Elsevier

Gait & Posture

Volume 33, Issue 2, February 2011, Pages 227-232
Gait & Posture

Old age affects gaze and postural coordination

https://doi.org/10.1016/j.gaitpost.2010.11.010Get rights and content

Abstract

Visual tracking of the surrounding environment is an important daily task, often executed simultaneously with the regulation of upright balance. Visual and postural coordination may be affected by aging which is associated with a decline in sensory and motor functions. The aim of the present study was to assess the effects of aging on the control of saccadic and smooth pursuit eye movements when standing on a moving surface. Nineteen young and 12 elderly subjects tracked a visual target presented as unpredictable smooth pursuit or saccadic displacements. Subjects were instructed to maintain gaze on target during quiet stance with or without yaw surface rotations. Elderly subjects followed both saccadic and pursuit targets with less accuracy than young subjects. Moreover, elderly subjects responded with longer time lags during saccadic target shifts and executed more catch-up saccades during smooth pursuits than younger subjects. Standing on a moving surface induced larger target-gaze errors. Catch-up saccades during pursuit occurred more frequently during surface perturbations. Our results suggest that visual tracking abilities decline with age and that postural challenge affects accuracy but not timing of gaze responses. Such declines observed with aging may result from multiple but minor sensory and motor deficits.

Introduction

Vision is an interface providing the central nervous system with important information on the environment (e.g., obstacle, slope, slippery floor). Both saccadic and smooth pursuit eye movements enable us to track objects in our environment. Saccadic eye movements are very fast motions shifting the fovea on a target. Slowly moving targets (<100°/s) are maintained on the fovea by smooth pursuit eye movements. While eye movements induced by smooth pursuit have shown to increase postural sway in young subjects [1], little is known on how gaze and posture interact in older adults. Sensorimotor integration for the control of posture has been studied and modeled in young healthy subjects [2], [3], [4], [5] and there is emerging evidence that multisensory integration for postural control is affected by aging.

The onset latency for saccadic eye movement is known to be longer in older adults than in younger subjects [6], [7], [8], [9], [10], [11], [12], [13], [14], [15], [16], [17]. In addition, older adults execute more saccades to reach a target [12], [17], [18], [19]. Pursuit eye movements are also altered with aging. For the eye to follow a slowly moving target accurately, both target and eye must move with the same velocity, at a gain equal to one. Reduced gain (lower eye pursuit accuracy) has been reported in older adults [12], [15], [20], [21]. When the eye diverts from target during pursuit, catch-up saccades are executed to reposition the eye on target. In elderly subjects, the number of catch-up saccades executed during pursuit is larger [20], [21]. In addition, the onset latency of pursuit eye movements is delayed in older adults [21], [22].

Unfortunately, these effects of aging on eye movements were only assessed during sitting. It is unclear whether oculomotor control deficits in older age are further impaired during balance or even locomotion. In fact, it is during walking or postural transitions (e.g., getting up, turning around) that most falls occur in persons aged 65 years and older [23]. Such challenges to balance are encountered on a daily basis from internal (e.g., bending over, quickly raising the arm to reach an object) and external disturbances (e.g., pushed by a closing door, riding the bus). In a previous study, we have shown that the saccadic latency of young healthy subjects is modulated when a yaw surface rotation is presented in temporal proximity to a visual target [24]. Currently, it is unknown whether gaze control in older adults is affected during quiet or perturbed stance. Thus, there is a need to determine whether gaze control is affected by aging when eye tracking movements are executed during upright stance and when balance is challenged.

The objective of this study was to determine the effects of aging on the accuracy and timing of saccadic and pursuit target tracking, when upright posture is perturbed with axial rotations of the support surface. We hypothesize that maintaining the eye on target will be more challenging for elderly subjects, as compared to healthy young subjects. Specifically, we expect to find increased gaze tracking errors and more corrective responses in the elderly group.

Section snippets

Subjects

Nineteen healthy young (8 males, mean age: 26 years, range: 18–35) and 12 healthy elderly subjects (4 males, mean age: 76 years, range: 70–81) without history of neurological disease or ophthalmologic conditions that could contribute to movement dysfunction participated in this study. All subjects gave their informed consent in accordance to the CRIR Research Ethics Board regulations and the Helsinki Declaration, prior to their participation in the study.

Experimental setup and protocol

Subjects were required to track a visual

Visual stimuli

Visual stimuli were programmed using the EyeLink Software Development Kit (version 2.1 GDI). Both saccade and smooth pursuit modes had a maximum target amplitude of 35° in each direction (Fig. 1C). Target position was pseudo-randomized to maintain the upcoming position unpredictable. Smooth pursuit target position was determined by combining position segments with the following parameters selected randomly: duration (0.5–1.5 s), target direction (left or right), and velocity (0–25°/s). For

Surface motions

Platform motions consisted of a computer-controlled sequence of ramp functions delivered pseudo-randomly, depending on the current surface position (16° right or left in center position: 16° or 32° in opposite direction when rotated right or left; see example trace Fig. 1C). The surface yaws were separated by pause periods varying between 0.5 s and 1.5 s.

Age differences in saccadic eye movements

All subjects, elderly and young, successfully followed the visual target while maintaining balance without falling or taking a step. In fact, whole-body movement excursions between groups were very similar (difference in head excursion between elderly and young 2.4 ± 1.4°, F(1,25) = 2.040, p = 0.17). As depicted in Fig. 2A, tracking errors in saccade mode, measured from the average RMS of the target-gaze errors were significantly larger in elderly than in young subjects (elderly 15.8 ± 0.8° vs. young

Discussion

This is the first study to assess gaze control accuracy in older adults during standing. In this distinctive protocol, we studied gaze accuracy during both quiet and perturbed stance. Although older adults can successfully track targets in standing, they are less efficient than young adults, and their tracking errors become significantly larger with surface perturbations, thus supporting our hypothesis that simultaneous regulation of gaze and balance proves challenging for older adults.

With our

Acknowledgements

We thank Valeri Goussev for his contribution to data analysis; Cynthia Thompson, Nancy St-Onge, Nicoleta Bugnariu, and Elizabeth Dannenbaum for their assistance in data collection; as well as Angie Ip for her help with the figures. This project was funded by the Canadian Institutes of Health Research (CIHR) and the Canada Foundation for Innovation. C. Paquette was supported by studentships from CIHR-JRH, Québec research funding agencies (FCAR-FRSQ-santé/REPAR) and a studentship from the McGill

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    Present address: Neuroplasticity Laboratory, Department of Neurology & Neurosurgery, McGill University at SMBD-Jewish General Hospital & Lady Davis Institute, Montreal, Quebec, Canada.

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