Effect of Efferent Stimulation on the Differential Sensitivity in Individuals with Normal Hearing

Abstract

The aim of the article was to compare the conditions of silent and contralateral noise on Differential sensitivity in normal hearing individuals. A total of 40 participants (20 males and 20 females) were enrolled in the study with a mean age of 21.7 years, participants with normal hearing thresholds and no history of middle ear pathology were enrolled for the study. Difference limen tests such as difference limen for intensity (DLI), difference limen for frequency (DLF), and difference limen for time (DLT) were carried out in these 40 individuals in the two conditions of silent and contralateral noise using MATLAB. Statistical analysis was carried out using the SPSS version 25.0 were descriptive and inferential statistics were carried out. Data was normally distributed on the Shapiro–Wilk’s test of normality due to which a paired t test was carried out to establish the nature of significance between the silent and contralateral noise condition. Results reveal the presence of significant difference (P < 0.01) between the groups for DLF and DLT with contralateral noise condition performing better than silent condition for the parameters. However, no significant difference was obtained for DLI. There is a positive effect of the efferent auditory pathway on the Differential sensitivity thus implying that speech perception in noise is improved in the presence of background noise for normal hearing individuals due to this effect. But in case of DLI, the reduced spread of excitation could be the reason why there were no significant differences between silent and contralateral noise condition.

Introduction

In mammals, the efferent innervations to the cochlea are supplied by the Olivocochlear bundle (OCB), which consists of mainly two sets of neurons. The medial olivocochlear bundle and lateral olivocochlear bundle (MOCB and LOCB), which originates from superior olivary complex (SOC) [1]. They form the primary descending pathway, which controls various functions of the cochlea. It includes improved frequency selectivity, an improvement in signal-to-noise ratio, localization, maintenance of optimal electrical and mechanical states of the cochlea for encoding the acoustical signal by reducing the cochlear outer hair motility protecting the cochlea from overstimulation by reducing the OHC activity [2]. By presenting an acoustic signal in the contralateral ear, the olivocochlear efferent pathway can be activated. Various animal studies have demonstrated the activation of the olivocochlear pathway having suppressing effects on cochlear basilar membrane responses [3]. Physiological and electrophysiological studies have shown an anti-masking role of olivocochlear efferents, which significantly affects speech perception in noisy environments [4]. The otoacoustic emissions are the byproduct of outer hair cell mechanical activity [5]. Many literatures have reported the inhibitory effect observed in otoacoustic emissions amplitude when measured in the presence of contralateral acoustic stimulation in humans [6, 7]. There are also studies that have attempted to study the effect of contralateral acoustic stimulation on speech perception and have found that the speech perception scores tend to improve when tested in the presence of contralateral noise [4, 8].

The ability of an individual to detect the slightest change in acoustic stimuli concurrent to time is defined as temporal resolution. It can be assessed by varying the intensity, frequency, and duration of a continuous signal. The absolute minimum perceptible differences in amplitude, frequency, and duration are referred to as difference limen for intensity, frequency, and duration, respectively [9–11]. These parameters have a vital role in speech perception as speech is a complex stimulus with rapidly varying and multiple spectral properties. Hence, the temporal resolution abilities of an individual play an essential role in speech perception in quiet as well as in noise [12]. Comparatively, very few studies have been conducted to check for the suppressing effects of the contralateral MOCB on human auditory temporal sensitivity [12, 13]. Duration discrimination (DD), difference limen for intensity (DLI), and difference limen for frequency (DLF) are relatively simple psychoacoustic tests for measuring differential sensitivity and temporal resolution abilities [14]. The present study compares the effect of contralateral noise on differential sensitivity of the auditory system for contralateral acoustic stimulation in individuals with normal hearing.

Methods

Forty subjects (20 males and 20 females) aged between 18 to 27 years (mean age-21.8) participated in this study. All the participants were right-handed individuals. None of them had any otological complaints like reduced hearing sensitivity, ear infections, ear pain, tinnitus or no history of noise exposure or intake of ototoxic medicines.

All subjects had normal hearing thresholds (< 15 dB HL) tested at octave frequencies from 250 Hz to 8 kHz. Their speech identification scores were greater than 80%. The tympanograms were A-type with the presence of acoustic reflexes in both ears.

Procedure

Detailed explanation about the procedures and informed consent was taken from all the subjects. Pure Tone Audiometry was performed to determine the hearing thresholds, using Inventis Piano, a two-channel diagnostic audiometer (Inventis, 35127 Padova, ITALY). The estimation of Air conduction thresholds was done with TDH 39 headphones at octave frequencies (250 Hz to 8000 Hz). The bone conduction thresholds with Radio ear B-71 bone vibrator (250 Hz to 4000 Hz). To measure the hearing thresholds Modified Hughson-Westlake procedure was used [15]. A speech Identification test was carried out using Phonemically Balanced Words in Kannada for adults in Kannada, developed by Yathiraj and Vijayalakshmi [16]. Immittance evaluation was done to rule out the presence of any middle ear pathology using GSI Tympstar Pro (Grason Stadler Inc.-GSI-61; Milford, NH, USA). Acoustic reflex thresholds were obtained for the frequencies 500 Hz, 1000 Hz, 2000 Hz, and 4000 Hz.

