Influence of auditory-based cognitive training on auditory resolution, executive function, and working memory skills in individuals with mild cognitive impairment – a pilot randomized controlled study

Introduction

Aging is a natural process that affects people, causing a decline in cognitive and sensory abilities.¹ Aging leads to degenerative changes in the auditory structures and functions in older adults above 65 years, resulting in Presbycusis or Age-Related Hearing Loss (ARHL). Around 65% of adults above 60 experience this hearing loss, with the prevalence rate increasing from 15.4% among older adults above 60 to 58.2% among older adults above 90.² ARHL is caused by the loss of sensory cells and degenerative changes in the central auditory nervous system.³ Another common condition that affects older adults is mild cognitive impairment (MCI). MCI is characterized by a decline in memory, attention, and cognitive function,⁴ and it is a precursor of dementia, especially if it is an amnestic type.⁵ ARHL makes it difficult to perceive speech, particularly in noisy environments, and can lead to a decline in cognitive function.^6,7 MCI can exacerbate speech perception problems.^8,9 Therapeutic management or training addressing sensory, cognitive, and learning issues may slow down or lessen the impact of aging.

Auditory and cognitive training are important components of rehabilitation for both healthy and aging populations, including those with disorders. Auditory training actively involves the trainees distinguishing the sounds presented systematically.¹⁰ Although auditory training was initially used to enhance sensory refinement of speech sounds (bottom-up), literature shows it can also be beneficial for top-down processes, which are important for listening, especially in challenging conditions.^11,12 Cognitive training involves using standardized tasks that are cognitively challenging to improve an individual’s cognitive functions.¹³ Studies have shown that cognitive interventions effectively enhance the cognitive function of older adults with Mild Cognitive Impairment (MCI).^14–16 They also improve auditory and cognitive functions, enhancing speech perception in various situations.^17,18

Many people have shown interest in exploring this type of training to alleviate cognitive and perceptual impairments.¹¹ In 2009, Smith conducted cognitive training sessions for older adults with normal cognitive function and observed improved auditory memory and attention.¹⁹ Similarly, Yusof et al. (2019) examined the benefits of auditory-cognitive training among older adults with and without neurocognitive impairment.²⁰ Participants were trained in auditory perception, such as word and sentence recognition in noise, and auditory-cognitive tasks, such as word span, word order, and word position. Though both groups benefited from the training, improvement was more noticeable among individuals with normal cognitive functions in various domains. Similarly, in 2014 Avila and her colleagues studied the effectiveness of auditory training on the auditory and cognitive skills of older adults with Mild Cognitive Impairment. The training stimulated auditory skills such as auditory memory, selective attention, figure-ground, temporal processing, auditory closure, and binaural integration. The training resulted in the improvement of auditory skills but did not generalize to cognitive skills.²¹

A recent study by Kawata et al. (2022) investigated the benefits of auditory and cognitive training in healthy older adults.²² They provided auditory-cognitive training (ACT), auditory training (AT), and cognitive training (CT). The results indicated that the ACT group exhibited significant differences in brain structure changes compared to the other groups. It is worth noting that the study had a limitation in that it relied solely on pure tone audiometry as an auditory measure.

Murphy et al. (2011) conducted a study on the effectiveness of auditory training in an adult who had suffered a traumatic brain injury. The patient had difficulties with auditory processing and cognitive skills such as temporal processing, verbal memory, working memory, and verbal fluency. The auditory training not only enhanced auditory skills but also led to improvements in central processes (top-down processing), which consequently had a positive impact on cognitive abilities as well. Both auditory and cognitive training can strengthen neural pathways and circuits through training, leading to improved auditory perception and cognitive abilities.²³ Therefore, actively involving older adults in such training can bring about changes in the brain, ultimately enhancing their auditory and cognitive functions.

Numerous studies have demonstrated that cognitive interventions can enhance the quality of life in older adults with and without Mild Cognitive Impairment MCI.^24–26 However, there is a dearth of literature on auditory-based cognitive training, and the few existing studies have varying participant selection, training materials, and assessment measures. One study evaluated auditory-based cognitive measures alongside auditory cognitive training, but they used pure tone audiometry as an outcome measure, which is a peripheral test considered to be less influenced by cognitive function.²⁰ Therefore, the current study was designed to evaluate the impact of auditory-based cognitive training on auditory processing skills and cognitive abilities of older adults with cognitive impairment.

