Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging

Abstract

Natural aging entails progressive deterioration in a variety of biological systems. This study focuses on visual and vestibular influences on human eye movements as a function of aging. Eye movements were recorded (search-coil technique) during visual, vestibular, and combined stimuli in subjects across a broad range of ages (18–89 years). Two types of visual following were assessed: smooth pursuit (SP) of a small discrete target, and optokinetic (OKR) following of a large-field striped image. The vestibulo-ocular reflex (VOR) was studied during head rotation in darkness. Visualvestibular interactions were recorded during rotation in two ways: when the optokinetic scene was earth-fixed, resulting in visual enhancement of the VOR (VVOR), and when the visual image was head-fixed, allowing visual suppression of the VOR (VSVOR). Stimuli consisted of horizontal sinusoidal oscillations over the frequency range 0.025–4 Hz. Trials were analyzed to yield response gain (peak horizontal eye/stimulus velocities) and phase (asynchrony, in degrees, between eye and stimulus velocity signals). VOR gain in young subjects was greatest (near 0.9) at 2.5–4 Hz but declined steadily with decreasing frequency, while phase hovered near zero until 0.1 Hz and then developed a progressively increasing lead. Effects of advancing age were small, given the modest head velocities presented, and were most noticeable as an increase in phase lead and decline in gain at the lowest frequencies (≤0.1 Hz). The two forms of visual following and all conditions of visual-vestibular interactions displayed more prominent age-dependent changes. OKR and SP response characteristics (0.25–4 Hz) closely resembled each other. Gain was greatest at 0.25 Hz, while phase was near 0°. As frequency increased, gain declined while phase lag rose. However, both gain and phase lag tended to be slightly greater for OKR than for SP responses. Both SP and OKR response properties deteriorated progressively with increasing age, as witnessed by a progressive decline in gain and increase in phase lag, even at modest frequencies (e.g., 0.25–1.0 Hz). VVOR responses were generally closer to the ideal of 1.0 in gain and 0° in phase than either the VOR or visual following alone. A subtle but significant age-dependent decline in VVOR performance occurred at the lowest frequencies. VSVOR response characteristics were close to those of the VOR and VVOR at 4 Hz, where visual influences on eye movements are generally inconsequential. As frequency declined, visual suppression became more robust and gain dropped. The SP stimulus seemed surprisingly more effective than the OK scene in suppressing the VOR, but this effect is predicted by a linear model of visual-vestibular interactions. As age increased, visual influences on the VOR became progressively weaker, in concert with deterioration of visual following. The subjective sensation of circular vection (CV), a psychophysical measure of VVI, was assessed during optokinetic stimulation at 0.025 Hz. Interestingly, the likelihood and intensity of CV increased with aging, suggesting that visual inputs to the perception of self-motion are enhanced in the elderly. This may represent a form of visual compensation for age-dependent loss of vestibular self-rotation cues. In brief, the VOR, visual following, and their interactions display specific changes in response properties as a function of natural aging. The modifications may be interpreted as age-dependent deteriorations in the performance of systems underlying the control of human eye movements.