Influence of Different Types of Contralateral Suppression Tones on Otoacoustic Emission in Children With Autism Spectrum Disorder
Article information
Abstract
Background and Objectives
Auditory sensory gating deficits are abnormalities in patients with autism spectrum disorder (ASD) that may lead to sensory processing difficulties. It is particularly difficult for children with ASD to distinguish multiple auditory stimuli, which hinders them from focusing on a single auditory stimulus and separating unnecessary sounds. Suppression of otoacoustic emission (OAE) is an approach used to identify sensory gating deficits in the general population, specifically for children with ASD. This study aimed to investigate the suppression effect of various types of sound suppressors to measure their sensory gating capacity in children with ASD.
Subjects and Methods
Twenty children including 10 with ASD and 10 normally developing children aged 6-12 years were recruited for this study. One accessible ear was exposed to transient-evoked OAE, whereas the other was exposed to suppressor tones. Contralateral suppressors included white noise, Quranic recitations, environmental noise, and natural sound. The magnitude of OAE suppression was determined from the difference between the OAE amplitude with and without the masker (in dB sound pressure levels) for all sound types. The sound with the highest suppression effect was determined using effect size calculation and repeated-measures analysis of variance at a 95% confidence level. A high suppression effect may suggest a high sensory gating performance, whereas low suppression may indicate low sensory gating performance.
Results
Based on the analysis, the sound with the highest suppression effect was that of the waterfall. The suppression results were supported by descriptive analysis findings and effect-size calculations.
Conclusions
This study provides a better understanding of the alternative sound stimuli, besides the standard white noise tone, for the assessment of sensory gating deficits among children with ASD. Sounds with a high suppression effect have the potential to be used as sound therapy interventions for children with ASD as part of rehabilitation and therapy.
Introduction
Autism spectrum disorder (ASD) has been found to have abnormal pathology of inhibitory interneurons and imbalance between excitation and inhibition in the hippocampus causes the sensory information cannot be processed and transferred properly. Neuroanatomical abnormalities of ASD has been reported including the reduction of size and misalignment of medial olivocochlear bundle (MOCB), abnormal cortical growth pattern, and disorganization of neuronal activities of the brain [1-3]. These abnormalities suggest that ASD disorder may be extended and affecting the function of olivocochlear region [4].
The neuroanatomical abnormalities at MOCB may impede its function to protect the cochlear damage from the noise-induced environment peripherally and to enhance speech perception in the presence of noise, where it guides the development of attention during listening and aids in processing the complex auditory signals at central pathways [5-7]. In addition, the malfunction of MOCB may include the inability to suppress the noise by reducing the neural adaptation thus making the neuronal stimulation less adapted and less stimulated and making the neural fibres to response more or stimulated strongly. As a result, background noise will be as audible as the main sound which triggers some abnormal behavior among ASD patients [8]. The behaviour shown by ASD patients includes that they may be easily get distracted with the sound of air conditioner in a room as compared to the speaker’s voice for instance. In school environment, this individual might be unable to focus in class and to the teacher’s voice as the voice heard might be as loud as the background sound such as the ceiling fan sound, voices of the classmates, school bell, and many more.
MOCB function can be assessed in several ways. This includes the psychophysical tuning curve, fixed duration masking curve, intensity discrimination limens, localization-in-noise test, auditory evoked potential test, electroencephalography as well and magnetoencephalographies test. Of those assessments, OAE is one of the audiological tests that has been widely reported to examine the function of MOCB [1,8-11]. OAEs are sound presented at the outer ear to the cochlear. The emission was obtained from the outer hair cell (OHC) and the reflected sound was propagated backward to the outer ear to be recorded as a response. A previous study investigated the behavior changes of gerbils when MOCB was removed and exposed to intense noise based on the OAE test [12]. In general, without MOCB animals appear to be in stressful conditions upon exposure to a loud sound. On the other hand, animals with MOCB remain calm and relaxed when exposed to the loud sound. The relation between MOCB and the suppression OAE was reflected in the findings mentioned earlier where suppression OAE is the byproduct of the cochlear active mechanism and MOCB. The MOCB function is considered to be related to the sense of comfort, relaxation, and possibly to emotional functions as well. Specifically, studies have shown that individuals with enhanced MOCB function tend to exhibit higher levels of subjective well-being and report greater emotional stability [13,14]. Furthermore, the disruptions in MOCB function can also contribute to the development of emotional dysregulation and mood disorders such as anxiety and depression [15]. Therefore, investigating the relationship between MOCB function and emotional experiences holds significant potential for improving therapeutic approaches and interventions.
