Single exposure to optokinetic stimulation through virtual reality decreases reliance on visual inputs for posture control

Abstract

[Purpose] The potential of using optokinetic stimulation (OKS) in conjunction with virtual reality (VR) for balance training merits further investigation. We examined the effects of a single exposure to OKS through VR on the visual dependence of postural sway and control among healthy adults. [Participants and Methods] A two-minute virtual reality (OKS) task was performed by 30 healthy adults without balance impairment. The center of gravity was measured before and after completing the task in the standing position with the eyes open and closed to ascertain the Romberg ratio, which is a measure of visual dependence. [Results] The Romberg ratio of the VR + OKS group significantly decreased from before to after task completion. [Conclusion] The findings indicate that OKS applied with VR enhances visual dependence. These findings facilitate the future use of VR in postural control rehabilitation.

INTRODUCTION

The maintenance of postural control in the standing position is dependent on the integration of information from three primary sensory systems: the somatosensory/intrinsic, visual, and vestibular^{1, 2)}. Sensory integration enables the body to respond instantaneously and automatically to a multitude of challenges, including activation of the appropriate muscles through sensory-to-motor conversion, the maintenance of static balance under the influence of gravity, and resistance to imbalances. However, these three senses are not only integrated as individual modalities; indeed, they are continuously optimized to facilitate adaptive responses to environmental changes via a process known as sensory reweighting^{3, 4)}. As an illustrative example, when the environment transitions from a bright to a dark setting, visual data becomes unreliable for postural control. Consequently, greater reliance is placed on other highly accurate sensory inputs, such as somatosensory information. As the conditions shift, the senses dynamically reassign weighting to optimize postural control at all times^{2, 5)}. The key to inducing sensory reweighting is to reduce the reliability of incoming sensory information. Exposure to optokinetic stimulation (OKS) has also been demonstrated to increase postural sway in the direction of motion in healthy adults^{6, 7)}, which is thought to improve visual dependence in postural retention by reducing the reliability of visual information. Visual dependence on postural control is associated with several problems that can significantly affect balance and orientation. Individuals with visual dependence have increased postural sway and reduced postural control, particularly in complex visual environments⁸⁾. Visual dependence has a significant impact on postural control; however, OKS can effectively reduce this dependence. OKS induces sensory reweighting in the central nervous system, which adjusts the relative importance of different sensory inputs to maintaining balance⁹⁾. This process reduces the over-reliance on visual cues while improving the integration of vestibular and proprioceptive information. As a result, OKS exposure is a valuable tool in vestibular rehabilitation, particularly in patients with visual vertigo or balance disorders characterized by excessive visual dependence⁸⁾.

Akizuki et al. previously reported that the Romberg ratio decreased following repeated exposure to virtual reality (VR) images in which visual information was inaccurate in relation to head movements¹⁰⁾. The Romberg ratio (eyes closed/eyes open [EC/EO]) is a method used to indirectly assess visual dependence in posture control by comparing postural sway under the EO and EC conditions. This allows the degree of balanced deterioration in the absence of vision to be quantified compared with open-eye conditions¹¹⁾. The advent of VR technology has facilitated the use of cost-effective goggles and applications that permit the implementation of OKS in any setting. Consequently, the OKS can now be deployed in any location using inexpensive goggles and applications.

The extant literature on the effects of VR technology on visual dependence currently presents only inconclusive results. While some studies have reported that VR technology improves visual dependence¹²⁾, others have found no effect⁹⁾. As such, the effects of VR on visual dependence remain unclear, as does the impact of a single exposure to OKS with VR.

If studies can prove that participants’ visual dependence is readily amenable to improvement through the utilization of OKS in conjunction with VR, then the application of OKS for the purpose of balance training should become more prevalent. Accordingly, the present study examined the effects of a single exposure to OKS using VR on visual dependence in postural sway and postural control among healthy adults. The efficacy of the EO condition as a control and the EC condition as a method of visual deprivation was subsequently compared and examined, with a view to establishing its potential as a method to improve visual dependence.

PARTICIPANTS AND METHODS

This study enrolled 30 healthy adults [mean (SD); age: 21 (0.9) years; 10 women; height: 166.8 (6.6) cm] as participants. All patients who met the following conditions: no acute lower limb disorders, no motor system disorders, no neurological disorders affecting postural control, and no prior VR experience were selected to eliminate the potential confounding effects of VR familiarity on intervention outcomes. The study was conducted in accordance with the Declaration of Helsinki, and its purpose and content were explained to the participants in advance, after which written informed consent to participate was obtained. The research content and methodology were approved by the Ethical Review Committee of Biwako Rehabilitation Professional University (approval number: BR24011).