Methods

Cognitive measures

The study assessed the cognitive abilities of the participants using the Neurocognitive Toolbox (ICMR-NCTB), which The Indian Council of Medical Research developed. For this study, two tests from the toolbox were considered: the Trail Making Test (TMT) and the Verbal Learning Test. The TMT (Black & White) evaluates a person’s executive function through two segments: TMT Part A and TMT Part B. In TMT Part A, the participant must draw a line sequentially connecting 25 numbered circles on a page as quickly as possible. In TMT Part B, the participant must connect circles while alternating between numbers and circles in two colors, black and white. The TMT Part B is more challenging and takes longer time than TMT Part A. Both parts are timed, and the time taken to complete the task is recorded as the response. The difference in time to complete the task between Part A and Part B estimates the person’s executive function index (Part B-A).

The Verbal Learning Test measures the participants’ episodic memory and records their immediate and delayed recall and recognition memory. The test presents a set of ten unrelated words orally to the participants over three trials. After each trial, the participants are asked to recall the words immediately in any order, and their responses are recorded. After 20 minutes, the participants are asked to recall the set of 10 words and identify the 10 words from a list of similar words. A diagram of participant flow is shown in Figure 1.

Figure 1. Participant flow diagram.

Results

During the study period, out of 43 participants who were assessed for eligibility, 22 of them were enrolled in the study. All 11 participants in the experimental group completed the training, and their data was included in the analysis. The statistical analysis indicated no significant differences in baseline assessments between the control and experimental groups for most outcome measures, except for TMT Part B-A ( Table 1). Table 2 presents the mean and SD values for auditory resolution tasks, TMT, and DR outcome measures. The study found that AbCT was effective in three outcome measures: MD, TMT-B, and TMT B-A. The MD task showed a significant main effect of group versus time interaction (p=0.038). However, no significant main effect was observed for either group (p=0.497) or time (p=0.186). No significant main effect of time, group, or interaction between time and group was found for the FD and GDT tasks.

For the TMT-A task, there were no significant differences in time (p=0.164), group (p=0.733), and the interaction between group and time (p=0.196). However, significant main effects of time and group versus time interaction were observed in Part B and Part B-A, respectively, while the group effect was insignificant. There was a significant difference in the delayed recall tasks over time (p<0.001), but not between groups (p=0.525) or group versus time (p=0.575).

Post hoc analysis revealed a significant score difference between baseline-follow-up and post-follow-up in the Modulation Detection task. Furthermore, TMT-B and TMT B-A had statistically significant differences (p=0.023) during the TMT in the baseline-post and baseline-follow-up conditions.

Discussion

This study aimed to investigate the benefits of AbCT in improving auditory processing and cognitive functions among older adults with mild cognitive impairment. The results revealed that AbCT positively impacted MD function, but no significant improvements were observed in FD and GDT. Similarly, TMT-B (executive function) showed significant differences compared to TMT-A and DR.

The positive impact of AbCT can be explained by two mechanisms involved in auditory processing. The first mechanism is the neurocognitive mechanism of acoustic signals, which discriminates and recognizes specific functions. The second mechanism is the attentional process, involving phenomena such as attention and memory.²³ Anderson et al. (2013) conducted a study to evaluate the effect of auditory training with six modules designed to increase the speed and accuracy of auditory processing cognitive training on the temporal precision of subcortical speech processing in noise using frequency following response (FFR).¹⁷ They observed that the trained group exhibited faster neural timing and experienced improvements in memory, processing speed, and speech-in-noise perception compared to the control group. Song et al. (2012) investigated training-related malleability using a program that included cognitive based listening exercises to enhance speech-in-noise perception.²⁸ The trained individuals showed significant improvements in speech-in-noise perception, sustained even after six months of training. The subcortical responses in noise showed enhancements in the encoding of pitch-related cues, particularly for the time-varying portion of the syllable most susceptible to perceptual disruption. Similarly, Carcagno and Plack (2011) observed that the robustness of FFR neural phase locking to the sound envelope increased significantly more in trained individuals (pitch contour training) than in the control group.²⁹ These studies support the neurocognitive process and suggest that auditory cognitive training, or AbCT, can improve auditory processing.

Attentional processes and working memory are crucial in speech perception, especially in the presence of background noise. A study by Wong et al. (2010) found that activity in the prefrontal cortex and regions associated with memory and attention in speech perception in noisy environments increased, indicating that cognitive compensation may play a crucial role in aiding hearing in noisy environments and that the recruitment of general cognitive areas accompanies declines in sensory processing.³⁰ Similarly, O’Brien et al. (2017) provided auditory cognitive training (Brain fitness) to healthy older adults and observed that a P3b event-related potentials amplitude, latency, and P1-N1-P2 complex significantly improved post-training. However, no advantage was found in auditory perceptual processing.³¹ Studies have shown that P3b originates from temporal-parietal activity associated with attention and appears related to subsequent memory processing.³² Therefore, our study emphasized that AbCT could improve the efficiency of attention allocation and working memory, which might explain the training-related changes in the auditory processing and neurocognitive processes.