Evaluation of differential sensitivity for frequency, intensity, and duration were carried out. These tests were carried out for all subjects in two conditions: in silence and in contralateral acoustic stimulation. Since numerous literatures have reported the dominance of the left hemisphere in temporal processing abilities, the right ear of every subject was chosen for conducting tests [17–19]. Duration discrimination (DD), pitch discrimination test (PDT), and intensity discrimination test (IDT) were carried out on all the participants using MATLAB software (Mathworks, R2014b, Standford University, California) using an MLP toolbox.

The duration discrimination was performed using two tasks: one using a complex tone and another using white noise. In the duration discrimination for complex tone, a tone with four harmonics (f0 = 330 Hz, mi4) was used. The subject has to identify the longest tone among the standard stimuli presented in 3-AFC trials. For the duration discrimination task for white noise, a white noise with a 10 s raised cosine onset and offset was presented. The target stimulus will be longer from the standard stimuli. The subject has to identify the noise stimulus with a longer duration [20, 21]. A three-down, one-up rule was used to estimate the difference equivalent to the 79.4% psychometric function.

Similarly, in pitch discrimination testing, the subject has to identify two tones as different in terms of perceptual difference of pitch of the stimuli. It was carried out in the 3-AFC method in which the listener has to identify the target stimulus having a different frequency with respect to the standard stimuli. In the intensity discrimination task, three tones among which one block will have the target stimulus with higher intensity than the other two blocks having identical standard stimuli. Similar to the other tests, this is also carried out as 3-AFC. The subject is asked to identify the loudest tone among each trial. In all these tests, the threshold calculation is based on a probability derived from the subject’s response to previous trials.

The testing was carried out by delivering test stimuli at 80 dB SPL through a laptop computer calibrated with HDA-300 headphones. White noise was presented to the left ear for stimulating the efferent pathway at a level of 40 dB SPL through another laptop calibrated with Eartone ER-3A insert phones. All the tests performed in a quiet room using the test standard test settings provided in the “mlp” MATLAB toolbox [21]. The full set of test procedures took almost 45 min per subject, so considering the long duration of testing time might induce attentional fatigue or distract alertness, the testing procedure was carried out as two halves. In order to prevent a practice effect, the order of tests was randomized among each subject. The second half of testing procedure for every subject was conducted during the same time of the day during which the initial half was performed. This was done to prevent diurnal effects that can act as an extraneous variable influencing the thresholds [22].

Statistical Analysis

Statistical analysis was carried out using SPSS (Statistical Package for Social Science) version 25.0, where descriptive and inferential statistics were obtained [23]. The data were normally distributed upon the Shapiro–Wilk’s normality test (sig > 0.05); hence, a parametric test was carried out. The nature of significance was established between the groups of with and without noise conditions for the parameters such as difference limen for intensity (DLI), difference limen for frequency (DLF), and difference limen for time (DLT) using a parametric paired t test.

Results

Concerning the DLI test, no significant differences (P > 0.05) were observed between the conditions of silent and contralateral noise with no noticeable variations seen in the DLI in conditions of silent and contralateral noise respectively (refer Table 1 and Fig. 1 for mean values). These values indicate that the efferent auditory pathway has no effect on the difference limen values for intensity.

Table 1.

Descriptive statistics (Mean and SD) for all 3 variables in conditions of with and without noise

Groups	Mean and SD	DLI (dB)	DLF (Hz)	DLT (ms)
Group 1 (without noise)	Mean	4.18	37.25	98.09
	SD	1.2	5.76	8.52
Group 2 (with noise)	Mean	4.47	34.84	90.11
	SD	0.98	3.74	7.26

Fig. 1.

The figure illustrates the DLI thresholds in conditions with and without noise

With frequency, the DLF values showed high statistical differences (P < 0.01) between the silent and contralateral noise conditions. A better value in noise condition obtained indicates a positive effect of the contralateral noise on the difference limen capacities for frequency (refer to Table 1 and Fig. 2 for mean values).

Fig. 2.

The figure shows the change in mean DLF thresholds in conditions with and without noise

The difference limen for time in complex tone were observed to be more in silent condition than in the presence of contralateral noise condition with highly statistically significant differences between the groups (P < 0.01), indicating positive effects of the efferent pathway on the duration discrimination thresholds (refer Table 1 and Fig. 2 for mean values) (Table 2, Fig. 3).

Table 2.

Depicts the nature of significance between the silent condition and noise conditions for all 3 parameters of different limen thresholds

Without noise-with noise	t value	Nature of significance (P value)
DLI	2.03	P > 0.05
DLF	3.98	P < 0.01
DLT	5.91	P < 0.01

^*P  < 0.05 indicates presence of significant difference between the groups

Fig. 3.

