Effects of Different Auditory Stimuli and Cognitive Tasks on Balance in Healthy Young Adults

Postural stability is the ability to maintain balance by keeping the center of gravity within the base of the support surface [1]. Correct visual, vestibular and proprioceptive inputs are needed for good postural stability and balance. It is thought that the auditory system is an additional source of balance [2, 3]. The auditory system and other sensory information provide valuable information about body orientation and contribute to postural control by providing spatial orientation, especially in people with visual, vestibular, and proprioceptive system damage [3]. Visual, somatosensory, and vestibular cues have a more significant influence on postural regulation. The auditory fixation theory is one of the hypotheses considered for integrating auditory information into postural control [4]. According to this theory, sound sources help the brain to construct a spatial image of the environment. This spatial image allows the brain to use this information for stabilization [5]. Additionally, sounds influence postural stability only when individuals pay attention to them [5]. Postural stability control is thought to be influenced by both the peripheral vestibular and the auditory systems. Vibrations sent via auditory pathways might interfere with stability control processes. According to findings from another study, people only exhibit these symptoms in response to high-intensity noise at a specific frequency [6]. Acoustic stimuli typically affect body sway and motor control, regardless of the exact mechanism by which they affect the human body [2].

Factors such as task complexity, muscle strength, height, weight, and gender influence static balance. Many healthy young adults should be able to finish the easy tasks in the allocated time. Reducing the area of the support surface and visual perturbation can make the task more difficult [6, 7]. Maintaining a stable and upright posture requires complex nervous system processes and cognitive processes [2]. Performance differences between dual-task and single-task conditions were assessed to determine how cognitive resources support postural control and gait. The results suggest that performing a postural task and a cognitive task simultaneously creates competition for the cognitive resources shared by both tasks, and this affects postural control [8]. Even simple postural activities demand attention, as demonstrated by several studies using dual-task paradigms in young and old individuals [9, 10].

Auditory stimulus prevents falls for people with imbalance due to visual, vestibular, or somatosensory deficits in middle aged and older adults [11]. Auditory stimulus reduces postural sways [12]. The underlying mechanism is unknown in various studies conducted with healthy individuals. However, it is suggested that auditory cues may stabilize balance [3, 13]. There are also studies reporting various findings such as increase [14], decrease [12] or no change [15] in postural sway in the presence of auditory stimuli in healthy subjects [5, 16].

In the literature, a limited number of studies investigating the effect of auditory stimuli on balance focused on static postural stability. Our study aimed to evaluate the effect of different auditory stimuli and simultaneous cognitive tasks on balance using static and dynamic postural stability and limits of stability (LOS) tests in healthy young adults.

The prospective study was conducted at the Audiology Clinic and the Division of Physiotherapy and Rehabilitation of Bezmialem Vakif University. University Research Ethics Committee approved the study on January 24, 2023 (Ethics Committee decision No.: 2023/27). Written informed consent was obtained from the individuals participating in the research by adhering to the ethical principles of the Declaration of Helsinki. Tests were administered to participants between February 13, 2023, and September 15, 2023.

Participants consist of healthy young adults who were admitted to the Bezmialem Vakif University Audiology Clinic and individuals who have 20 dB HL or better pure tone averages of 500-1,000-2,000–4,000 Hz frequencies [17], satisfied the inclusion criteria and agreed to participate in the study. The study excluded participants with a body mass index (BMI) of 30 or higher. In the literature, obese individuals (BMI ≥30) have been reported to have poor balance and motor control skills. In our study, in order to prevent balance disorders that may occur due to obesity, individuals with BMI ≥30 were not included to the study [18, 19]. Individuals without any vestibular, neurologic, systemic and musculoskeletal diseases were included in the study. The other inclusion criteria were as follows; having type A tympanogram (0.37–1.66 mmho static acoustic admittance and tympanometric peak pressure −100 daPa to +50 daPa) [20], attention levels within normal limits and general stability index values between 0.82 and 2.26 [21].

AT235 (Interacoustics, Middelfart, Denmark) tympanometer was used to evaluate middle ear function. AC40 (Interacoustics, Middelfart, Denmark) clinical audiometer was used to determine the hearing levels of the participants. TDH 39 headphones (Telephonics, Farmingdale NY, USA) were used to determine air conduction hearing thresholds, and a B-71 bone vibrator (RadioEar Corporation, New Eagle, PA, USA) was used to determine bone conduction thresholds. Stroop test TBAG form was applied to evaluate the attention levels of the individuals [22, 23]. The Stroop test TBAG form consists of four cards with six rows of 4 items randomly ordered and was administered in five sections. There are different versions of this neuropsychological test battery. Our study used the Stroop test TBAG form, a combination of the original Stroop test and the Victoria form, which has standardization, reliability, and validity studies for our national culture. The test was scored by recording the time to complete each section based on the norm study.