In ASD, the function of MOCB has been studied using suppression OAE test by using white noise as contralateral suppressor (CS) [16-18]. These studies found reduction in the contralateral suppressive effect on OAEs in ASD children as compared with normal groups. This remarks that the efferent auditory pathway, which controls the responses from OHCs, is not as effective in ASD children as in control groups. Based on the function of OHCs and the reported findings of the suppressive effect of the MOCB, it is hypothesized that hypersensitivity to sounds and poor performance in background noise in ASD children may be explained by increased activity of the electromotility of OHCs or lack of suppressive effect of the MOCB causing the reduction of OAE suppression [19,20].
Several studies have investigated pure tones as sound suppressor for OAEs, as well as the use of musical sound instruments, environmental noise sounds, natural sounds, amplitude-modulated broadband noise (AM BBN), speech babbles, cafeteria noise, traffic noise, envelope-modulated BBN (temporally complex noise) and Quranic recitation [18,21-25] in different types of population includes in normal young adults and normal children. The results from the studies found a different suppression effect using various types of sound suppressor depending on several factors including the population of interest and the experimental design. Studies from Maison, et al. [18] and Namyslowski, et al. [25] in normal hearing school-aged children and adults revealed that the BBN showed a better OAE suppression effect as compared to pure tone and narrow band noise (NBN) given the large bandwidth spectrum of BBN as compared to the three CS. Najem, et al. [24] investigated the use of pure tones of 1,000 Hz able to suppress 1,000 Hz tone pip and pure tone of 8,000 Hz able to suppress 4,000 Hz tone pip and compound action potential click in normal hearing adult and found that the suppression effect seemed to depend on the frequency cues of the stimulus and the suppressor tones. A study by Maison, et al. [18] also revealed that the AM BBN CS has larger OAE suppression as compared to unmodulated BBN in normal hearing adults. A study by Kalaiah, et al. [23] in normal hearing school-aged children compared the effects of using several types of suppressor signals on the medial olivocochlear system activation and found that the largest transient evoked otoacoustic emission (TEOAE) suppression was observed in white noise and the least suppression was observed in speech babble. The authors also concluded that the TEOAE suppression of cafeteria noise CS was larger as compared to the traffic noise CS. Based on previous findings that have yielded a variety of results in different population tested, it has become necessary to explore the findings in ASD population.
To the author’s knowledge, only one study investigated the suppression effect using different suppressor signals namely 1,000 Hz NBN and BBN among ASD population [1]. The result shows that BBN causes more suppression effect as compared to NBN. Since Danesh and Kaf [1] found that BBN has highest suppression effect as compared to NBN, it is merely important to explore the other types of sound suppressor that have potential or have similar strength with BBN to stimulate the MOCB function.
Apart from the function of MOCB that needs to be catered to improve the suppressor effect, several potential benefits that were considered in finding alternative sound suppressors particularly for individuals with ASD were in aiding in sensory regulation and improving focus and attention. The alternative suppressors can create a more comfortable and manageable sensory environment for individuals with ASD, promoting a sense of calmness and reducing potential distress. Apart from that, by introducing the comfortable sound suppressors, it can potentially enhance the attention and focus. This can be especially beneficial in educational settings, where individuals with ASD may benefit from better engagement in tasks, following instructions, and absorbing information even in noisy environment [26].
