Auditory training for tinnitus treatment: a scoping review

Highlights • Auditory training for tinnitus is studied as an auditory rehabilitation strategy.• There is still no consensus on the best practice methodology.• There is a need for further high-level studies in this area.• Auditory discrimination training was the most studied type.• Considering attentional factors and multisensory paths may lead to future research.


Introduction
Auditory perception of sound in the absence of corresponding external stimuli is described as tinnitus.Factors that affect auditory health can lead to this symptom.Underlying mechanisms are still being studied and include abnormal synchronous neural activity throughout auditory pathway, increasing rates of spontaneous neural discharges in the auditory cortex and subcortical structures, and modifications in the auditory cortex's tonotopic representation maps. 1---3t is estimated that 10%---15% of the general population presents tinnitus. 4,5In 20% of these, the symptom negatively impacts quality of life, impairing aspects related to sleep, communication, concentration, and social interaction.It is associated with anxiety, irritability, stress, and depression. 5 populational study conducted in the city of São Paulo found a 22% prevalence of tinnitus, occurring mostly in females and with advancing age. 6ny abnormality that can damage the auditory pathways, various non-auditory conditions, and organic statuses can generate tinnitus. 7Hearing loss is related to tinnitus in about 90% of the cases, and hyperacusis may occur in 25%---40%. 4Tinnitus is associated with dizziness in cases of Ménière's disease 8 and other conditions that simultaneously affect the auditory and vestibular systems. 9here is a continuous effort to find alternatives in tinnitus auditory rehabilitation, addressing its heterogeneity of causes and manifestations. 3,10Treatment is still challenging in some cases, there is no single and exclusive path for everyone, regarding not only drug therapies or medical procedures but also approaches that involve complementary disciplines.
A systematic review of the existing guidelines to assess and treat tinnitus in adults revealed a consensus in the recommendation of audiological assessments and validated self-assessment questionnaires to investigate stress or suffering generated by the symptom.Documents recommended educational interventions for tinnitus and hearing aids for those with hearing loss. 11und therapy uses sound stimulation to promote reorganization of the cortex attempting to relieve tinnitus.It has numerous approaches, such as hearing aids and sound generators combined when tinnitus is accompanied by hearing loss, masking to reduce the audibility of tinnitus totally or partially, 10 and various potential mechanisms of effect, as habituation 12 and gain reduction. 3Customized sound therapy uses a tinnitus management strategy based on the individual's tinnitus symptoms.Active discrimination training tasks are another form of pitch-based therapy. 3,13uditory training strategies have been used as possible tools in the treatment of perceptual relief from tinnitus. 10A previous systematic review investigated the efficacy of auditory perceptual training for tinnitus treatment and revealed the necessity of higher quality evidence on the topic. 13It has been thirteen years since this publication, therefore new evidence on auditory training for tinnitus treatment should be investigated.
The question that motivated the present study was: ''What is the evidence of auditory training employed in the audiological treatment of tinnitus in adults and older adults?''.

Methods
This scoping review followed the quality parameters of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR). 14Its protocol was published in the Open Science Framework (OSF) under DOI 10.17605/OSF.IO/P9GFY.

Eligibility criteria
Studies were selected based on the criteria described in Table 1.

Search
Terms from the Medical Subject Heading (MeSH) vocabulary and free terms were used (Table 2), search was conducted   15 Sample was selected by convenience, including all studies that met the inclusion criteria.

Selection of sources of evidence
Rayyan QCRI was used to select studies and identify duplicates, in a three-stage process, as described in Fig. 1.

Data extraction
Data were extracted with an instrument developed for the study and categorized according to the CASP recommendation. 16Results were described and summarized according to the objectives of this review and qualitatively assessed based on the Critically Appraised Topics (CAT), which makes critical analyses of the level of evidence of selected articles. 17he instrument informs the study design when it is not explicitly reported by the authors and establishes the studies' level of reliability, considering methodological adequacy (Table 3) and methodological quality (strengths and weaknesses of the study).Studies' level of reliability was classified into very high (Level A+), high (Level A), moderate (Level B), limited (Level C), low (Level D), or very low (Level D−).