The differences in performance between the GDT and TMTF tests may be due to the sensitivity and reliability of the training and testing methods. A study by Yusof et al. (2019) investigated the impact of auditory-cognitive training on older adults with normal cognitive function and neurocognitive impairment.²⁰ They found that there was an improvement in some auditory measures such as HINT (quiet), GIN, PPST (humming), and DDT but not in HINT (Composite) and PPST (verbal) for both normal cognitive (NC) and neurocognitive impairment (NCI) groups. Additionally, they observed that the NC group showed more significant improvements than the NCI group, suggesting a higher potential for learning among NC participants. Furthermore, Shen (2014) reported no correlation between GDT and TMTF, and that age and hearing status had no impact on the tests. However, TMTF sensitivity improved as hearing thresholds decreased and worsened with age.³³

The other finding of our study revealed that the AbCT training positively impacted central executive function and attention, as indicated by a significant improvement in TMT-B and TMT B-A, while TMT-A and DR remained unaffected. This suggests that the training primarily influenced cognitive abilities related to attention and executive function rather than psychomotor skills or working memory. This observation agrees with the study by Kawata et al. (2022). They compared four groups - an auditory cognitive training group, an auditory training group, a cognitive training group, and a control group. The results showed that the auditory cognitive training group demonstrated more significant changes in regional gray matter volume in several brain regions than the other groups. The auditory training group significantly improved auditory measures and increased regional gray matter volume and functional connectivity (FC) in the left temporal pole.²² These observations suggest there exists a functional connectivity between the auditory and cognitive processes. Therefore, auditory and cognitive training can improve cognitive and auditory skills in healthy older adults. However, they used a pure tone audiometer as an outcome measure that was less influenced by cognitive and auditory training. A study by Ruscheweyh et al. (2013) reported that executive function is related to regional gray matter volume, also a biomarker, in healthy older individuals.^34,35 These studies justify the improvement in executive function. Given the significant differences observed at baseline for TMT Part B-A, post training significance should be interpreted cautiously before generalizing. No significant difference in digit recall could be attributed to the persistence of benefits for speed of processing/auditory processing but not for memory, which is consistent with the findings of Borella et al. (2010), who showed that older adults maintained training enhancements for fluid intelligence and speed of processing but not for memory.³⁶

The current study results evaluated the potential of AbCT on the auditory and cognitive skills of older adults with MCI. However, these findings may not be generalized to a wider population due to several concerns. First, the relatively smaller sample size and the absence of electrophysiological tests, which are considered the highest level of evidence for assessing training-related benefits. Second, the characteristics of the participants involved in the study, where recruitment was based on MoCA screening rather than clinical diagnosis of MCI, may have influenced the results. This is mainly due to challenges in obtaining consent from the participants to undergo detailed cognitive and audiological assessment due to practical issues, less motivation, and family consent. Additionally, the number and duration of the training sessions were determined based on a literature search. An interventional study recommended an optimal dose of 12 to 14 sessions for cognitive training and 15 to 20 sessions for multidomain training. Variations in the individual characteristics of the participants were also observed in the study, which directly impacted the optimal dose and dose-response functions.³⁷

The secondary concern is that the heterogeneity of the MCI population makes it challenging to apply the findings broadly. Though all the participants were recruited based on the cut off score of MCI, their performance on the auditory, cognitive and baseline assessment before training were highly variable. Participants in this study performed slightly poorer in digit span tasks (forward and backward) when compared to a normative data obtained from older adults with MCI.³⁸ Including an active control group in this study would have eliminated the possibility of a placebo effect in the experimental group. Additionally, various factors, such as participant motivation and health condition on the day of assessment, could have influenced their performance. Furthermore, the literature supports the absence of evidence indicating differences between the active and passive control groups in cognitive interventions.³⁹ We also observed significant variability in the baseline data of the experimental and control groups, which we tried addressing using linear mixed models for statistical analysis, accounting for unbalanced data. As this was a preliminary study, future randomized controlled trials (RCTs) must consider these variations and address these limitations.

Conclusion

This current preliminary study suggests that AbCT seems to restore age-related deficits in temporal processing in the brain, promoting better cognitive and perceptual skills, particularly in older adults with MCI. The results also suggest that auditory temporal skills could be adaptable and can be a favorable prognostic indicator. However, further research in this area is warranted with a large sample size to determine whether such auditory cognitive training can change auditory and cognitive functions.

Ethics and consent

This study protocol was reviewed and approved by the Institutional Ethics Committee, Kasturba Hospital, Manipal (IEC 704/2017) on 15.11.2017, and the Clinical Trials Registry of India (CTRI/2019/01/017073). Written informed consent was obtained from all the participants who participated in this study.