The aim of this study was to examine the function of MOCB by stimulating the OHC responses towards various sound suppressors apart from white noise. Additionally, this study aims to investigate which sound suppressor has the highest suppression effect in ASD population.
Subjects and Methods
Participants
This study had received full ethical clearance from International Islamic University Malaysia Ethics Committee (ID No: IREC 2020-063). All parents and participants were given a sheet of information on the study procedure and have given consent to proceed. A total of 20 children aged 6 to 16 years old participated. The participants were recruited from various sources including from Psychiatry and Mental Health Clinic, Sultan Ahmad Shah Medical Centre (SASMEC), IIUM Hearing and Speech Clinic, Kuliyyah of Allied Health Sciences, and circulating messages through an online platform. Of those 20 participants, 10 were ASD children as an experimental group and 10 were normal developing children (ND) as the control group with a total of 12 males and 8 females. The ND group consists of 4 males and 6 females aged 6 to 16 years (mean=11.2 years). For the ASD group, there are 8 males and 2 females within the same age range (mean=9.8 years). All ASD participants were screened and diagnosed by Clinical Psychiatrist to only recruit participants with ASD as primary diagnosis and having mild to moderate level of ASD who were at least able to understand and follow instructions. The tests required the ASD to sit still while performing tasks; thus, it is important to include only ASD children with a mild to moderate degree of symptoms as research participants to avoid excessive noise interference during OAE recording. Eight of the ASD participants have no comorbidities with other disabilities, while 2 participants have comorbidity with attention-deficit/hyperactivity disorder (ADHD), as confirmed by a clinical psychiatrist.
Prior to the OAE recording, all participants underwent diagnostic hearing assessments. This includes full history taking procedure, otoscopic examination, tympanometry, acoustic reflex testing, and pure tone audiometry testing. All participants were in normal and healthy state of health, and they reported to have no history of noise exposure, ototoxic drug intake, chronic middle ear disease, or familial hearing loss. Participants with impacted and maximum ear wax were subjected to have removal of earwax from ENT before proceeding to the conventional tympanometry (226 Hz), acoustic reflex testing (500 Hz to 4,000 Hz), and pure tone audiometry testing (250 Hz to 8,000 Hz). All participants had type A tympanogram suggesting normal middle ear function, normal ipsilateral and contralateral acoustical reflex threshold using diagnostic acoustic reflex test and hearing threshold of below 20 dB intensity across frequencies tested.
Instrumentation and stimuli
Otodynamics OAE ILO version 6 apparatus (ILOv6) by Otodynamics Ltd, United Kingdom was used for TEOAE recordings. Sennheiser 280 HD Pro headphone (Sennheiser) and Sound Blaster X-fi (Creative Technology) were used so that the output of the calibrated sound is presented constantly on the contralateral ear (left ear). Sound suppressor signals used in this study were white noise, nature sound (river, ocean, waterfall, rainfall), environmental noise (air conditioner compressor), and Quranic recitation sounds. All suppressor’s sound were calibrated using 6 cc acoustic coupler and a sound level meter type I in accordance with standard ISO 389-1 and IEC 303 to ensure proper sound pressure level for all stimuli and presented at 60 dBA which is believed to be sufficient to stimulate MOCB and is insufficient to initiate the middle ear acoustic reflex [27].
Suppression TEOAE measurement
All participants were tested with TEOAE in two conditions on their right ear with CS presented on the left ear. The first condition is a baseline OAE recording without CS and the second condition is the OAE recordings with CS using 7 different sound suppressors as described earlier. Participants were first tested in quiet TEAOE recording as a baseline testing. One minute break was given after the baseline recording to ensure the activation of MOCB activities from previous CS was completed before presenting the next CS. Then, the TEOAE was recorded again after 30 seconds of initial continuous sound presentation with the presence of contralateral presentation of suppressor noise (also known as forward masker). TEOAE was obtained by using linear click stimuli at 60 dBpeSPL amplitude through pediatric-type acoustical probe inserted into the external ear canal. TEOAE recordings were automatically stopped after 260 responses had been recorded. TEOAE was only accepted when the stimulus stability was at least 90% and recording reproducibility was 70%. The tested frequencies were 1,000 Hz, 1,400 Hz, 2,000 Hz, 2,800 Hz, and 4,000 Hz. TEOAE was only considered present if the signal-to-noise ratio (SNR) was greater than 6 dB at majority of the tested frequencies. The OAEs recording with CS were randomized for each or the participants to avoid order effects.
