Changes in cortical auditory evoked potentials in response to auditory training in elderly hearing aid users

Abstract

Objective

To compare the cortical auditory evoked potential responses pre-and post-Auditory Musical Training associated with hearing aid adaptation in elderly people with presbycusis. Design: this is a prospective, randomized, single-blind study. Study Sample: eight presbiacusis elderly people between 65 and 80 years, new hearing aid users, divided into two groups participated in the study: Hearing Aid Group: use of hearing aid; and Auditory Training Group: use of hearing aid in addition to musical auditory training for 16 sessions. All participants were submitted to cortical auditory evoked potential tests with verbal stimulation in two different moments: Initial assessment, carried out before hearing aid adaptation and auditory training, and after three months, final assessment at the end of the auditory training sessions. All participants were adapted bilaterally with digital mini hearing aids. Results: There was a decrease in the P3a latency component for the Auditory Training Group when initial and final assessment were compared. Conclusion: There was a change in the CAEP in elderly people with presbycusis in response to the Musical Auditory Training associated with the use of hearing aids in elderly people with presbycusis.

Introduction

Hearing loss associated with aging - presbycusis - affects not only the peripheral auditory system; but changes in the anatomy and physiology of the central auditory system of the elderly can also occur, in addition to the changes caused by the aging process itself [1].

Even in mild hearing loss, a fundamental impact on the organization and functioning of the auditory cortex follows, as there is the recruitment of other sensory systems, such as the somatosensory system in an attempt to regulate the deficient neural processing of auditory information [2].

The impacts resulting from hearing deprivation in the elderly can be reduced with the appropriate intervention for hearing loss [2, 3].

Hearing rehabilitation may include hearing aid adaptation and auditory training, which is essential for the development of central auditory skills, such as auditory closure, auditory figure-ground, temporal ordering (duration pattern and frequency pattern), binaural separation and binaural integration [4].

The objective of auditory training, according to Bamford [5] is to develop or rehabilitate auditory skills, necessary for understanding sounds. Auditory training does not improve peripheral auditory sensitivity, that is, there is no change in tonal thresholds. However, this intervention proposal through auditory stimulation is directly related to brain reorganization through patients’ Central Auditory Nervous System (CANS) plasticity, improving attention and perception of more complex sounds, such as speech, allowing the individual to experience different sounds more clearly [6, 7].

Chermak and Musiek [4] state that in the elderly population the neural substrate is also subject to changes after auditory training, despite the plasticity potential reduction of the nervous system at this stage of life. For this reason, training strategies provide more compensation than recovery.

Musical Auditory Training (MAT) is an auditory training program developed to meet the needs of elderly hearing aid users, focused mainly on the auditory skills of temporal processing - resolution and temporal ordering - and selective attention. After the MAT application in elderly hearing aid users, an improvement in temporal auditory skills was found, proven by behavioral tests, evidencing the benefit of MAT in these skills [8–10]. However, this investigation found no studies that used electrophysiological measures to assess the effects of this auditory training program on the elderly’s auditory function.

The electrophysiological measure is one of the means of investigating the functions of the central auditory pathways and has been an important instrument in monitoring the therapeutic evolution of the elderly in the auditory rehabilitation process [11, 12]. Cortical Auditory Evoked Potential (CAEP) is one of these measures and allows the assessment of cortical activities, more specifically the discrimination, integration and attention skills of the brain, involving the function of the thalamocortical and corticocortical auditory pathways, primary auditory cortex and associative cortical areas [13]. Considering the complexity of the factors that may be associated with hearing difficulties in the elderly, aging has been the subject of several studies in the area. Understanding the central auditory mechanisms involved in the auditory adaptation and rehabilitation process in this population is a challenge. Thus, this study seeks to investigate the therapeutic evolution at a central level in the elderly through Electrophysiology, more specifically the CAEP.

The hypothesis is that auditory rehabilitation through Musical Auditory Training (MAT) associated with the use of hearing aids is capable of generating changes in the auditory function in elderly people with presbycusis. If the hypothesis is confirmed, there may be a change in the clinical routine, favoring the indication of controlled auditory training programs, which added to the benefits obtained from the use of hearing aids can contribute to the full restoration of the hearing function of elderly people with difficulty in speech recognition in noise.

Objective

To compare the cortical auditory evoked potential responses pre- and post-Auditory Musical Training associated with hearing aid adaptation in elderly people with presbycusis.

Method

The present study was a prospective, randomized, single-blind study. It was carried out after approval by the Research Ethics Committee of the Faculty of Philosophy and Sciences – UNESP campus of Marília, under number 02848918.2.0000.5406, in accordance with Resolution 466/2012. To participate in the sample the patients signed a form of free and informed consent after being given information about the research.

Results

Following, Table 1 shows the descriptive data for HAG and ATG participants to characterize the sample.

Based on these data, the statistical analysis was performed to verify group homogeneity, as shown in Table 2.

Note: * p <0.05 significant association by Fisher's exact test.

Table 3 shows the comparison between the groups for the CAEP responses from the mean latencies of the P1-N1-P2-N2-P3a complex for the two moments of assessment, and the ANOVA results.

Note: multivariate analyzes were based on the assumption of equality of covariance matrices through the Box’s test. * Significant difference in relation to the initial assessment within the group through the Holm-Sidak Post-hoc test for p-value ≤ 0.05. † main effect of time within the group through mixed ANOVA of repeated measures for p-value ≤ 0.05.

There was a statistically significant difference for the P3a component in the ATG when initial and final assessment were compared, indicating a time effect within the group, with a latency decrease in this component after hearing rehabilitation.

