Age-related changes in head-to-foot proprioception do not influence vestibular-evoked balance response direction

Introduction: As the vestibular system is fixed within the skull, its afferent signal must be transformed from head- to body-centred coordinates to serve whole-body postural control. This coordinate transformation process explains why, in response to identical vestibular input, the direction of the evoked balance response depends on the orientation of the head relative to the rest of the body (Lund & Broberg, 1983; Mian & Day, 2009). Our sense of head-to-body position is derived from other sources, including proprioception. This raises the possibility that, if proprioceptive abilities decline in older adults, the vestibular coordinate transformation process may also be impaired. We therefore aimed to investigate whether head-to-foot proprioception is affected by ageing and, if so, whether this has any bearing on the accuracy and/or precision of balance responses to electrical vestibular stimulation (EVS).Methods: Head-to-foot proprioception and EVS-evoked response direction were assessed in the same group of 62 participants ranging from participants ranging from 20 to 87 years (mean ± 1SD = 56.5 ± 20.1 yrs). To assess head-to-foot proprioception, participants stood upright with eyes closed while the right foot was passively rotated to one of seven angles of external rotation between 0-60°. Participants were then required to actively rotate their head to match the static horizontal angle of the foot. To assess the EVS-evoked response direction, standing participants adopted one of five angles of horizontal head-to-foot rotation between -60-60° before closing their eyes. Stochastic EVS (0-20 Hz, 0.6 mA RMS) was then applied via the mastoid processes while simultaneously recording ground reaction forces, and a previously validated technique was used to determine response direction (Mian & Day, 2009).Results: Mean signed error (i.e., bias) in the proprioceptive estimate of the head relative to the foot across all trials was -2 ± 9° and did not significantly change with age (r = 0.013, p = 0.921). There were, however, age-related increases in mean absolute error (r = 0.324, p = 0.010) and angular deviation (r = 0.331, p = 0.009), which indicate reduced accuracy and precision, respectively. The EVS-evoked response direction was, on average, -1 ± 5° from the theoretically predicted interaural response direction. Age was not associated with changes in response direction bias (r = 0.131, p = 0.310) or accuracy (r = -0.110, p = 0.394), and angular deviation was reduced, indicating improved precision (r = -0.370, p = 0.003). Furthermore, there were no significant correlations between proprioceptive and response direction measures (all p ≥ 0.109).Conclusions: Despite providing evidence for age-related proprioceptive decline, our results suggest that this does not influence the accuracy or precision of vestibular-evoked balance responses. It appears that the subconscious coordinate transformation of the vestibular afferent signal for balance is not impaired with age and is unrelated to the conscious perception of head orientation that was measured in the current study.Acknowledgements: This work was funded by the UK Biotechnology and Biological Sciences Research Council (BB/I00579X/1 and an Industry Interchange Award) and UK Medical Research Council (MR/X013944/1).