The baseline measurement of TEOAE was taken by placing OAE probe with a microphone into the right ear while the participants were asked to sit still while playing games using an iPad Air with OS version 16 (Apple Inc.) to ensure the attention of participants was controlled to obtain robust and stable recordings [28,29]. Similarly, all recordings were taken in an attention state where participants were asked to play the attention games but with no sounds coming from the games. Next, the second condition proceeded where the TEOAE was acquired with the presence of CS tones based on random sequence for the presentation of seven different CS types. For this condition, the CS was presented first on the contralateral ear (left ear) at 60 dBA for 30 seconds through headphones before the recording of TEOAE begins. A one-minute stimulus-interval was set between each CS presentation to ensure the MOCB activities from the predecessor CS stimulation had been completed as it was reported to last for 1 minute [30].
Data analysis
The TEOAE suppression effect was defined as the difference score between the TEOAE without and with CS condition (TEOAE without suppression minus the TEOAE with CS). The positive value indicates the presence of suppression TEOAE while negative value indicates an absence of suppression TEOAE. The mean of suppression value was computed for all CS recorded. All data was analyzed using Statistical Package for the Social Sciences (SPSS) software version 26.0 (IBM Corp.). All the data met the parametric assumptions for both repeated measures (RM) analysis of variance (ANOVA) and multivariate analysis of variance (MANOVA). The data in general was normally distributed and the variance was homogenous. This was supported by the visual inspection of the data and the non-significant finding identified from Mauchly’s test of sphericity (p>0.05).
RM ANOVA at 95% confidence level was used to compare the mean suppression value between stimulus sounds on the same subjects whereas MANOVA was used to compare the suppression effect between groups (ND and ASD). If the RM ANOVA or MANOVA result was significant, a post hoc analysis with Bonferroni adjustment was used to account for type I error following multiple comparisons conducted across the groups. The effect size was also used to support the statistical findings in which the effect size was not affected by the sample size regardless of the statistical differences [31]. The effect size ranges reported in the form of partial eta squared (η2) using the following values in order to determine the effect size: small (0.01), moderate (0.06), and large (0.14) [32].
Results
Table 1 shows the comparisons of p-value and effect size for both ASD and ND group. Table 2 shows the mean of overall suppression TEOAE response, standard deviation, and effect size of TEOAE suppression in both ASD and ND groups.
MANOVA identified no significant difference in the mean of suppression TEOAE between ASD and ND groups (p= 0.372) for all CS; however, a large effect size was indicated (partial eta squared η2=0.41). The effect size comparisons between ASD and ND groups for each CS were tabulated in Table 2. Based on the analysis, the means of TEOAE suppression was considered as higher in ND group in comparison to the ASD group for all CS.
RM ANOVA showed no statistically significant difference (p>0.05) in the mean of TEOAE suppression among different suppressor types in the ASD group at F (6,54)=1.013, p=0.427; however, a large effect size was indicated (partial eta squared value of 0.101). On the other hand, a significant difference was found in the mean of TEOAE suppression among different suppressor types in ND group (p<0.05) at F (6,54)=3.474, p=0.006, consistent with large effect size (partial eta squared value of 0.278).
Based on both the effect size and p-value, it provides an indication that the sound suppressor noise was effective in stimulating MOCB in both normal and ASD groups. The highest contralateral TEAOE suppression was obtained when using waterfall for ASD group and rainfall for ND group. The lowest contralateral TEAOE suppression effect was obtained when using river sound as CS in both groups.
