Acessibilidade / Reportar erro

Cortical Reorganization Following Psychoeducational Counselling and Residual Inhibition Therapy (RIT) in Individuals with Tinnitus

Abstract

Introduction

Psychoeducational counselling and residual inhibition therapy (RIT) are traditional approaches used in many clinics to manage tinnitus. However, neurophysiological studies to evaluate posttreatment perceptual and functional cortical changes in humans are scarce.

Objectives

The present study aims to explore whether cortical auditory-evoked potentials (CAEPs; N1 and P3) reflect the effect of modified RIT and psychoeducational counselling, and whether there is a correlation between the behavioral and electrophysiological measures.

Methods

Ten participants with continuous and bothersome tinnitus underwent a session of psychoeducational counselling and modified RIT. Perceptual measures and CAEPs were recorded pre- and posttreatment. Further, the posttreatment measures were compared with age and gender-matched historical control groups.

Results

Subjectively, 80% of the participants reported a reduction in the loudness of their tinnitus. Objectively, there wasasignificant reductioninthe posttreatment amplitude of N1 and P3, with no alterations in latency. There was no correlation between the perceived difference in tinnitus loudness and the difference in P3 amplitude (at Pz).

Conclusion

The perceptual and functional (as evidenced by sensory, N1, and cognitive, P3 reduction) changes after a single session of RIT and psychoeducational counselling are suggestive of plastic changes at the cortical level. The current study serves as preliminary evidence that event-related potentials (ERPs) can be used to quantify the physiological changes that occur after the intervention for tinnitus.

Keywords
residual inhibition therapy; tinnitus; psychoeducational counselling; treatment; cortical reorganization

Highlights

A single session of modified RIT and psychoeducational counselling can bring about perceptual and functional changes at the cortical level.

Event-related potentials (ERPs) may serve as a tool to quantify functional changes after tinnitus treatment.

Introduction

Tinnitus is a heterogeneous condition prevalent across the globe. It affects approximately one in ten adults.11 Bhatt IS. Prevalence of and risk factors for tinnitus and tinnitus-related handicap in a college-aged population. Ear Hear 2018;39 (03):517–26 The diverse causes of tinnitus make itdifficult to narrow downtoa single mechanism. A variety of mechanisms targeting the auditory periphery to the central level has been postulated. A definitive cure for tinnitus is still a pipe dream for researchers worldwide. Traditional management techniques aim at either eliminating tinnitus or reducing the individual’s response to it.22 English K. Counseling in audiologic practice: Helping patients and families adjust to hearing loss. 2005 These methods include tinnitus retraining therapy (TRT), cognitive behavioral therapy (CBT), sound therapy, neuromodulation, relaxation therapy, educational counselling, residual inhibition therapy (RIT), yoga etc.

Counselling, a cornerstone in tinnitus treatment, will empower individuals to de-attend to their tinnitus and eventuallyget habituatedtoit.33 Searchfield GD, Magnusson J, Shakes G, Biesinger E, Kong O. Counseling and psycho-education for tinnitus management. In: Textbook of tinnitus. Springer; 2011:535–556 There is a strong relationship between tinnitus and psychological symptoms like anxiety, distress, and depression, which highlights the importance of a psychoeducational approach in counselling. The more knowledge an individual holds about his or her condition, the better the therapeutic outcomes.44 Lukens EP, McFarlane WR. Psychoeducation as Evidence-Based Practice: Considerations for Practice, Research, and Policy. Brief Treat Crisis Interv 2004;4(03):205–225 Psychoeducational counselling aids in correcting maladaptive thoughts and behaviors by exploring the problem and clarifying the purpose and expected outcome of the intervention.55 Tyler RS, Noble W, Preece JP, Dunn CC, Witt SA. Psychological treatments for tinnitus. Tinnitus: Theory and Management 2004: 314–323 Education alone may be sufficient for some individuals. However, for some individuals an education on tinnitus solely can be sufficient.66 Henry JL, Wilson PH. The psychological management of tinnitus: comparison of a combined cognitive educational program, education alone and a waiting-list control. Int Tinnitus J 1996;2:9–20,77 Kröner-Herwig B, Frenzel A, Fritsche G, Schilkowsky G, Esser G. The management of chronic tinnitus: comparison of an outpatient cognitive-behavioral group training to minimal-contact interventions. J Psychosom Res 2003;54(04):381–389

