wave, has become more common. These stimuli have been used to induce stochastic resonance-like effects at low amplitudes ( Mulavara et al, 2011 ), to model the postural instability that occurs following space flight ( MacDougall et al, 2006 ; Moore et al, 2006 ), and for their utility as a vestibular probe ( Dakin et al, 2007 ; Blouin et al, 2011 ; Reynolds, 2011 ; Dietrich et al, 2020 ; For review see Forbes et al, 2015 ). For this latter use, researchers often employ analysis methods that assume the stimulus’ influence on the body has a linear (one-to-one) relationship to stimulus frequencies.…”