The waveform spectrum for the four CS with the highest suppression and the CS with the lowest suppression for ASD group is shown in Fig. 1. The waveform spectrum of each natural sound revealed that the waveforms of white noise, rainfall and waterfall were similar to each other in terms of their energy distribution over time. From Fig. 1, the energy distribution seems not consistent with fluctuating energy and irregular peaks for both ocean and river sound suppressors.
Discussion
The aim of this study is to examine the function of MOCB to inhibit OHC responses using suppression TEOAE using different sound suppressor types among the ASD population. The activation of the MOCB may activate neural inhibitory response towards electromotility of the OHCs. This inhibitory response, also called as suppressive effect reduces the amplitude of OAE responses [20,33]. It has been suggested that the suppression effect of the MOCB system plays a role as an auditory filter, improving SNR, especially in speech-in-noise intelligibility [20,33] and detection of multi-tone complex in noise [34]. Moreover, Giraud, et al. [33] suggested that the MOCB is engaged in the protection of the auditory system via its regulatory role on the OHCs. Thus, MOCB is considered to function well when the suppression effect can be observed and vice versa [1]. From the result, ND group has higher suppression effect as compared to ASD for all CS. This result indicates that the MOCB is well-functioned in ND as compared to the ASD children. The lower suppression effect found in ASD might be an indicator that one or more of the MOCB functions are defective as discussed in the previous studies [1,4].
The size of the MOCB structure in ASD children was reduced, absent, or misaligned, suggesting olivocochlear dysfunction [4], which causes the OHC to remain active regardless of how loud the sound is. This making all the sound perceived unfiltered and resulting to less or no inhibitory response causing less suppression observed in ASD subjects. Danesh and Kaf [1] also found a reduced contralateral suppressive effect on OAEs in ASD children as compared with normal groups using BBN. This remarks that the efferent auditory pathway, which controls the responses from OHCs, is not as effective in ASD children as in control groups not only when stimulated using white noise but also using different types of CS namely 1,000 Hz NBN. This coincides with the present study that further found another six CS that demonstrated poor suppression TEOAE amplitude in comparisons with normal hearing children.
The present study found nature sounds such as rainfall and waterfall have stronger TEOAE suppression effects in ASD and normal children in comparison to the standard CS using white noise. White noise has been remarked as the most effective suppressor to measure the MOCB [27,35-37]. The proposed explanation for the highest suppressive effects using white noise CS is due to its large bandwidth that activates a large number of neurons at once causing a reduction of the OAE amplitudes thus creating high OAE suppression [23]. In the present study, white noise suppressor was the third effective suppressors among the seven types of suppressors used. The findings suggest that other nature sound (waterfall and rainfall) have similar or stronger effects in suppressing the MOCB. Since nature sound, specifically waterfall and rainfall also have large bandwidths that resemble white noise, a higher suppression effect also can be seen in waterfall which also can elicit a response from a larger number of neurons at once. However, this does not apply to river and ocean sound as the mean of suppression effect was low as compared to waterfall and rainfall. In general, these two sounds do not resemble a larger frequency spectrum bandwidth as opposed to the other nature sound as shown in Fig. 1.
From Fig. 1, a fluctuation of energy with irregular peaks was observed in both ocean and river CS that could be the results of the water flow current, frequencies of the waves, wind whistling, and other factors. Since the sounds suppressors were presented throughout the TEOAE recordings that took up around 60 seconds, the energy fluctuations occurred more than once. This might be the reason ocean and river sound produced a low suppression effect as compared to rainfall and waterfall sounds. Kalaiah, et al. [23] also reported similar findings where sounds with more energy fluctuations elicited weaken the MOCB suppression similar to this study.