A renowned and commonly used therapy in many clinics, RIT involves the use of external noise to alter the patients’ perception or reaction to tinnitus. Residual inhibition (RI, proposed by James Spalding in 1903) is a phenomenon in which there is a temporary quieting of the tinnitus after listening to a trigger sound. Acoustic stimulation can be provided using a variety of stimuli ranging from white noise, pure tones or noise that match an individuals tinnitus frequency, notched noise and filtered music. The effect of RI can last from a second to several hours, depending on the duration of the masking sound.88 Hazell JW, Wood S. Tinnitus masking-a significant contribution to tinnitus management. Br J Audiol 1981;15(04):223–230,99 Terry AM, Jones DM, Davis BR, Slater R. Parametric studies of tinnitus masking and residual inhibition. Br J Audiol 1983;17(04): 245–256 Temporary suppression/desensitization of neuronal excitation1010 Dessai TD, Gopinath R, Krishnan L, Susan G. Effectiveness of residual inhibition therapy. Int Tinnitus J 2014;19(01):63–67 and the action of metabotropic glutamate receptors (mGluRs) in inferior colliculus (IC) neurons1111 Voytenko SV, Galazyuk AV. mGluRs modulate neuronal firing in the auditory midbrain. Neurosci Lett 2011;492(03):145–149 have been postulated as underlying reasons for the effectiveness of RI. However, the neural mechanism underlying RI and its neurophysiological correlates in humans are yet to be completely understood. Approximately 80% of individuals suffering from tinnitus are known to have some degree of RI,1212 Roberts LE, Moffat G, Bosnyak DJ. Residual inhibition functions in relation to tinnitus spectra and auditory threshold shift. Acta Otolaryngol Suppl 2006;126(556):27–33,1313 Vernon JA, Meikle MB. Tinnitus: clinical measurement. Otolaryngol Clin North Am 2003;36(02):293–305,1414 Witchard C. Residual inhibition. In: 2013 which tends to last one minute on average. 1515 Roberts LE. Residual inhibition. Prog Brain Res 2007;166:487–495 However, there are also studies1010 Dessai TD, Gopinath R, Krishnan L, Susan G. Effectiveness of residual inhibition therapy. Int Tinnitus J 2014;19(01):63–67 that report contradictory findings, with either little or no improvement in tinnitus on any of their participants. The provision of RITusing frequency-specific narrow-band noise, at 10dBSL for 60 seconds, was questionable, and a modification in its paradigm has been suggested.1010 Dessai TD, Gopinath R, Krishnan L, Susan G. Effectiveness of residual inhibition therapy. Int Tinnitus J 2014;19(01):63–67 It has been shown that the duration, the intensity, and the sound spectrum used to induce RI influence its magnitude and duration.1616 Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13 Hence, in the present study, a modified RI paradigm was incorporated to intensify the treatment results.

The effectiveness of any tinnitus therapy can be determined by either subjective or objective measures. The most commonly-used subjective measures are questionnaires (such as the Tinnitus Handicap Inventory [THI], the Tinnitus Functional Index [TFI], and the Tinnitus Questionnaire [TQ]) and scales (such as the Likert scale and the Visual Analogue Scale [VAS]). They are mostly patient- or client-centered.

With cortical auditory-evoked potentials (CAEPs), on the other hand, physicians examine functional changes in the cortical processing using an external stimulus. The early waves or components peaking roughly within the first 200ms after the onset of the stimulus reflect the sensory processing, and are termed exogenous components (P1, N1, P2 and N2). Event-relatedpotentials (ERPs) generatedin later parts reflect the “cognitive” process, and are termed as “endogenous” ERPs (P3, N4 etc.). P3 is a cognitive potential that peaks around 250ms and 400ms poststimulus for most adults between 20 and 70 years of age. It has a topographic maximum distribution at frontoparietal regions linking to attention and memory processes.1717 Pfefferbaum A, Ford JM, Wenegrat BG, Roth WT, Kopell BS. Clinical application of the P3 component of event-related potentials.I. Normal aging. Electroencephalogr Clin Neurophysiol 1984;59(02):85–103,1818 Picton TW, Stuss DT, Champagne SC, Nelson RF. The effects of age on human event-related potentials. Psychophysiology 1984;21 (03):312–325,1919 Polich J. EEG and ERP assessment of normal aging. Electroencephalogr Clin Neurophysiol 1997;104(03):244–256 There are diverse regions that contribute to the generation of P3, including the hippocampus, temporal, frontal, and parietal cortical areas, structures within thelimbic system, andthe thalamus. P3 is reported to be altered in individuals with tinnitus, which indicates attentional dysfunction.2020 Asadpour A, Alavi A, Jahed M, Mahmoudian S. Cognitive Memory Comparison Between Tinnitus and Normal Cases Using Event-Related Potentials. Front Integr Nuerosci 2018;12:48,2121 Santos Filha VA, Matas CG. Late Auditory evoked potentials in individuals with tinnitus. Rev Bras Otorrinolaringol (Engl Ed) 2010;76(02):263–270,2222 Gabr TA, El-Hay MA, BadawyA. Electrophysiological and psychological studies in tinnitus. Auris Nasus Larynx 2011;38(06):678–683,2323 Mannarelli D, Pauletti C, Mancini P, et al. Selective attentional impairment in chronic tinnitus: Evidence from an event-related potentials study. Clin Neurophysiol 2017;128(03):411–417,2424 Wang Y, Zhang JN, Hu W, et al. The characteristics of cognitive impairment in subjective chronic tinnitus. Brain Behav 2018;8 (03):e00918,2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842

The literature on CAEPs in individuals with tinnitus reports varied results. There have been shreds of evidence that tinnitus affects either or both the sensory and cognitive components of CAEPs, suggesting a difference in the way sound is being processed.2020 Asadpour A, Alavi A, Jahed M, Mahmoudian S. Cognitive Memory Comparison Between Tinnitus and Normal Cases Using Event-Related Potentials. Front Integr Nuerosci 2018;12:48,2121 Santos Filha VA, Matas CG. Late Auditory evoked potentials in individuals with tinnitus. Rev Bras Otorrinolaringol (Engl Ed) 2010;76(02):263–270,2222 Gabr TA, El-Hay MA, BadawyA. Electrophysiological and psychological studies in tinnitus. Auris Nasus Larynx 2011;38(06):678–683,2323 Mannarelli D, Pauletti C, Mancini P, et al. Selective attentional impairment in chronic tinnitus: Evidence from an event-related potentials study. Clin Neurophysiol 2017;128(03):411–417,2424 Wang Y, Zhang JN, Hu W, et al. The characteristics of cognitive impairment in subjective chronic tinnitus. Brain Behav 2018;8 (03):e00918,2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842,2626 Attias J, Urbach D, Gold S, Shemesh Z. Auditory event related potentials in chronic tinnitus patients with noise induced hearing loss. Hear Res 1993;71(1-2):106–113,2727 Jacobson GP, McCaslin DL. A search for evidence of a direct relationship between tinnitus and suicide. J Am Acad Audiol 2001;12(10):493–496,2828 Hsu SY, Wang PC, Yang TH, Lin TF, Hsu SH, Hsu CJB-E. Auditory efferent dysfunction in normal-hearing chronic idiopathic tinnitus. B-ENT 2013;9(02):101–109 In vitro animal studies1616 Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13 have shown that the hyperactive neuralfirings decrease as a result of RIT. However, there are no neurophysiological studies reported on humans following RIT or educational counselling.