The figure shows change in mean DLT thresholds in conditions with and without noise

Discussion

In our study, the effect of the efferent auditory pathway on the difference limen thresholds were explored. Concerning the DLI, it was observed that there was no effect of efferent stimulation. This could be discussed with respect to the frequency selectivity methods, and one such method is PTC [24]. The psychophysical tuning curves (PTC) are used to assess the cochlea nonlinearity and its fine-tuning property, and its Q10 value determines the curve's width. For a normal hearing individual, the Q10 value would be less, indicating a narrow curve. Individuals with sensorineural hearing loss would have larger Q10 values indicating a broader curve due to the outer hair cell damage. Their cochlea becomes more passive—the better the Q10 value, the better the frequency selectivity [25, 26]. It is well-known that individuals with sensorineural hearing loss have broad frequency tuning curves due to the lack of functioning of outer hair cells resulting in a passively functioning Cochlea [27]. Due to the broad auditory filters, there is uncontrolled movement of the basilar membrane causing the spread of excitation, thus creating better intensity discrimination scores than normal hearing individuals.

On the other hand, normal-hearing individuals have lesser spread of excitation giving them higher DLI values than hearing impaired [28]. Literatures states that the PTC does not significantly differ between silent and contralateral noise conditions [29, 30]. The similarity in fine tuning with and without noise is the one of the reasons why DLI thresholds were not significantly different between the silent and contralateral noise condition. However, a study done by Delphi et al. (2009) contradicted our findings, stating that there is a significant effect of contralateral noise on difference limen intensity thresholds, especially white noise when compared to narrowband noise [13]. Another study done by Roverud and Strickland [31] stated that the mid-level hump in intensity discrimination was better in quiet condition followed by ipsilateral noise condition then contralateral noise condition [31].

With respect to efferent stimulation and frequency selectivity, Vinay and Moore [30] stated that the olivocochlear bundles play a significant role in manipulating basilar membrane functioning. The basilar membrane's velocity reduces with efferent activation around the characteristic frequency, thus enabling better frequency selectivity. It was shown that patients with an impaired efferent system have a reduced ability to focus attention in the frequency domain and detect signals at unexpected frequencies better than before [30]. The better frequency selectivity with efferent activation supports our findings showing significant difference between silent and contralateral noise condition with better values towards contralateral noise.

Concerning the Difference Limen in Time or the Duration Discrimination Test (DDT), the physiology of discriminating based on time extends beyond the peripheral system into the central auditory nervous system. Our study showed a significant difference between the silent and noise conditions with better scores towards the contralateral noise condition. The physiological basis for this could be the caudal projection, which extends from superior olivary complex to outer hair cells and rostral projections, extending from layer V and VI from the auditory cortex to the inferior colliculus [32]. Even though caudal and rostral projections are known to only influence only the outer hair cells, a study done by Grummer et al. (1988) on modulation transfer function of efferent neurons in the guinea pig Cochlea reveal that efferent auditory system create a shorter phase delay and tight distribution creating an impact on the shape of the modulation transfer functions (MTFs) which could be due to the involvement of a polysynaptic pathway involving brainstem levels at higher level than the superior olivary complex [33]. These anatomical projections create a positive effect on DLT thresholds. These positive effects improvise speech perception in noise abilities in normal-hearing individuals. A review of existing literature related to speech perception in noise with efferent stimulation has been documented extensively. Maruthy et al. [32], in their literature, were able to establish a functional interplay between putative measures of rostral and caudal efferent regulation of speech perception in noise, where they stated that the two efferent systems function independently but have a common goal to enhance the signal in the presence of noise [32]. Another literature by Yashaswini and Maruthy [34] stated that contralateral noise impacted the SIS and SNR 50 levels. However, they concluded that the intensity of noise directly influences medial olivocochlear bundle–mediated efferent inhibition, and the role of the medial olivocochlear bundle in regulating speech perception in noise needs to be revisited [34]. Mertes et al. [35] established a trend in signal-to-noise ratio improvement with increasing contralateral inhibition at the lowest SNR, thus showing a correlation between psychometric function curve and contralateral inhibition [35].

Limitations and Future Directions

The paper could have yielded better results if there were a greater number of participants. The study could have added Oto Acoustic Emissions, speech perception, temporal processing tests, and Difference Limen tests to establish a correlation. As a future direction, similar parameters could be used to compare the effect of the efferent pathway on the difference limen thresholds between normal hearing and sensorineural hearing loss individuals. Electrophysiological measures could be used to explore the neurophysiological basis of the efferent auditory pathway.

Conclusions

The study concludes a positive effect of the efferent auditory pathway on difference limen thresholds, which gives us additional evidence that normal-hearing individuals have good frequency selectivity and speech perception than individuals with hearing loss, especially in the presence of background noise. The results also prove that the contralateral stimulation directly impacts the difference limen thresholds due to the cochlear fine tuning and the physiological changes at the subcortical and cortical levels. The auditory efferent is often not prioritized as the afferent, but these physiological effects signify the importance of the auditory efferent pathway on the auditory system.

Funding

There is no funding by any agency for the manuscript.

Declarations

Conflict of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

Ethical Standards

In the present study, all the testing procedures were carried out on humans using non-invasive techniques, adhering to the guidelines of the Ethics Approval Committee of the institute. All the procedures were explained to the participants, and informed consent was taken from all the participants of the study.