Old age affects gaze and postural coordination
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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2023, Human Movement ScienceCitation Excerpt :Therefore, the more variable head movement does not seem to be the reason for the increased CoP range noted in the smooth pursuit task compared to fixation and thus appears not to hamper balance control. This might be related to the fact that target motion was relatively slow (≅ 15o/s) compared to previous studies (> 20o/s; e.g., Paquette & Fung, 2011; Maruta et al., 2017), and so the induced head rotation during the smooth pursuit task in our study might have been relatively slow, minimizing inertial influences that could compromise postural stability. Our study reveals, for the first time, that when the head is unrestrained during the performance of visual tasks, gaze smooth pursuit of a horizontally moving target increases CoP sway to a greater extent in older than young individuals.
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2020, Neuroscience LettersCitation Excerpt :In recent years, advances in gaze-tracking technology (e.g., head-mounted eye trackers, head free eye trackers) have enabled the growth of studies recording eye movements during a variety of motor actions [5,12]. Using eye tracker devices in postural protocols as a methodological tool has allowed, for instance, better understanding of the vision-posture relationship [5,13,14]. Specifically, analyses from eye movements directed to a visual target have aimed to examine the way the eyes behave while the subject is actually performing the required visual task (e.g., saccadic eye movements) and how this gaze behavior is related to postural stabilization in a variety of postural challenges; prior to the development of such technologies, visual task performance was subjectively checked by experimenter’s observation or video recording.
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2023, Experimental Brain Research
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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.