This study comprised a pre-measurement (Pre), a two-minute standing task conducted under each task (EO, EC, VR+OKS), and a post-measurement (Post). During the preliminary and subsequent measurements, each participant was instructed to maintain a static standing position for 30 seconds on two occasions, with open and closed eyes, using a balance function meter (Gate View, aison Ltd., Saitama, Japan). The participants were further instructed to assume a static standing posture with their feet and heels together and both upper limbs in a relaxed position, while barefoot. In the open eye condition, an index finger was placed 1 m from the participant at eye level, and the participant was instructed to stare at it.

In the VR+OKS condition, a smartphone (iPhone SE, Apple Inc., Cupertino, CA, USA) was attached to VR goggles for smartphones (VRG-M02RBK, ELECOM Inc., Osaka, Japan), with the participant’s eyes open. Additionally, a participantive visual vertical position application (SVV, Kuroda ENT. Clinic, Version 2.6) was used to maintain a closed leg standing posture with both legs, while a rotational optokinetic stimulus with a black dot rotating clockwise at 60°/s was applied for 2 minutes. There have been no reports of VR sickness from participants during or after the intervention. In the EO, participants were instructed to maintain a closed leg standing posture, while gazing at an index placed at eye level, 1 m away, for a period of 2 minutes. In the EC, participants were instructed to maintain the closed leg standing posture for a period of two minutes with their eyes closed, thus blocking visual information. Participants were instructed to perform each condition randomly, with sufficient rest periods between conditions. Following a two-minute period of standing in each condition, the Post measurement was taken using an equilibrium function meter in a manner consistent with that employed for the Pre.

To calculate the visual dependence of each participant from the data obtained by the equilibrium function meter, the Romberg ratio was further calculated by dividing the center of pressure (COP) sway value during the EC by that during the EO. The Romberg ratio A (Area: Romberg A) was further calculated from the measured outer circumferential area, which represents the magnitude of the center of gravity sway of the EO and EC. The Romberg ratio V (velocity: Romberg V) was also calculated from the unit time trajectory length, which represents the speed of the center of gravity sway during EC and EO.

In the statistical process, repeated-measures ANOVA (Bonferroni corrections) were performed on the outer circumferential area, unit time trajectory length, Romberg A, and Romberg V obtained before and after each task. Where a main effect was found as a result of repeated-measures ANOVA, multiple comparisons with Bonferroni correction were performed. Statistical software (IBM SPSS Statistics version 29.0, IBM, Armonk, NY, USA) was used to perform statistical analyses, with a significance level of <0.05 set in all cases.

RESULTS

No significant main effects were observed for the task outer circumferential area with eyes open (F (3, 87)=3.315, p>0.05, ηp²=0.103) or for the unit time trajectory length with eyes open (F(3, 87)=0.522, p>0.05, ηp²=0.017) (Figs. 1, 2).

Fig. 1.

Comparison of the outer circumferential area and unit time trajectory length before and after each condition task.

Before and after each condition task, a comparison of the outer circumferential area and unit time trajectory length. Data are presented as mean ± SD (n=30). OCA: outer circumferential area (cm²); UTL: unit time trajectory length (cm/s); EO: eyes open; EC: eyes close. *p<0.05, **p<0.01.

Fig. 2.

Comparison of the Romberg ratio before and after each condition task.

Before open and after each condition task, a comparison of the Romberg ratio. Data are presented as mean ± SD (n=30). EO: eyes open; EO: eyes close; *p<0.05, **p<0.01.

In contrast, a significant main effect was found for the outer circumferential area with eyes closed (F (3, 87)=47.387, p<0.01, ηp²=0.620). Post hoc analyses using Bonferroni correction revealed significant differences between the pre-task and VR+OKS conditions (p=0.0048, Cohen’s d=0.98), as well as between EO and VR+OKS (p=0.0424, Cohen’s d=0.79) and EC and VR+OKS (p=0.0232, Cohen’s d=0.79). However, no significant differences were observed between the pre-task and EO conditions (p>0.05) or between the pre-task and EC conditions (p>0.05).

Similarly, a significant main effect was observed for the unit time trajectory length with eyes closed (F (3, 87)=9.592, p<0.01, ηp²=0.249). Post hoc analyses indicated significant differences between the pre-task and VR+OKS conditions (p=0.000015, Cohen’s d=0.42), EO and VR+OKS (p=0.0164, Cohen’s d=0.72), and EC and VR+OKS (p=0.00012, Cohen’s d=0.96). However, no significant differences were found between the pre-task and EO conditions (p>0.05) or between the pre-task and EC conditions (p>0.05).