Aim of the Study

The present study aims at evaluating the perceptual and functional cortical changes following a session of modified RIT and psychoeducational counselling using auditory components N1 and P3.

Objectives

  1. To evaluate the perceptual changes after a single session of tinnitus treatment.

  2. To evaluate the neurophysiological changes associated with the perceptual changes using CAEPs.

  3. To observe the correlation or lack thereof between the perceptual and functional cortical changes.

Materials and Method

The present study included 10 (5 female and 5 male) participants aged between 20 and 50 years with continuous and bothersome tinnitus lasting for 3 months or more. In total, 3 patients had bilateral tinnitus (subjects [SUB] 02, 07, and 09), 4 had tinnitus in their left ear (SUBs 01, 04, 08, and 10), and the remaining 3 (SUBs 03, 05 and 06), in the rightear. Detailed information regarding the participants is provided in ►Table 1. The study was approved by the institutional research committee and ethics committee (IEC516/2017). Written consent was obtained from all the participants before the initiation of the study. The present is the continuation of a previous study2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842 which compared individuals with tinnitus to an age-, gender- and hearing-matched control group; the participants in the tinnitus group of the previous analysis formed the case group of the present study. To check if they could be included in the study, all participants underwent audiological and tinnitus evaluations performed using the Madsen-Astera (ANSI S3.43-1996) double-channel diagnostic audiometer coupled with TDH-50P (Telephonics Corporation DBA Communications System Division, New York, United States) headphones and Radio ear B-71 bone vibrator (Radio Ear, Denmark). Preliminary measures like tinnitus pitch and loudness matching were performed using a two-alternative forced-choice method. The participants’ hearing thresholds were lower than 40 dBHL and they scored at least a minimal degree of handicap (that is, grade I), as indexed by the THI.2929 Newman CW,Jacobson GP, Spitzer JB. Developmentof the tinnitus handicap inventory. Arch Otolaryngol Head Neck Surg 1996;122 (02):143–148 In addition to the aforementioned, they were asked to estimate the magnitude of their tinnitus loudness on a scale of 1 to 10, in which 10 corresponded to “extremely loud”. The magnitude score before the actual testing served as the baseline for the subjective evaluation of tinnitus loudness.

Table 1
Participants characteristics

Before the ERP Recording

Compumedics Neuroscan system (SCAN 4.5, Charlotte, USA) with a standard 32 channel EazyCapTM and combined mastoid reference was used to acquire the ERPs. Ocular potentials were acquired using the vertical electroocculogram (VEOG) and horizontal electrooculogram (HEOG) channels. Electrode impedance was ensured below 5 KΩ. The ERPs were recorded using a randomized auditory odd-ball paradigm with 1,000 Hz and 1,500 Hz pure tones serving as frequent and rare tones respectively. A total of 100 stimuli (at 75dB SPL over calibrated ER3A insert earphones) with frequent to rare ratios of 80:20 and interstimulus interval [ISI] of 1,000 ms were presented. The responses obtained were filtered using a band-pass filter with a high-pass and low -pass cut off at 1Hz and 30Hz respectively at a sampling rate of 500Hz. The participants were instructed to quietly count the number of rare stimuli and reveal them at the end of the testing. At the end of the recording session, the electrode connector was carefully detached, and the cap was retained on the participant’s head for the rest of the procedure to prevent electrode migration or bridging.

Psychoeducational Counselling

Following the recording of ERPs (pre), all participants underwent a session of non-standardized structured psychoeducational counseling for tinnitus management, which lasted ~ 30 minutes and was provided by an experienced and qualified audiologist.33 Searchfield GD, Magnusson J, Shakes G, Biesinger E, Kong O. Counseling and psycho-education for tinnitus management. In: Textbook of tinnitus. Springer; 2011:535–556 The counselling focused on the anatomy and physiology of the human ear, the audiological test results of the patients, the tinnitus and its causes, habituation, the role of attention in tinnitus, possible management options, RIT, and the procedure. The participants were also informed that there could be no benefit, or the benefits of RIT might be temporary. The main reason behind the counseling session was to make the participants aware of tinnitus and its causes, to reduce the fear and anxiety related to tinnitus by answering their questions, and to list the treatment options available.

Residual Inhibition Therapy (RIT)

The counselling session was followed by a session of modified RIT in an audiometric double room. In the modified RIT, all three parameters (intensity, duration, and spectrum) of the stimulus were modified to intensify the magnitude of tinnitus reduction and the duration of the RI. The participants were provided with white noise at a suprathreshold level (60dBSL) for 2 minutes, which served as an acoustic enricher. We ensured that the stimulus did not reach an uncomfortable level for the participants. White noise was provided using the Madsen-Astera audiometer coupled with TDH-50P Headphones. Following the RIT, the patients were asked two questions: Does the tinnitus sound the same now? If not, how does it differ? The responses of all the participants were recorded; further, they were also asked to estimate a percentage for the change noted following the RIT. This estimated percentage served as the postsubjective measure.

Measures after the ERP

Following the RIT session, the participants underwent the ERP testing once again after 40 minutes to 1 hour. The test setting and paradigm remained constant. The impedance was tested for the second time, and was ensured to be lower than 5 KΩ.