Biodex Balance System^® (Biodex, Inc, Shirley, NY, USA) was utilized to evaluate static, dynamic postural stability, and LOS tests. In the static postural stability test, the recording was 20 s while the floor was stationary. Anterior/posterior, medial/lateral, and overall stability indexes were calculated. In the dynamic postural stability test, evaluation was performed in the ground mobility level 6 state, and the recording was 20 s. Anterior/posterior, medial/lateral, and overall stability indexes were calculated. The LOS test was used to determine the ability to move and control the center of gravity within the body’s stability limits (general, forward, backward, right, left, forward/right, forward/left, backward/right, backward/left), while the floor was stationary.

Spondee is considered to be a single semantic expression that is a combination of two long, equally stressed and meaningful syllables. However, there are few words in Turkish according to this definition [24]. For our study, we used two- or three-syllable words recommended by Yalçınkaya et al. [25] and indicated these words as spondees. Words that individuals are familiar with from everyday life were used to generate word lists. Spondee word lists at 70 dB (A) and spondee word lists with a signal-to-noise ratio (SNR) of −6 dB in the presence of white noise were used as auditory stimuli. Auditory stimuli were presented bilaterally to the participants via supra-aural headphones. The SNRs of the spondee word lists were generated with Python Software Language Reference, version 3.11.1. The intensity levels of the auditory stimuli were calibrated using the AEC 201 ear stimulator (Larson Davis Depew, Depew, NY, USA) and System 824 Sound Level Meter (Larson Davis Depew, Depew, NY, USA).

Before starting the test, we asked the participant to stand on the static platform with his/her arms crossed in front of him/her and in a comfortable position. We adjusted the foot placement according to the center of gravity image on the screen and entered the foot positions on the platform. We told the participant not to change the position of their feet during the test. To avoid the learning effect and help the participant become acclimated to the test, we conducted a familiarization test before each test. The results of this test were not included in the analysis. In order to avoid feedback, we also turned off the cursor during the static and dynamic postural stability assessments. Participants were asked to maintain an upright posture in the static and dynamic postural stability tests and to catch the target with trunk movement without changing their feet’ positions during the LOS tests. The evaluations were performed together with the audiologist and physiotherapist. No one else was allowed in the test room. The ambient noise was kept below 40 dB (A). Static, dynamic postural stability and LOS tests were performed in an order. In each test, three different conditions were determined after the familiarization phase. Participants rested for 1 min after each test parameter. The results were obtained by averaging the scores of the three different measurements.

In each condition, participants had TDH 39 headphones connected to an Interacoustics AC40 clinical audiometer (Fig. 1). In the first condition, no auditory stimuli (quiet) were presented; in the second condition, spondee words were presented binaurally (spondee), and in the third condition, noise and spondee words (noise+spondee) were presented together binaurally. In all three conditions, the tests were repeated 3 times. Auditory stimuli started and ended simultaneously with the test. The auditory stimulus (spondee) was presented at 70 dB(A) in the second condition. In the third condition, auditory stimuli (spondee + noise) were presented at 70 dB(A) with a SNR of −6 dB. Participants were asked to repeat each word they heard in spondee and spondee+noise conditions in order to maintain their listening. After each test repetition the participants were given a 10-s rest.

G Power software [26] was used for power analysis. A total sample size of 28 participants is required to achieve a power of 0.80 with an effect size of 0.25, an alpha level of 0.05, and three repeated measurements based on the power analysis. Descriptive statistics of the evaluated parameters were performed using IBM SPSS version 22.0. First, the Kolmogorov-Smirnov test was performed to determine whether the data of the variables showed normal distribution. According to the Kolmogorov-Smirnov result, the significance value of LOS-overall, LOS-forward, LOS-backward, LOS-left, LOS-right, LOS-forward left, LOS-forward right, LOS-backward left, and LOS-backward right variables was calculated as p > 0.05 and it was determined that they were normally distributed. The significance value of static general stability, static antero-posterior stability, static medio-lateral stability, dynamic general stability, dynamic antero-posterior stability, dynamic medio-lateral stability, and LOS-time variables was calculated as p < 0.05, and it was determined that they were not normally distributed. One-way analysis of variance (one-way ANOVA) was used for variables with normal distribution and homogeneous group variances. Kruskal-Wallis analysis was applied for variables that did not show normal distribution and whose group variances were not homogeneous [27].

Thirty three healthy young people, 26 females and 7 males, aged min: 21 max: 29 (23.33 ± 2.43 years), participated in the study. The BMI of the participants was min: 18.65 max: 29.80 (22.62 ± 3.23) for females and min: 22.26 max: 29.7 (24.07 ± 2.55) for males.

