Research articleSemi tandem base of support degrades both saccadic gaze control and postural stability particularly in older adults
Introduction
Gaze behavior affects postural stabilization. The magnitude of body sway of young adults is attenuated during continuous saccadic eye movements compared with fixation directed to a target [[1], [2], [3], [4], [5]]. During eye movement tasks, the central nervous system uses additional sensory information from extraocular muscles (efferent perception mechanism) and optical flow characteristics (afferent perception mechanism) to estimate the body position in space, increasing postural stability [6]. A more stable visual scene due to this decreased body sway facilitates more accurate gaze shifts, indicating functional integration of posture and gaze control [2].
Some studies have manipulated bases of support challenges and characteristics of saccadic tasks to examine the posture-gaze relation in young and older adults and have indicated that changes in postural demands may interact with visual task constraints altering the way the posture and gaze control are integrated [5,7]. Rodrigues et al. [5]. examined the effect of different frequencies of horizontal saccades (1.1 Hz and 0.5 Hz) on body sway of young adults during different bases of support demands (wide and narrow stances). Results have shown additional attenuation of trunk sway and head movements in wide stance during the high saccadic frequency condition indicating that the postural control was modulated to facilitate rapid and accurate gaze shifts to the target but only on a less demanding base of support. The authors suggested an adaptive resource-sharing interpretation for these results which states that limited attentional resources are shared according to the demands of each task (i.e. postural and suprapostural tasks) [8].
This interplay between postural demands and saccadic task constraints should be considered when examining the effects of eye movements on postural stabilization of older individuals. It is known that postural control is affected by the aging process [9]; older adults present sensory and motor deficits which lead to increased postural instability, mainly during challenging stances [10]. In addition, there are declines in gaze performance; for instance, older adults present longer latencies of voluntary vertical and horizontal saccades to visual targets compared to young adults [11,12]. However, little is known about how these aspects interfere with the postural stabilization of older adults during the performance of saccades.
Aguiar et al. [13], examining the effects of frequency of saccades and bases of support demands in older adults, pointed out that older adults did not show reduced body sway in wide stance during the performance of the more demanding visual task (1.1 Hz), as previously found in young adults [5]. In fact, older adults seem to be more affected by visual task demands since their sway magnitude was not increased in narrow stance (more demanding base of support) compared with wide stance. This suggests that older adults likely adopted a more rigid postural response strategy (i.e. stiffened posture) in narrow stance to stabilize posture in order to facilitate gaze shifts. However, without gaze position measures, it is unclear if older adults successfully achieved gaze performance. Thomas et al. [14], conversely, did not demonstrate the effect of saccades on the postural sway and gaze performance of both young and older females, in narrow stance, through measures of center of pressure displacement (CoP). These results did not corroborate the previous studies [4,5,13] in two respects: reduction in postural sway due to saccades during narrow base of support and effect of aging on gaze performance. The authors suggested that long periods of fixation on the target due to lower saccadic frequency (0.3 Hz) stabilized the sway magnitude, not requiring further postural attenuation. Older adults demonstrated similar gaze errors during the saccadic task compared to young adults.
Despite the contribution of these studies, lack of systematic control over the demands of visual and postural tasks means that there is not yet clarification as to whether greater postural instability affects gaze performance during a more demanding visual task and, in this case, whether there is an interaction between the saccadic task demands and stance difficulty.
In the present study, we examined whether the effects of saccadic eye movements on postural performance might be related to changes in saccadic direction and bases of support demands. Vertical and horizontal saccades, at high saccadic frequency (1.1 Hz), are thought to challenge eye movements in different movement axes. It is known that latency of vertical saccades increases with age [15] and is longer than horizontal saccades [11]. Performing vertical saccades might potentially generate higher attentional demands compared to horizontal saccades, differently influencing postural stability. There is no consensus in the literature regarding the effect of horizontal and vertical saccades on postural sway in different body movement axes (anterior posterior - AP and medial lateral - ML). However, some studies have indicated that changes in postural sway may occur in one specific movement axis depending on the demands of postural and visual tasks [1,2,7,14]. Thus, we examined whether greater mechanical postural instability in the ML axis would affect gaze performance in horizontal and vertical saccadic directions. Body sway and gaze displacement were measured to examine how both systems (balance and oculomotor) deal with the interactions between postural and visual tasks. In addition, we used measures of postural sway based on analysis of both CoP and head displacement in order to provide a more complete description regardingthe effects of saccades on postural stabilization of older adults.
The aim of this study was to investigate the effects of saccadic eye movements in horizontal and vertical gaze directions on the postural control of young and older adults during different bases of support and also to examine whether gaze behavior is affected by demands of both postural and visual tasks. In this context, this is the first study to quantify the effects of eye movement on postural control of older adults in different saccadic directions and base of support demands relating measurements of gaze behavior and balance control. Our hypotheses were: 1) The attenuation effect of horizontal and vertical saccades on sway magnitude would be higher during the semi tandem base of support condition compared to the feet apart base condition. We also expected that standing in semi tandem base, ML sway magnitude would be attenuated by horizontal saccades and AP sway magnitude would be attenuated by vertical saccades; 2) Older individuals would demonstrate decreased performance of saccades (increased gaze latency mean and variability) compared to young adults in horizontal and vertical directions, which would be more pronounced during the semi tandem base of support condition.
Section snippets
Participants
Ten healthy older adults (71.6, ± 3.1years-old) and ten young adults (20.7, ± 3.4years-old) participated in the study. The participants did not report diagnosed neurological diseases, musculoskeletal disorders, or visual impairments which could compromise performance of the experimental conditions. All participants presented normal or corrected to normal vision by glasses or contact lenses. A written consent was signed by the participants. The experimental procedures were approved by the local
CoP displacement
The group by base of support interaction was significant for mean velocity (ML) and mean amplitude (ML) (Table 1); post hoc tests indicated that only in the semi tandem condition, older adults showed higher values for mean velocity (p < 0.001) and mean amplitude (p < 0.002) in the ML axis compared to young adults.
Head displacement
There was a significant group by base of support interaction (Table 2) and the post hoc analysis revealed, on the semi tandem base, higher mean velocity (AP – p < 0.002 and ML -
Discussion
The present study aimed to investigate the effects of horizontal and vertical saccades on postural stabilization of young and older adults during different bases of support and to examine how gaze performance is affected by postural and visual task demands. Our results revealed that challenging stance condition degraded postural stability, increasing head displacement during the saccadic tasks compared to fixation task. This greater postural instability modified the way the eyes moved toward
Conclusion
The results of the present study contribute to our understanding of the gaze-posture relationship, demonstrating that greater demands for the postural control system from challenging bases of support interfere in how the eyes are controlled during saccadic eye movements. Moreover, the results indicate that the known decline in the postural control system with aging (i.e. greater postural instability) does not seem to affect the accomplishment of saccadic visual tasks in older adults but
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Post-graduation Program in Movement Sciences, São Paulo State University - UNESP.
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