Historical Control Group

A historical control group2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842 containing ten individuals matched for age and gender was used to compare the functional cortical changes after a single session of modified RIT and psychoeducational counselling. The participants in the control group had no history of tinnitus or a diagnosis of neurological or psychiatric problems.

ERP Preprocessing and Analysis

The ERP data recorded were pre-processed using EEGLab (open source), version 14.1.1b,3030 Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004;134(01):9–21 which runs in Matlab R2017a (The Math Works, Inc., Natick, MA, US). The data was preprocessed by providing channel locations using the BESA 4 Shell sphere model and manually interpolating or removing bad channels and blocks with any ocular or muscular artifact. The obtained waveforms were placed into two bins named frequent and infrequent. An epoch was run across each bin with a time window of 800ms and a prestimulus duration of -200ms. Independent component analysis (ICA) was performed regarding the epochs, followed by automated artifact rejections with the help of multiple artifact rejection algorithms (MARA)3131 Winkler I, Haufe S, Tangermann M, Functions B. Automatic classification of artifactual ICA-components for artifact removal in EEG signals. Behav Brain Funct 2011;7(01):30 to correct for ocular artifacts. Finally the epoched data was common referenced to the mastoid and the rand average waveform was computed using the ERPLab module in MATLAB (version 6.14). The peak latency and absolute amplitude of the sensory components (N1 and P2) were obtained from the frequent waveform, and that of the cognitive component (P3), from the rare waveform. The latency and amplitude of the sensory components were computed from two electrode sites (Fz and Cz), while, for the cognitive component, three midline electrode sites were considered (Fz, Cz, and Pz). The statistical analysis was performed using the Statistical Package for the Social Sciences (IBM SPSS Statistics for Windows, IBM Corp., Armonk, NY, US), version 20.1. The pre- and posttreatment data were subjected to normality testing using the Shapiro-Wilk test, and were found to be normally distributed. Repeated measures analysis of variance (ANOVA) (two levels of within-subject factor [electrodes Fz and Cz] for the N1 and P2 analysis, and three levels of within-subject factor [electrodes Fz, Cz, and Pz] were compared between the groups [pre- and posttreatment]) to compare the latency and amplitude of N1, P2, and P3. A simplified flowchart of the methodology is shown in ►Fig. 1.

Fig. 1
Simplified flowchart of methodology of the present study.

Results

The mean age of the individuals with tinnitus was 38.8 (±10.27) years. The mean pure-tone average (PTA) of all participants was 17.42 (±5.89) dBHL in the right ear, and 19.53 (±8.36) dBHL in the left ear. All participants had bothersome tinnitus with at least a grade-I handicap as indexed using the THI.

Subjective Measures

The subjective outcome measures of all the participants are summarized in ►Table 2. Overall, 90% observed a change in the tinnitus loudness after undergoing psychoeducational counseling and RIT. In total, 8 out the the 10 participants had residual inhibition, 1 (SUB 03) had residual excitation, and 1 (SUB 10) had no change.

Table 2
Subjective outcome measures of the individual participants

Objective Measures: (CAEP Results)

The means and standard deviations of the latency of N1 and P2 and the amplitude before anf after the tinnitus treatment are shown in ►Table 3. The repeated mesures ANOVA showed no significant main effect of the electrode (F [1, 9] = 0.748; p = 0.410; η2 = 0.077) and the treatment (F [1, 9] = 0.002; p = 0.964; η2 = 0.000) on the latency of N1,. neither was their interaction significant (F [1, 9] = 0.987; p = 0.346; η2 = 0.099). There was a significant main effect of the treatment on the amplitude of N1 (F [1, 9] = 19.088; p = 0.002; η2 = 0.680), which was was reduced after the treatment (►Table 3). The amplitude of N1 also differed significantly regarding electrode sites (F [1, 9] = 6.159; p = 0.035; η2 = 0.406). There was no significant interaction effect (F [1, 9] = 1.375; p = 0.271; η2 = 0.133). The repeated measures ANOVA showed no significant main effect of the electrode sites (F [1, 9] = 1.699; p = 0.225; η2 = 0.159) or of the treatment (F [1, 9] = 0.140; p = 0.717; η2 = 0.015) on the latency of P2. The interaction between the electrode sites and the treatment was not significant (F [1, 9] = 0.234; p = 0.640; η2 = 0.025). The statistical results for the amplitude of P2 were similar to those of the latency: there was no significant main effect of the electrode sites (F [1, 9] = 0.000; p = 0.989; η2 = 0.000) and of the treatment (F [1, 9] = 1.425; p = 0.263; η2 = 0.137). Moreover, the interaction effect regarding the treatment and electrode was not significant (F [1, 9] = 1.161; p = 0.698; η2 = 0.018).

Table 3
Means and standard deviations of the latency and amplitude of the N1, P2, and P3 components

P3 Component

The mean and standard deviation of the latency and amplitude of P3 before and after the tinnitus treatment are shown in ►Table 3. There was no significant main effect of the treatment (F [1, 9] = 0.005; p = 0.943; η2 = 0.001) on P3 latency. The results showed that there was a main effect of the electrode sites (F [2, 18] = 5.949; p = 0.010; η2 = 0.398) on P3 latency, but no interaction between the electrodes and the treatment (F [2, 18] = 0.227; p = 0.799; η2 = 0.025). The analysis of the amplitude of P3 showed a significant main effect of the treatment (F [1, 9] = 15.40; p = 0.003; η2 = 0.631): after the treatment, there was a reduction in the amplitude of P3 compared tobefore the treatment. There was no significant main effect of the electrodes (F [2, 18] = 1.332; p = 0.289; η2 = 0.129), but the interaction between the electrodes and the treatment was significant (F [2, 18] = 7.816; p = 0.004; η2 = 0.465).