In the analysis performed with one sample t-test, the mean duration scores of the participants for the five sections of the Stroop test TBAG Form did not differ from the norm values specified for the same age group. The mean scores of the participants were 9.00 ± 1.30 (STP1TIME), 9.75 ± 1.67 (STP2TIME), 12.06 ± 1.54 (STP3TIME), 16.32 ± 2.68 (STP4TIME), and 26.32 ± 1.58 (STP5TIME). In the comparison with normative data, p values were 0.405, 0.269, 0.345, 0.193, and 0.834, respectively. The results of the attention assessment with the Stroop test TBAG form showed that the participants' selective and focused attention were within normal limits [23].

The mean and standard deviation values of the variables of the static and dynamic postural stability and LOS tests performed in three conditions are shown in Table 1. No significant differences were observed between the variables of static and dynamic postural stability and LOS tests in the quiet condition, in the presence of auditory stimulus (70 dB (A) spondee), and in the presence of auditory stimulus in spondee+noise (−6 dB SNR 70 dB (A)) (See Table 2)

In the spondee condition, none of the participants made word repetition error in the static postural stability test, while one (3%) participant made one word repetition error in the dynamic postural stability test. Two (6%) participants made two word repetition errors in the LOS test. In the spondee+noise condition, 12 (36%) participants made at least 1 and 6 errors at most in the static postural stability test, while 25 (75%) participants made at least 1 and 6 errors at most in the dynamic postural stability test. In the LOS test, 21 (63%) participants made at least 1 error and 6 errors at most (See Table 3 for word repetition errors of all participants).

In the literature, different results have been reported on the effect of auditory stimulus on postural stability. In our study, the balance of healthy young adults was evaluated in the presence and absence of auditory stimuli. The evaluations in the presence of auditory stimuli were not performed as passive listening but under conditions where there was a cognitive task. Furthermore, adding white noise to the speech stimulus made this cognitive task more challenging. As a result, no change in balance was observed in healthy young adults in all three conditions.

In order to succeed in mobility-related activities in daily life, correct interactions and integration between sensory and motor inputs are required [10]. Human postural control is a complex multisensory process. Visual, somatosensory, and vestibular systems are known to contribute to balance control [28]. The auditory system is also thought to contribute to balance control. Despite its great potential to provide spatial information, its contribution to balance has not been sufficiently investigated [29].

Results regarding the effect of different auditory stimuli on postural control show variability in the literature. In the postural sway evaluation, where 65 dB pure tone stimulus and 65 dB background speech were presented via speakers, the sway was greater in both auditory stimulus types than in the absence of auditory stimulus [3]. Chen and Qu [30] reported that wider antero-posterior sway was obtained in the presence of unpleasant auditory stimuli compared to other auditory stimuli. However, the other study found that auditory information improved balance control by contributing to spatial localization [13]. In addition to this finding, the researchers reported that high-frequency sounds significantly reduced postural sway, while low-frequency sounds had no effect on postural control in young adults were presented with 80 dB pure tone auditory stimuli via headphones [31]. Ross, and Balasubramaniam [12] reported that the variability in postural sway decreased when the 75 dB white noise was presented to the participants via headphones while the eyes were open. On the other hand when evaluated with eyes open and closed, no change was found in the sway area using 70 dB SL pure tone stimuli and 70 dB peSPL click and tone burst stimuli [15]. Tandem Romberg test and Fukuda stepping, force/biomechanical measuring platform used in the studies mentioned about. Palm et al. [32] used Biodex in the assessment of dynamic stability. According to Palm et al. [32] no effect on dynamic stability index values were observed in healthy young adults, even with eyes closed. In this study, 75–80 dB SPL instrumental music was presented as an auditory stimulus. We used Biodex similar to Palm et al. [32] in our study, but we measured static and dynamic postural stability and LOS in three conditions (quiet, 70 dB (A) spondee and 70 dB (A) spondee+noise) and compared the test results. We found no significant differences in static, dynamic postural stability and LOS tests among spondee, spondee+noise and quiet conditions. Although our results showing that dynamic stability is not affected by auditory stimuli and noise support the results of Palm et al. [32] and Mainenti et al. [15] on dynamic stability, the stimuli used in the studies and the fact that the results are very variable show that more studies are needed in this regard.

It is suggested that passive listening is not cognitively demanding and does not require attention, and cognitively demanding task alongside the auditory stimulus is more effective on balance [33]. Behavioral results vary depending on the type of task and difficulty [34]. In a study conducted with individuals between the ages of 26 and 54, it was suggested that focusing on the external environment increases attention, and the increase in postural stability in the presence of auditory stimuli results from increased attention [35].

No deterioration was observed in the balance performance of the participants in our study, but errors were observed in word repetition in the presence of spondee and spondee+noise stimuli. This finding is in line with the studies that show the prioritization of postural control when healthy adults find themselves in cognitively demanding situations [36, 37].