Results
A total of 2160 articles were identified in databases, 189 duplicates were excluded, leaving 1971 articles, whose titles

Study design Level
Systematic review or meta-analysis of randomized controlled studies AA Systematic review or meta-analysis of non-randomized controlled and/or before-after studies A Randomized controlled study Systematic review or meta-analysis of controlled studies without a pretest or uncontrolled study with a pretest B Non-randomized controlled before-after study Interrupted time series Systematic review or meta-analysis of cross-sectional studies C Controlled study without a pretest or uncontrolled study with a pretest Cross-sectional study (survey) D Case studies, case reports, traditional literature reviews, theoretical papers D− and abstracts were read.Then, 1956 articles were excluded for not meeting the eligibility criteria, leaving 15 selected papers.These articles were read in full, and three of them were excluded for not meeting the eligibility criteria, leaving 12 articles to be included in this review.The references were hand-searched, and three additional articles were found that met the eligibility criteria, totaling 15 articles.Fig. 2 shows the selection process.Studies included were published between 2004 and 2022, from New Zealand, Spain, the United Kingdom, Germany, Brazil, Canada, and Australia.Studies were described in detail and categorized as follows: author/date, study design, level (according to qualitative analysis with CAT), sample characterization, auditory training tasks, sound stimuli, outcome measures, and study results (Table 4).Studies and auditory training's main features were described in Table 5.
A review produced by Hoare et al. 13 encompassed studies with active hearing tasks of various kinds and diverging stimuli.The study by Searchfield et al. associated multisensory perceptual training with drug therapy to verify whether the drug would enhance the effects of training. 24Searchfield and Sanders 25 used attentional auditory training with stimulus to move attention away from tinnitus in auditory space and to attend to different locations or sounds responding to prompts.Eight studies 18,21,23,24,26,28---30 reported statistically significant improvements in at least one of the outcome measures.Four studies 19,20,22,25 did not find statistically significant effects of the auditory training.Tinnitus Handicap Questionnaire (THI) was the tool with the most changes in post-intervention administration, 18,28,31 followed by attentional skill tests, 21,23 Tinnitus Functional Index (TFI), 21,30 VAS, 26,27 and Client Oriented Scale of Improvement in Tinnitus (COSIT). 25mprovement after auditory training was reported in tinnitus classification scales 24 and queries developed by the authors, 18,26,27 as well as greater intrinsic motivation to train in interactive game platforms. 20One study mentioned a decrease in psychoacoustic measures of loudness and Minimum Masking Level (MML) after auditory training. 29oare et al. 19 observed generalized benefits after auditory training, which could not be ascribed to a specific stimulus or auditory training program.Searchfield et al., 24 using functional imaging, verified changes in the connectivity pattern of the sensory and attentional neural networks after multisensory perceptual training, with no additional effect due to medication.
Frequency discrimination training was the type of auditory training with the most changes in the outcome measures, 18,26---28 followed by selective auditory attentional training, 23,25,29,30 localization, 25,29,30 and multisensory attentional training, which involved auditory, tactile, and visual stimuli. 21erraiz et al. 31 presented the essentials of frequency discrimination training as a treatment for tinnitus.Frequency discrimination training could partially reverse changes in tonotopic representation due to peripheral damage and improve tinnitus, making it a new therapeutic option to be developed.
A systematic review 13 verified low to moderate evidence quality levels on auditory training interventions studies.Few randomized controlled clinical trials provided impartial and generalizable evidence, which would prove that the perceptual auditory training had a relevant clinical effect on tinnitus.
Our research shows new studies focused on the topic 19---25,30 after this review and quality of evidence improvement since the majority were randomized controlled trials, 9,20---25 high-quality evidence level (A).Studies published after 2010 included procedures that ranged