Correlation between Subjective and Objective Measures

The Pearson correlation was performed to assess the relationship between the perceived difference in tinnitus loudness and P3 amplitude (at Pz). There was no correlation between the two variables (r = -0.575; n = 10; p = 0.082), which suggests no correlation between the reduction in P3 amplitude (at Pz) and the perceived loudness. The scatter plot summarizing the results is provided in ►Fig. 2.

Fig. 2
Scatter plot (correlation between the difference in P3 amplitude at Pz and the perceived reduction in loudness).

Comparison with the Historical Control Group

The historical control group2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842 was matched in terms of age (t [18] = 0.194; p = 0.848), gender and hearing (right PTA: t [18] = 2.011; p = 0.060; left PTA: t [18] = 1.882; p = 0.076) to the case group. The mean latencies and amplitudes of the historical control group are shown in ►Table 3. The analysis of the posttreatment CAEPsand thehistorical controlgroup using repeated measures ANOVA indicated that the latencies (N1: F [1, 18] = 0.006; p = 0.939; η2 = 0.000; P2: F [1, 18] = 1.227; p = 0.283; η2 = 0.064; and P3F [1, 18] = 0.726; p = 0.405; η2 = 0.039) and amplitudes (N1: F [1, 18] = 3.288; p = 0.086; η2 = 0.154;P2:F[1,18] = 0.808;p = 0.380; η2 = 0.043;andP3F [1, 18] = 0.192; p = 0.667; η2 = 0.011) of the ERPs were comparable between the two groups (►Figs. 3 and 4).

Fig. 3
N1 waveform pre- and posttreatment with results of the control group as well.

Fig. 4
P3 waveform pre- and posttreatment with results of the control group as well.

Discussion

Residual inhibition is a commonly-used procedure, but there are very few studies on the mechanism of RI to relieve tinnitus. The present study aimed at exploring whether CAEPs reflected the effect of RIT and educational counselling using the N1 and P3 auditory components and their correlation with behavioral measures. Overall, the results of the present study reflected both subjective and objective changes in individuals with tinnitus after a single session of RIT and psychoeducational counseling. The results are discussed in the following sections.

Subjective Measures

The literature3333 Goldstein BA, Lenhardt ML, Shulman A. Tinnitus improvement with ultra-high-frequency vibration therapy. Int Tinnitus J 2005; 11(01):14–22,3434 Sockalingam R, Gulliford K, Gulliver M, Whitehead G. Effectiveness of Frequency-Matched Masking and Residual Inhibition in Tinnitus Therapy. Asia Pac J Speech Lang Hear 2007;10(02): 87–103 supports a reduction in the severity of the tinnitus after RI to different stimuli. The present study is in line with these findings: 80% of the participants reported a reduction in tinnitus loudness after a session of modified RIT and psychoeducational counselling. However, SUB03 and SUB10 reported no change in loudness. It is noteworthy that SUB03 reported a catastrophic handicap due to tinnitus in the THI. The duration of RI for the other eight participants was of at least one hour (until the participants were in the hospital for the posttreatment evaluation). The participants were informed that the effect may be temporary and can ricochet. They were advised not to panic in case the tinnitus reoccured, and to reach out to us in such situations. All participants were counselled on environmental modifications basedontheir RITresults and futuretinnitus care. None of the participants returned complaining of tinnitus.

Objective Measures

N1 Component

The results of the present study show a significant reduction in the amplitude of N1 after the treatment. The pre- and posttreatment N1 waveforms are shown in ►Fig. 3.

It is known that individuals with tinnitus have a larger N1 amplitude.2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842,3535 Yang H, Xiong H, Yu R, Wang C, Zheng Y, Zhang X. The characteristic and changes of the event-related potentials (ERP) and brain topographic maps before and after treatment with rTMS in subjective tinnitus patients. PLoS One 2013;8(08):e70831 Enhanced neural synchrony resulting in higher baseline activity or an impaired adaptation of cortical neurons following noise exposure/cochlear damage are thought to be the underlying mechanisms. Residual inhibition directly influences the neural firing of cortical neurons by reducing the neuronal hyperexcitability in animals suffering from tinnitus.1616 Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13 The amplitude of N1 indexes the strength of the neural firing. Hence, it can be deduced that the reduction in N1 amplitude can be related to neuronal silencing. With the assessments conducted in the present study, we may not be able to pinpoint the exact mechanism triggering this change. Nevertheless, the change in the sensory component indicates an unambiguous plastic change at the cortical level after a single session of modified RIT and psychoeducational counseling. N1 latency indexes the speed of stimulus detection or the conduction delay. Concerning N1 latency, there was no observable change after RIT and psychoeducational counselling, which implies that the treatment does not alter neuronal efficiency. The N1 reduction (at Fz) for the individual subjects is shown in ►Fig. 5. Eight out of the ten participants showed a clear reduction in their N1 amplitude posttreatment. Overall, the results regarding N1 suggested a measurable difference before and after a single session of tinnitus treatment. It is plausible that this change in N1 is a result of neuronal silencing contributing to tinnitus reduction. However, considering that not all the participants showed a reduction in N1 amplitude and thesample size of the study, thesefindings must be interpreted with caution.

Fig. 5
Pre- and posttreatment N1 and P3 amplitudes for the individual participants

P3 Component

The current study showed a reduction in P3 amplitude after RIT and psychoeducational counselling without any latency change. The pre- and post treatment P3 wave forms are shown in ►Fig. 4.