In our study, although the inter-gender variability of postural control was not examined, all participants performed well in postural stability in the presence and absence of auditory stimuli. Research shows that females perform better in postural stability control than males in the absence or presence of acoustic stimuli [2].

The presence of noise seems to have a positive effect on balance stability. However, there may be lower and upper limits of noise intensity in terms of effectiveness for balance stabilization. In our study, evaluation was performed with spondee at 70 dB(A) and spondee+noise at −6 dB SNR at 70 dB(A). Since there is no clear information about the accepted limit value for sound intensity in the literature, it is not known whether the auditory stimuli used are among the limit values. So, it is thought that since the sensory system utilizes noise only if it is presented within certain limits [38], we also believe that these limits need to be investigated further.

In a study with a poor SNR, participants were presented with sentences in normal posture and tandem posture in the presence of competing speech or noise, and it was reported that postural control was adversely affected as the listening situation became more difficult due to increased cognitive load. It has also been suggested that these changes in postural control will be greater in middle-aged adults than in younger adults [39]. The literature has argued that this is due to decreased cognitive resources allocated to postural control [40]. In our study, the most challenging cognitive task was in the third test condition (−6 dB SNR spondee+noise). There was no significant difference in test results in healthy young adults compared to the other conditions. Evidence suggests that age effects during dual tasking are more pronounced in middle age when combined with a memory task alongside speech comprehension [39, 41]. Based on this information in the literature, there was no difference in the results between the conditions in our study because the evaluation was performed in the young age group.

It has been reported that the deterioration in postural stability under cognitive load with the listening comprehension task was greater in older adults than in younger adults [40]. Unlike Qu [40], in our study, the participants were asked to repeat the words and the conditions gradually became more difficult. While no change was observed in the stability of the participants, it was observed that the number of errors they made in word repetition increased as the task became more difficult.

Cluff et al. [33] showed that adding a cognitive task during standing leads to greater automaticity in the balance process, which in turn increases stability. However, passively listening to a single continuous auditory signal has not been shown to affect postural sway [42]. In our study, giving cognitive tasks during the postural task to participants with normal Stroop test results did not cause any changes. It can be thought that there was no effect on balance performance in individuals with normal attention because the cognitive tasks did not cause any change in the attention of the individuals.

It has been suggested that impairment in the visual, proprioception or vestibular systems leads individuals to rely more on hearing. One study reported that auditory input significantly reduced postural sway in people with bilateral vestibular loss when visual and somatosensory information was limited [11]. Patients with bilateral vestibular loss reported higher postural sway than healthy individuals when eyes were closed, and cocktail party noise was used. Even under conditions where visual and proprioceptive inputs were interfered, auditory stimuli had no effect on healthy subjects. This result suggests that auditory stimuli have a more pronounced effect on posture, especially when the vestibular system is damaged. The interaction between auditory and vestibular information occurs at the cortical level [43]. Although the presence of auditory stimuli did not affect the postural stability of the participants in our study, based on this information in the literature, it is thought that our test procedure may cause changes in postural stability if applied to people with vestibular system damage.

Since our study included only healthy young adults, the results cannot be considered valid for all age groups. The lack of investigating the inter-gender variability may be considered a limitation of our study. Unlike previous studies, we also examined the LOS test to evaluate the dynamic balance under different listening conditions. There was no change in the balance of healthy young adults in the presence of auditory stimuli and a cognitive task. However, as the cognitive task becomes more complex, the increase in errors made in word repetition suggests that people pay more attention to maintaining their balance. Future studies will contribute to the literature by examining the relationship between auditory stimulation and balance in different age groups and individuals with auditory and/or vestibular system pathologies, attention deficits, and high listening effort.

The authors are grateful to Kerem TOKER, Assoc. Prof., for his support in the statistical analysis.

Bezmialem Vakif University Research Ethics Committee approved the study on January 24, 2023 (Ethics Committee decision No. 2023/27). Written informed consent was obtained from all participants. A photograph (Fig. 1) of one of the participants was used in the text. Written permission was obtained from the owner of the photograph. All participants verbally and in writing declared that they volunteered to participate in the study.

The authors have no conflicts of interest to declare.

This study was supported by the Bezmialem Vakif University research fund.

Ö.G.T.: project administration, conceptualization, methodology, investigation, data curation, formal analysis, and writing – original draft. E.D. and K.A.: conceptualization, methodology, investigation, data curation, formal analysis, and writing – original draft. E.E.Y.: conceptualization, methodology, investigation, software, data curation, and formal analysis. H.N.G.: conceptualization, methodology, formal analysis, visualization, validation, and writing – review and editing.

Data supporting the findings of this study can only be provided upon reasonable request by the corresponding author Ö.G.T (e-mail: [email protected]) as they may contain information that could jeopardize the privacy of research participants.