Furthermore, significant main effects were identified for both Romberg A (F (3, 87)=36.501, p<0.01, ηp²=0.557) and Romberg V (F(3, 87)=21.591, p<0.01, ηp²=0.427). Post hoc analyses revealed significant differences between the pre-task and VR+OKS conditions for both Romberg A (p=0.0011, Cohen’s d=0.96) and Romberg V (p=0.0091, Cohen’s d=1.01), as well as between EO and VR+OKS for Romberg A (p=0.0094, Cohen’s d=1.02) and Romberg V (p=0.0036, Cohen’s d=0.87), and between EC and VR+OKS for Romberg A (p=0.0115, Cohen’s d=0.7) and Romberg V (p=0.0043, Cohen’s d=0.5). However, no significant differences were observed between the pre-task and EO conditions or between the pre-task and EC conditions for either Romberg A or Romberg V (all p>0.05).

DISCUSSION

This study aimed to investigate the effects of a single exposure to OKS using VR, a method that could be easily applied in clinical practice, on visual dependence. Comparisons were made under open-eye (EO) and visual deprivation (EC) conditions, which could be used as a simple method to improve visual dependence. The results showed that the peripheral area and unit time trajectory length during eye closure and the Romberg ratio (Romberg A, Romberg V), an index of visual dependence, both decreased only in the VR+OKS condition. This is due to inaccuracies in the visual input information in OKS, which means that participants need to reduce their reliance on visual input and increase their reliance on somatosensory input, which provides more accurate feedback in postural sway, to maintain an upright posture. Following a single exposure to OKS with VR in the present study, the effect was related to the sensory modality weighting in healthy adults, which influenced a reduction in visual dependence.

OKS induces sensory reweighting, a process critical for optimizing postural control under changing environmental conditions^{8, 9)}. This phenomenon occurs by reducing the reliability of visual information, thereby necessitating a shift in sensory weighting⁸⁾. When exposed to OKS, healthy adults showed increased postural sway to their visual motion. This response is considered a compensatory mechanism that reduces visual dependence in postural control. The inaccuracies in visual input introduced by the OKS force individuals to reduce their reliance on visual cues and increase their reliance on more accurate somatosensory feedback to maintain an upright posture⁸⁾. This study has shown that even a single exposure to OKS using virtual reality can affect the weighting of sensory modalities in healthy adults and reduce visual dependence. This finding supports the hypothesis that OKS can effectively induce sensory reweighting and potentially improve postural control strategies in individuals with excessive visual dependence.

In the VR+OKS condition, the weighting of the visual input needs to be reduced, while the weighting of the somatosensory and vestibular systems needs to be increased to maintain postural control in the upright position. Normally, the somatosensory system primarily contributes to the estimation of the relative spatial positional relationship between the self’s body and the visual ground. In contrast, vestibular sensation is informed by the acceleration applied to the head, and thus its contribution in static standing is low¹³⁾. Consequently, we consider that the compensation for the reduced visual dependence caused by VR+OKS was predominantly caused by an increase in somatosensory weighting.

The removal of sensory input by eye closure has long been used in studies of sensory cross-weighting¹⁾. The effect of visual interventions on sensory reweighting has been reported to be more pronounced in the disturbance condition as an immediate change rather than a blockade¹⁴⁾. No effects on visual dependence occurred in the closed-eye condition; however, the results of the present study direct that report.

The present study was conducted using VR goggles, which are easy to use in clinical practice and inexpensive to implement, as well as a free application on a smartphone. OKS, which can be performed without using any special environment, can also be used in rehabilitation for visually dependent balance disorders and vestibular disorders. The results of this study further suggest that entertainment, such as video viewing and games such as OKS using VR goggles or HMDs, could be applied to balance rehabilitation.

The intermodal effect of visual systems on the somatosensory system is smaller than the intermodal effect of the somatosensory system on the visual system¹⁵⁾, likely due to the ceiling effect of the somatosensory system, which reduces the increase in the contribution of the already high somatosensory system during visual system perturbations. Consequently, the motor strategies employed during the OKS in the present study are likely to be influenced by the participant’s reliance on the somatosensory system. As such, future studies should examine whether the degree of dependence on the somatosensory system influences the effectiveness of the OKS. There is also a risk of age-related changes in the somatosensory system, and a decrease in balance after VR+OKS due to a decrease in visual dependence when used in older people with high visual dependence. Consequently, it is necessary to consider not only healthy adults, but also the elderly.

The limitations of the study include the small sample size and the fact that it was a single-exposure effect study of VR + OKS. Therefore, it is necessary to increase the number of participants and study the long-term effects of exposure in the future. The VR set used in this study weighed 550 g (comprising the VR goggles (approximately 400 g) and the iPhone (approximately 150 g)). This weight is a significant load for elderly individuals to bear on their head. Consequently, the effect of wearing a set must be considered.

The present study examined the single exposure effects of OKS using VR goggles and a smartphone app as a conveniently accessible sensory intersensory weighting intervention in upright postural control. The results of this study suggest that OKS in VR improves visual dependence. These results will facilitate the future use of VR in rehabilitation in postural control.

Conflict of interest

The authors have no conflicts of interest directly relevant to the content of this article.