Table 4 shows the means of the amplitudes of the P1-N1-P2-N2-P3a complex for the two moments of assessment, and ANOVA results.

Note: multivariate analyzes were based on the assumption of equality of covariance matrices by the Box’s test.

There was no statistically significant difference in relation to the amplitudes of the P1-N1-P2-N2-P3a complex considering the analysis of the group and time effect, and the interaction between group and time.

Figure 1 shows the grand average of CAEP of both groups HAG and ATG pre- and post-Auditory Musical Training associated with hearing aid adaptation.

Discussion

Auditory rehabilitation process involves several factors that can interfere with the successful hearing aid adaptation and the benefits obtained with hearing training programs. Among them, the time of hearing deprivation, adherence to the use of hearing aids, among other factors that influence each case toward a different prognosis and require careful evaluation by the involved professionals [19].

Considering these factors, it is important to initially reckon the characteristics of the study sample. The groups were homogeneous in relation to age, education level, score obtained on the MoCA instrument, time of hearing deprivation and average hours of using hearing aids daily. There are no significant differences between them. In general, most of the elderly participants in the study were between 60 and 70 years old, had good cognitive level, time of hearing deprivation of up to 5 years, and systematic hearing aid use.

Assuming that AEPs provides rich information for reasoning and understanding the neuroelectrophysiological processes that are part of auditory and linguistic information processing, this investigation chose to assess the CAEP. This measure investigates the detection, attention, discrimination and recognition of sound automatically, without the need for active patient participation, which minimizes the negative interference of factors related to age, such as memory and cognitive processes [20].

Some studies report LLAEP increased latency in the elderly [21, 22] when compared to young people and adults. However, in the present study, latency values ​​within the reference intervals were observed. Even though comparison with young patients was not performed, the elderly in both groups had good cognitive levels and time of hearing deprivation of up to five years. Another study showed that 2–5 year-time of hearing deprivation in individuals with mild or moderate sensorineural hearing loss did not influence the results of the long-latency auditory evoked potential [23]. Another study assessed N1 and P2 latencies in elderly people with hearing loss from 4KHz frequency and complaints of speech comprehension, and observed no increased latencies for these components [24].

The comparison between the measures obtained in the initial and final assessments between the HAG and ATG identified a positive effect of auditory training for the elderly in the ATG, with a significant decrease in the latency of the P3a component after hearing rehabilitation compared to the values ​​of the initial assessment. For the other components of the wave complex, a decrease in latency was observed in the final assessment in ATG, but no statistically significant differences.

When latency decreases are observed after interventions, we can understand that the time of processing the acoustic information by CANS was reduced [25, 26]. Specifically for the P3a component, the reduction in latency shows improvement in attention, acoustic recognition and auditory-linguistic association (secondary auditory cortex and associative areas) after the musical auditory training sessions.

The P3a component reflects the automatic process of attention and perception of the distinctive acoustic characteristics of the rare stimulus during the CAEP examination. Studies show that P3a and P3b have different neural generators, and that P3a originates from frontal attention mechanisms [27]. A study carried out using the Low-Resolution Electromagnetic Tomography technique showed that P3a generators are located in the cingulate areas, frontal and parietal regions [28].

Studies involving auditory evoked potentials describe decreased latencies as a neurophysiological correlate of neural plasticity [29, 30]. Changes in P3 latency were observed in other studies involving elderly people who only used hearing aids [11, 31, 32], unlike our study, which did not observe significant changes for HAG.

Other studies assessing the effects of AT with electrophysiological measures showed an improvement in the neural representation of speech in noise after training [12, 33]. These studies did not associate the use of hearing aids with auditory training.

Some studies report P3 amplitude increase after auditory training [32, 34]. In this study, an increase in P3a amplitude was observed after AT, with no statistically significant difference.

The amplitude represents the magnitude of electrical activity involved in performing a task. When an increase in amplitude after interventions is observed, it is understood that there was activation of synaptic activity and an improvement in processing quality. And related to the P3a component, it reflects this activation for the process of redirecting attention to the automatic detection of the relevant acoustic stimulus [35].

The present study analyzed the CAEP measurements in sound field, in order to assess the neural responses to binaural hearing, considering its importance for the ability to recognize speech in noise in elderly people and your auditory and communicative decline related to age.

The sample size can be considered a limiting factor to this study, whose initial proposal was to have more participants in the groups. However, such results aroused the researchers' interest in continuing the study to promote longitudinal assessments and to investigate long-term effects.

Conclusion

There was a change in the CAEP in elderly people with presbycusis in response to Musical Auditory Training associated with the use of hearing aids in elderly people with presbycusis. Thus, auditory rehabilitation proved to be effective in generating neural changes for attention, acoustic recognition and auditory-linguistic association.

Declarations

ACKNOWLEDGMENTS

Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES).

Katya Guglielmi Marcondes Freire for granting access to the program Treinamento Musical Auditivo®.

AUTHOR CONTRIBUTIONS 

YBA carried out the conception and design of the study, analysis and interpretation of data; ATLC assisted in the design and development of the study and corrections to the article; EFBC analysed the results; WWFC assisted in the development, writing and review of the article; KRL assisted in the development of the article as well as data analysis; ACFF advisor of the project that conceived the proposal, assisted in the design and development of the study and corrections for the article. All authors reviewed the manuscript. 

DECLARATION OF INTEREST STATEMENT

There are no conflicts of interest.

FUNDING DETAILS

This study was financed in part by the Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES) - Finance Code 001.

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