On the other hand, it was observed that Quranic recitation is also among the highest CS (forth highest) as compared to others. Even though Quranic recitation has fluctuating energy distribution, due to its attributes that were similar to speech sounds and were affected by different reciter, Quranic recitation was proven to have a spiritual effect on the emotional part of the brain, specifically in the hippocampus of amygdala. In addition, the series of Quranic recitation were taken from the study by Irwansyah [38] that revealed few verses with positive emotional effect experimented with ASD children to study their emotional well-being. Apparently, a study has revealed that the presence of sensory stimuli activates brain areas connected to emotional processing and can reduce MOC function [3]. Neurophysiologically, in exposure to a certain stimulus, the central nervous system will react and respond to the various stimuli, including the hyperactivation in amygdala (emotional processing site) that later was interpreted as neural changes at low level exposures. Whereas the physiological role of the MOCB system is protecting from excessive sound transmission to the IHC by inhibition of OHC activity, thus the neural changes altering the auditory efferent system function, inhibit the hyperpolarization OHC activity by MOCB and cause the OAE amplitude to be reduced. In other words, the reduction of OAE amplitude might be due to the top-down brain processing which was triggered by the response of amygdala [39].
The present study concluded that the sound with the highest suppression effect was waterfall followed by rainfall, white noise, and Quranic recitation. Apart from white noise that was used as a standard CS sound in clinic, it is quite promising to utilize the use of other types of sounds that have similar effects as the white noise. Improvising the suppressor sound using waterfall, rainfall, and Quranic Recitation sound might be more pleasing and comfortable as compared to listening to the white noise sound which may give impact on the listener of those with sensory processing issues such as ASD children. The conclusions of this study were limited to the suppression effect in normal and ASD children, based on the age range of the participants and the comorbidities involved. MOCB reaches full maturation by birth; therefore, the suppression TEOAE findings should be adult-like regardless of participant age [40]. On the other hand, MOCB in ASD children has been reported to be dysfunctional. Due to this factor, there is a possibility of a delay in the maturation of MOCB, depending on the child’s age and the severity of the abnormality in MOCB. The wide age range of the study participants (6 to 16 years old) could hypothetically affect the suppression TEOAE results, as the delay in MOCB function could vary across different ages.
To further address this and broaden the scope, future research could consider to limit the age range of the study participants and include other populations, such as adults with ASD, to examine whether similar suppression effects are observed across different age groups. Additionally, investigating the potential impact of comorbid conditions, such as ADHD and hyperacusis, on the suppression effect could contribute to a deeper understanding of the underlying mechanisms and provide valuable insights for the intervention used.
Notes
Conflicts of Interest
The authors have no financial conflicts of interest.
Author Contributions
Conceptualization: Ahmad Aidil Arafat Dzulkarnian. Data curation: Fatin Nabilah Jamal, Fatin Amira Shahrudin. Formal analysis: Fatin Nabilah Jamal, Ahmad Aidil Arafat Dzulkarnian, Sarah Rahmat. Funding acquisition: Ahmad Aidil Arafat Dzulkarnian, Shahrul Na’im Sidek, Hazlina Md Yusof, Siti Rafiah Abd. Hamid. Investigation: Fatin Nabilah Jamal, Fatin Amira Shahrudin. Methodology: Ahmad Aidil Arafat Dzulkarnain. Project administration: Ahmad Aidil Arafat Dzulkarnian. Resources: Nadzirah Ahmad Basri. Software: Mohd. Zulfaezal Che Azemin. Supervision: Ahmad Aidil Arafat Dzulkarnian. Validation: Ahmad Aidil Arafat Dzulkarnian. Visualization: Fatin Nabilah Jamal. Writing—original draft: Fatin Nabilah Jamal. Writing—review & editing: Ahmad Aidil Arafat Dzulkarnian, Fatin Nabilah Jamal. Approval of final manuscript: all authors.
Funding Statement
This study has been funded under Ministry of Higher Education through Trans-disciplinary Research Grant Scheme (TRGS/1/2019/UIAM/02/4/2).
Acknowledgements
The authors would like to acknowledge staff from Department of Psychiatry and Mental Health, Sultan Ahmad Shah Medical Centre and Department of Audiology and Speech-Language Pathology, International Islamic University Malaysia for their assistance in the data collection process.