Discussion
Auditory-perceptual training can be defined as the auditory nervous system learning to hear with the active involvement of sounds, in which listeners learn to make certain distinctions in what they systematically hear. 32The auditory system is reorganized in response to changes in auditory input.This system is responsible for a complex mechanism composed of distributed nervous networks that integrate to represent auditory stimuli, due to auditory system plasticity. 33he term ''sound therapy'' has been generally and indiscriminately used to refer to the use of any sound in tinnitus treatment.However, the interaction mechanisms between input sound and tinnitus are heterogeneous, which is why maskers, hearing aids, and other stimulations are used with different sound changes, which are described in the literature to treat tinnitus. 10r study defined the patients' active participation as one of the inclusion criteria to investigate the evidence of auditory training as a therapeutic strategy for tinnitus.There are other audiological approaches to treat tinnitus that involve passive sound stimulation, more suitable to sound therapy strategies, rather than auditory training.Auditory training involves active listening to various auditory stimuli to improve auditory skills and trigger neuroplasticity. 34uditory rehabilitation may cause changes in the auditory system, leading to brain reorganization mechanisms, affecting auditory performance as well. 35Perceptual learning effects are accompanied by neural plasticity in the brainstem and cortex.Inferior colliculus plays an important role in auditory learning.Auditory system plasticity effectively occurs in young adults.In older adults, this brain mechanism is also present, with change possibilities associated with improved communication in challenging hearing situations. 36uration and frequency of auditory training varied in the selected studies.Except for one study, which conducted one 40-min session a week (totaling 8 weeks) of auditory training in a sound booth, 22 all other studies had at least five sessions a week.Daily training sessions were the most used frequency.The minimum stimulation time per day was 20 min, for 15---30 days.Almost all studies with daily auditory training sessions reported significant benefits demonstrated in at least one outcome measure. 18,21,23,24,26---29Searchfield and Sanders 25 did not find statistical differences, but results showed clinical effects of intervention.
Learning mechanisms must be established for auditory training to have relevant effects on increased neural plasticity and consequent changes in this system.Auditory training increases the area of cortical representation, changing these areas of the central nervous system regarding certain stimuli. 35he period of stimulation may have an impact on plastic changes, influenced by the time and frequency of training to which the subject is exposed.In our study, daily training proved to be more effective in the auditory training of subjects with tinnitus, regardless of the time of stimulation, which ranged from 15 to 30 days.
Based on the hypothesis that selective serotoninreuptake inhibitors could potentialize cortical plasticity in adults, use of fluoxetine was combined with the training strategy; however, there was no additional effect related to the drug administration along with training. 24innitus is strongly associated with symptoms of anxiety and depression.Severity of tinnitus and the subjects' predisposition to develop anxiety and depression are important factors that influence this association. 37Only three papers 21,24,28 investigated anxiety and depression symptoms in their outcome measures and there was no statistically significant difference in these measures before and after training.
Psychoacoustic measures can determine the perception characteristics in tinnitus frequency (pitch) and intensity (loudness) and verify the possibility of masking and its post-masking suppression, as in the assessment of residual inhibition effect, confirming that these sounds interact with the mechanism that generates tinnitus. 37hree studies 19,23,29 used psychoacoustic measures to assess tinnitus as outcome measures, establishing tinnitus pitch and loudness 19,29 and MML. 29,30MML was the only psychoacoustic measure that showed a statistical difference after the auditory training intervention. 29Modulating tinnitus with acoustic stimulation, as in tests that assess MML and tinnitus residual inhibition, may furnish prognostic data on the long-term effects of the treatments involving auditory stimulation. 38here is methodological variability in the clinical and scientific psychoacoustic measures assessment protocols. 39The lack of standardized protocols hinders comparisons and may lead to diversified findings in the measures.
Auditory Discrimination Training (ADT) was described in the literature based on the capacity to change brain tonotopic representation due to central nervous system plasticity.There is no consensus on the frequencies used as stimuli to obtain the best results in terms of relief from tinnitus perception.Studies considered hearing loss' frequency range, tinnitus pitch, or the tinnitus spectrum to define the stimuli used inside or outside these ranges.
In the present study, frequency discrimination was the type of auditory training that showed the most changes in outcome measures. 18,26---28Lack of standardization in tinnitus pitch mapping techniques proved to be a critical factor in treatments based on this measure, which can make some therapies unfeasible. 20Lack of consensus on the most effective strategy for sound stimuli, whose frequencies are or are not close to the one that corresponds to the tinnitus pitch, may complicate the procedures in ADT. 10 It was supposed that some widespread benefits from this approach should be related to other mechanisms such as selective attention or emotional state. 19ssessing auditory training methods for patients with tinnitus that used attentional auditory skill stimulation, 22,23,25,29,30 only two of them 22,25 did not have statistically significant results in their outcome measures.However, the first one used a standard auditory training program for central auditory processing disorders that stimulated auditory skills in general 22 and the other had clinically significant changes in the intervention that include the training. 25Other three studies with specific strategies aimed at tinnitus found improvements in at least one outcome measure. 23,29,30ubjects with tinnitus and normal hearing performed worse in tasks involving auditory attention skills and tinnitus might be associated with low performance in selective and sustained auditory attention. 40Attentional auditory skills stimulation may be an interesting path to be explored in future research addressing audiological therapeutic management of tinnitus, adapting, and customizing it to issues involved in processes underlying tinnitus considering current scientific understanding.
Considering that the consequences of tinnitus to the central nervous system would involve plastic reorganization encompassing auditory and non-auditory areas of the brain and that multisensory perceptual learning is usually more consistent than unimodal learning, multisensory training combined multimodal stimuli as a tinnitus treatment method. 21Also, combined therapeutic strategies like auditory attentional training, counseling, and passive auditory stimulation were developed aiming to modify tinnitusrelated neural networks. 24n the present study, two papers applied multisensory stimulation, combining auditory, tactile, and visual stimuli.There was a limited though statistically significant improvement in the subjective measures of tinnitus in the population studied, showing that multisensory attention training may be an effective tool to manage tinnitus. 21Resting-state functional magnetic resonance imaging found neuroplastic changes in neural connectivity after multisensory perceptual training, which showed the involvement of auditory and nonauditory cortical and subcortical areas in subjective chronic tinnitus. 24uditory training programs are often available on game platforms and need to be interesting enough to ensure the patients' adherence.An advantage of computerized programs is that it facilitates training at home while hearing health professionals are regularly visited to monitor the effects of training. 34In our review, seven studies 19---21,23,24,28,30 used computer-based auditory training in patients with tinnitus and one developed an app that provides auditory attentional training combined with other strategies. 25One study verified greater intrinsic motivation with the interactive game platform. 20he CAT methodological qualitative assessment classified the papers included in our results into varying reliability levels, ranging from very low (55%) to high (90%).Eight ran-domized controlled studies 18---25 obtained Level A in study design analysis and high reliability.
The studies that used auditory discrimination training 18---20,26---28,31 and attentional auditory skill stimulation 22,23,29,30 applied to tinnitus patients obtained quality evidence levels ranging from limited to high (C---A) whereas the studies that applied multisensory training 21,24 or attentional auditory training combined with passive listening and counseling 25 in tinnitus subjects got a high-quality evidence level (A).
A systematic review conducted on the topic in 2010 found a scarcity of randomized controlled clinical trials, whose levels of evidence ranged from low to moderate. 13There has been a positive qualitative change over the years in publications involving auditory training in patients with tinnitus, as there are currently more studies with higher methodological levels.
Our results revealed frequency discrimination training was the most studied auditory discrimination training type applied to tinnitus patients.However, most of the studies on this topic are dated before 2010.Further research incorporated other methodologies at the study design.The scientific work seems to get the other hand and the latest publications have considered attentional factors and multisensory paths, that can be correlated to tinnitus physiopathology, at the training program activities.
Most papers in the literature (which seek to customize the protocols used in tinnitus treatment with sounds) considered a specific dimension ---e.g., using tinnitus pitch as a reference measure ---to individually adapt tinnitus treatment, disregarding the complex combination of different dimensions in tinnitus.Therapy customization and planning tools should be included and assessed when treating such patients. 10lthough the quality of the studies improved in the last decade, a great challenge in auditory training for tinnitus treatment is to carry out methodologically replicable research.There is currently no predefined way for the auditory treatment of subjects with tinnitus aiming to improve the perception of the symptom and relieve the discomfort related to it.Another challenge is the number of research participants.Treatment takes time and the participants' active participation; hence, longitudinal follow-up with a significant sample and a consistent effect size has not yet been accomplished.
Along with these factors, methodological heterogeneity in the outcome measures is an issue that reflects current audiological assessment in the field.There are various nonhomogeneous protocols, including in the methodology of the subjective tests used as tinnitus audiological assessment instruments.
Studies are not yet comprehensive, with limited samples and variable methodologies.This hinders the comparison of auditory training effects and generalization of the results to the general population with tinnitus, which would validate their clinical applicability.