Individuals with tinnitus typically showed a mixed presentation, with associated hearing loss and psychological problems. These factors affect P3 in their ways, making it difficult to interpret. P3 amplitude is an index of central resource allocation and working memory processing. The literature supports that individuals with tinnitus usually have a decreased1616 Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13,2020 Asadpour A, Alavi A, Jahed M, Mahmoudian S. Cognitive Memory Comparison Between Tinnitus and Normal Cases Using Event-Related Potentials. Front Integr Nuerosci 2018;12:48,2323 Mannarelli D, Pauletti C, Mancini P, et al. Selective attentional impairment in chronic tinnitus: Evidence from an event-related potentials study. Clin Neurophysiol 2017;128(03):411–417 or unaffected P3 amplitude.3636 Houdayer E, Teggi R, Velikova S, et al. Involvement of corticosubcortical circuits in normoacousic chronic tinnitus: A source localization EEG study. Clin Neurophysiol 2015;126(12): 2356–2365 Similar findings are observed in individuals with pure sensory neural hearing impairment.3737 Oates PA, Kurtzberg D, Stapells DR. Effects of sensorineural hearing loss on cortical event-related potential and behavioral measures of speech-sound processing. Ear Hear 2002;23(05): 399–415,3838 Reis ACMB, Iório MCM. [P300 in subjects with hearing loss]. Pro Fono 2007;19(01):113–122 Such a decrease in P3 amplitude was related to insufficient resource allocation and/or working memory. However, individuals with psychological ailments (including phobia and anxiety) have been shown to have an increased P3 amplitude.3939 De Pascalis V, Strippoli E, Riccardi P, Vergari FJP, Differences I. Personality, event-related potential (ERP) and heart rate (HR) in emotional word processing. Pers Individ Dif 2004;36(04): 873–891,4040 Enoch MA, White KV, Harris CR, Rohrbaugh JW, Goldman D. Alcohol use disorders and anxiety disorders: relation to the P300 event-related potential. Alcohol Clin Exp Res 2001;25(09): 1293–1300,4141 Kolassa IT, Musial F, Mohr A, Trippe RH, Miltner WH. Electrophysiological correlates of threat processing in spider phobics. Psychophysiology 2005;42(05):520–530,4242 Kolassa I-T, Musial F, Kolassa S, Miltner WH. Event-related potentials when identifying or color-naming threatening schematic stimuli in spider phobic and non-phobic individuals. BMC Psychiatry 2006;6(01):38,4343 Li Y, Wang W, Liu T, et al. Source analysis of P3a and P3b components to investigate interaction of depression and anxiety in attentional systems. Sci Rep 2015;5:17138,4444 Miltner WH, Trippe RH, Krieschel S, Gutberlet I, Hecht H, Weiss T. Event-related brain potentials and affective responses to threat in spider/snake-phobic and non-phobic subjects. Int J Psychophysiol 2005;57(01):43–52 Increased attentional resources getting allocated for a target stimulus can increase the activity in the ventral attentional network (similar to anxiety disorders) which in turn can result in an enhanced P3.4343 Li Y, Wang W, Liu T, et al. Source analysis of P3a and P3b components to investigate interaction of depression and anxiety in attentional systems. Sci Rep 2015;5:17138 It is well known that individuals with tinnitus have increased anxiety and fear due to the involvement of the limbic and autonomic nervous systems.

Objective differences in the neuronal oscillatory bands have been foundafter anRI session.4545 Kahlbrock N, Weisz N. Transient reduction of tinnitus intensity is marked byconcomitant reductionsofdelta band power.BMCBiol 2008;6(01):4,4646 Schoisswohl S, Schecklmann M, Langguth B, Schlee W, Neff P. Neurophysiological correlates of residual inhibition in tinnitus: Hints for trait-like EEG power spectra. Clin Neurophysiol 2021; 132(07):1694–1707,4747 Sedley W, Gander PE, Kumar S, et al. Intracranial mapping of a cortical tinnitus system using residual inhibition. Curr Biol 2015; 25(09):1208–1214 In the present study, there was a reduction in P3 amplitude posttreatment. It is only plausible to expect that the fear and anxiety associated with tinnitus would have reduced post treatment which is projected via the P3reduction. Besides, RIT isknown to affect neuronal excitability1616 Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13 by causing neuronal silencing, triggering a temporary relief of the tinnitus. This temporary relief could have made the resource allocation simpler. The combined efforts of these mechanisms might have resulted in a moderated P3 amplitude, which was increased before the treatment.2525 Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842 Interestingly, the posttreatment P3 amplitudes were similar to those of the historical control group. However, since the participants performed the same task twice (before and after the treatment), the effect of practice cannot be neglected. In addition, since psychological factors related to tinnitus, such as anxiety and fear, were not measured using standardized scales, it is difficult toattribute the decrease in P3 to the impact of the psychological factors.

Fig. 5 displays the reduction in P3 amplitude for each individual after the treatment, and it shows that the reduction was unidirectional for all participants rather than just a group effect. Are duction of 2 µV to 3 µV in P3 was observed in all participants at the Cz and Pz electrode sites. Unlike the sensory component N1, the cognitive component P3 was found to be reduced in all the participants after the treatment, indicating that RIT and psychoeducational counseling not only influence the neuronal excitability but also has an influence on the central cognitive components of processing.

