Senescence of human visual-vestibular interactions. 1. Vestibulo-ocular reflex and adaptive plasticity with aging

Abstract

The human horizontal vestibulo-ocular reflex (VOR) was studied as a function of aging (18 to 89 years) over a broad range of frequencies (0.025 to 4 Hz) and peak velocities (50 degrees to 300 degrees/s) of angular head movement. Eye movements were recorded using the search-coil technique. High stimulus frequencies and amplitudes were employed in order to challenge the VOR sufficiently to enhance potential age-related deficits in its pathways and functions. Further, the possibility that adaptive plastic mechanisms, which normally restore failing VOR function, might themselves deteriorate with aging was tested. Subjects were studied before and after an 8-h period while wearing 2 x binocular magnifying lenses. Demonstrable differences were observed in the human VOR as a function of natural aging. These differences were most pronounced in phase measures (increasing lead with aging), both at low frequency and low head velocity, and at modest frequency but high head velocity. Gain decrements were also observed with aging, but the changes were more subtle. The modifications in the VOR may be interpreted as an age-dependent deterioration in VOR performance. The course of age-related changes in response characteristics, particularly phase lead at the highest stimulus amplitude, are similar to age-related anatomical deterioration reported in peripheral vestibular structures. These changes resemble those in young patients with vestibular lesions, and are consistent with the notion that aging entails a progressive bilateral peripheral vestibular loss. Adaptive plastic mechanisms, which normally maintain VOR performance when altered responses result in visual-vestibular mismatch during head rotation, also deteriorate with aging. Again, the phenomenon resembles that in younger but vestibulopathic individuals. The effect is most profound at high frequencies and head velocities commensurate with natural behavior.