Conclusion
Auditory discrimination training was the most studied approach.Recent studies had higher levels of evidence and considered attentional factors and multisensory pathways in auditory training strategies.Further large-scale research is necessary, using adapted strategies directed to the topic, considering current scientific knowledge.

Figure 1
Figure 1 Three-stage process for selection of sources of evidence.

Figure 2
Figure 2 Flowchart of the results.

Table 1
Eligibility criteria.Inclusion criteriaTypes of participants: adults and older adults with tinnitus (older than 18-years); types of intervention: auditory training in patients with tinnitus, with the patient's active participation, either alone or in combination with other interventions and stimulation modalities; types of study: experimental, quasi-experimental or observational studies in English, Portuguese, and Spanish, encompassing: cross-over studies, ecological studies, longitudinal studies, randomized and non-randomized clinical trials, before-and-after studies, case-control studies, cohort studies, and case series.Besides these, systematic reviews were also considered.No publication date limit was set to retrieve articles.Exclusion criteriaStudies addressing tinnitus without the therapeutic approach studied, papers exclusively on other therapeutic interventions, and studies that were not available in the database and/or in full text.

Table 2
Search strategy in the databases.

Table 3
Classification of methodological adequacy used in the Critically Appraised Topics.

Table 4
Description of the studies included in the review.

Table 5
Main features of auditory training for tinnitus patients' studies and strategies.