In the present study, no modification was observed on P3 latency posttreatment. The P3 latency indexes information processing and the speed of classification of a stimulus, andit is reported2121 Santos Filha VA, Matas CG. Late Auditory evoked potentials in individuals with tinnitus. Rev Bras Otorrinolaringol (Engl Ed) 2010;76(02):263–270,2222 Gabr TA, El-Hay MA, BadawyA. Electrophysiological and psychological studies in tinnitus. Auris Nasus Larynx 2011;38(06):678–683 to be longer in individuals with tinnitus; however, there are contradictory findings3636 Houdayer E, Teggi R, Velikova S, et al. Involvement of corticosubcortical circuits in normoacousic chronic tinnitus: A source localization EEG study. Clin Neurophysiol 2015;126(12): 2356–2365,4848 Shiraishi T, Sugimoto K, Kubo T, Matsunaga T, Nageishi Y, Simokochi M. Contingent negative variation enhancement in tinnitus patients. Am J Otolaryngol 1991;12(05):267–271 as well. A possible explanation for the lack of alteration in latency in the current study could be that RIT does not target the working memory, subsequently causing the efficiency of the stimulus classification to remain unaltered.

Correlation between Subjective and Objective Measures

In the present study, there was a reduction in both the perceptual (VAS) and functional (CAEPs) measures posttreatment. A decrease in tinnitus loudness could reduce the cognitive load, as discussed earlier. However, no significant correlation was observed between the reduction in P3 amplitude and the reduction in the perceived tinnitus loudness, though both of these measures changed in the same direction. This could be attributed to the small sample size or the mechanism underlying these measures, or both. P3 reflects the cognitive resources allocated to process a particular

stimulus and working memory, which is one of the stages that is involved in perception. Loudness is the psychological attribution of the intensity of a sound, which is an end product of multiple decision making process.

Limitations of the Study

First, the sample size of the present study makes generalization tricky. Nevertheless, it still comprises preliminary evidence in favor of psychoeducational counselling and RIT. Second, a follow-up evaluation of the participants would have provided more information on the duration of this effect of the treatment. This was not possible due to various reasons (including travel, distance, and financial issues involving the participants), making it a drawback of the study. Finally, the study included two individuals who did not fall within the persistent tinnitus category. Though the current study is a pre-post design the different categories of tinnitus could still be a confounding factor which needs to be studied further.

Conclusion

There was a significant reduction in the amplitude of both the sensory (N1) and cognitive (P3) ERP components, with no alteration in their latencies after psychoeducational counselling and RIT, possibly reflecting both perceptual and functional changes (evidenced as reduced N1 and P3). This is preliminary evidence that ERPs can be used to quantify the physiological changes that occur after tinnitus intervention. However, further randomized clinical trials with a large samples are warranted to establish this.

  • Funding
    The present research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

References

  • 1
    Bhatt IS. Prevalence of and risk factors for tinnitus and tinnitus-related handicap in a college-aged population. Ear Hear 2018;39 (03):517–26
  • 2
    English K. Counseling in audiologic practice: Helping patients and families adjust to hearing loss. 2005
  • 3
    Searchfield GD, Magnusson J, Shakes G, Biesinger E, Kong O. Counseling and psycho-education for tinnitus management. In: Textbook of tinnitus. Springer; 2011:535–556
  • 4
    Lukens EP, McFarlane WR. Psychoeducation as Evidence-Based Practice: Considerations for Practice, Research, and Policy. Brief Treat Crisis Interv 2004;4(03):205–225
  • 5
    Tyler RS, Noble W, Preece JP, Dunn CC, Witt SA. Psychological treatments for tinnitus. Tinnitus: Theory and Management 2004: 314–323
  • 6
    Henry JL, Wilson PH. The psychological management of tinnitus: comparison of a combined cognitive educational program, education alone and a waiting-list control. Int Tinnitus J 1996;2:9–20
  • 7
    Kröner-Herwig B, Frenzel A, Fritsche G, Schilkowsky G, Esser G. The management of chronic tinnitus: comparison of an outpatient cognitive-behavioral group training to minimal-contact interventions. J Psychosom Res 2003;54(04):381–389
  • 8
    Hazell JW, Wood S. Tinnitus masking-a significant contribution to tinnitus management. Br J Audiol 1981;15(04):223–230
  • 9
    Terry AM, Jones DM, Davis BR, Slater R. Parametric studies of tinnitus masking and residual inhibition. Br J Audiol 1983;17(04): 245–256
  • 10
    Dessai TD, Gopinath R, Krishnan L, Susan G. Effectiveness of residual inhibition therapy. Int Tinnitus J 2014;19(01):63–67
  • 11
    Voytenko SV, Galazyuk AV. mGluRs modulate neuronal firing in the auditory midbrain. Neurosci Lett 2011;492(03):145–149
  • 12
    Roberts LE, Moffat G, Bosnyak DJ. Residual inhibition functions in relation to tinnitus spectra and auditory threshold shift. Acta Otolaryngol Suppl 2006;126(556):27–33
  • 13
    Vernon JA, Meikle MB. Tinnitus: clinical measurement. Otolaryngol Clin North Am 2003;36(02):293–305
  • 14
    Witchard C. Residual inhibition. In: 2013
  • 15
    Roberts LE. Residual inhibition. Prog Brain Res 2007;166:487–495
  • 16
    Galazyuk AV, Longenecker RJ, Voytenko SV, Kristaponyte I, Nelson GL. Residual inhibition: From the putative mechanisms to potential tinnitus treatment. Hear Res 2019;375:1–13
  • 17
    Pfefferbaum A, Ford JM, Wenegrat BG, Roth WT, Kopell BS. Clinical application of the P3 component of event-related potentials.I. Normal aging. Electroencephalogr Clin Neurophysiol 1984;59(02):85–103
  • 18
    Picton TW, Stuss DT, Champagne SC, Nelson RF. The effects of age on human event-related potentials. Psychophysiology 1984;21 (03):312–325
  • 19
    Polich J. EEG and ERP assessment of normal aging. Electroencephalogr Clin Neurophysiol 1997;104(03):244–256
  • 20
    Asadpour A, Alavi A, Jahed M, Mahmoudian S. Cognitive Memory Comparison Between Tinnitus and Normal Cases Using Event-Related Potentials. Front Integr Nuerosci 2018;12:48
  • 21
    Santos Filha VA, Matas CG. Late Auditory evoked potentials in individuals with tinnitus. Rev Bras Otorrinolaringol (Engl Ed) 2010;76(02):263–270
  • 22
    Gabr TA, El-Hay MA, BadawyA. Electrophysiological and psychological studies in tinnitus. Auris Nasus Larynx 2011;38(06):678–683
  • 23
    Mannarelli D, Pauletti C, Mancini P, et al. Selective attentional impairment in chronic tinnitus: Evidence from an event-related potentials study. Clin Neurophysiol 2017;128(03):411–417
  • 24
    Wang Y, Zhang JN, Hu W, et al. The characteristics of cognitive impairment in subjective chronic tinnitus. Brain Behav 2018;8 (03):e00918
  • 25
    Vasudevan H, Palaniswamy HP, Balakrishnan R. Sensory and Cognitive Components of Auditory Processing in Individuals With Tinnitus. Am J Audiol 2019;28(04):834–842
  • 26
    Attias J, Urbach D, Gold S, Shemesh Z. Auditory event related potentials in chronic tinnitus patients with noise induced hearing loss. Hear Res 1993;71(1-2):106–113
  • 27
    Jacobson GP, McCaslin DL. A search for evidence of a direct relationship between tinnitus and suicide. J Am Acad Audiol 2001;12(10):493–496
  • 28
    Hsu SY, Wang PC, Yang TH, Lin TF, Hsu SH, Hsu CJB-E. Auditory efferent dysfunction in normal-hearing chronic idiopathic tinnitus. B-ENT 2013;9(02):101–109
  • 29
    Newman CW,Jacobson GP, Spitzer JB. Developmentof the tinnitus handicap inventory. Arch Otolaryngol Head Neck Surg 1996;122 (02):143–148
  • 30
    Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004;134(01):9–21
  • 31
    Winkler I, Haufe S, Tangermann M, Functions B. Automatic classification of artifactual ICA-components for artifact removal in EEG signals. Behav Brain Funct 2011;7(01):30
  • 32
    Lopez-Calderon J,Luck SJ. ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 2014; 8:213
  • 33
    Goldstein BA, Lenhardt ML, Shulman A. Tinnitus improvement with ultra-high-frequency vibration therapy. Int Tinnitus J 2005; 11(01):14–22
  • 34
    Sockalingam R, Gulliford K, Gulliver M, Whitehead G. Effectiveness of Frequency-Matched Masking and Residual Inhibition in Tinnitus Therapy. Asia Pac J Speech Lang Hear 2007;10(02): 87–103
  • 35
    Yang H, Xiong H, Yu R, Wang C, Zheng Y, Zhang X. The characteristic and changes of the event-related potentials (ERP) and brain topographic maps before and after treatment with rTMS in subjective tinnitus patients. PLoS One 2013;8(08):e70831
  • 36
    Houdayer E, Teggi R, Velikova S, et al. Involvement of corticosubcortical circuits in normoacousic chronic tinnitus: A source localization EEG study. Clin Neurophysiol 2015;126(12): 2356–2365
  • 37
    Oates PA, Kurtzberg D, Stapells DR. Effects of sensorineural hearing loss on cortical event-related potential and behavioral measures of speech-sound processing. Ear Hear 2002;23(05): 399–415
  • 38
    Reis ACMB, Iório MCM. [P300 in subjects with hearing loss]. Pro Fono 2007;19(01):113–122
  • 39
    De Pascalis V, Strippoli E, Riccardi P, Vergari FJP, Differences I. Personality, event-related potential (ERP) and heart rate (HR) in emotional word processing. Pers Individ Dif 2004;36(04): 873–891
  • 40
    Enoch MA, White KV, Harris CR, Rohrbaugh JW, Goldman D. Alcohol use disorders and anxiety disorders: relation to the P300 event-related potential. Alcohol Clin Exp Res 2001;25(09): 1293–1300
  • 41
    Kolassa IT, Musial F, Mohr A, Trippe RH, Miltner WH. Electrophysiological correlates of threat processing in spider phobics. Psychophysiology 2005;42(05):520–530
  • 42
    Kolassa I-T, Musial F, Kolassa S, Miltner WH. Event-related potentials when identifying or color-naming threatening schematic stimuli in spider phobic and non-phobic individuals. BMC Psychiatry 2006;6(01):38
  • 43
    Li Y, Wang W, Liu T, et al. Source analysis of P3a and P3b components to investigate interaction of depression and anxiety in attentional systems. Sci Rep 2015;5:17138
  • 44
    Miltner WH, Trippe RH, Krieschel S, Gutberlet I, Hecht H, Weiss T. Event-related brain potentials and affective responses to threat in spider/snake-phobic and non-phobic subjects. Int J Psychophysiol 2005;57(01):43–52
  • 45
    Kahlbrock N, Weisz N. Transient reduction of tinnitus intensity is marked byconcomitant reductionsofdelta band power.BMCBiol 2008;6(01):4
  • 46
    Schoisswohl S, Schecklmann M, Langguth B, Schlee W, Neff P. Neurophysiological correlates of residual inhibition in tinnitus: Hints for trait-like EEG power spectra. Clin Neurophysiol 2021; 132(07):1694–1707
  • 47
    Sedley W, Gander PE, Kumar S, et al. Intracranial mapping of a cortical tinnitus system using residual inhibition. Curr Biol 2015; 25(09):1208–1214
  • 48
    Shiraishi T, Sugimoto K, Kubo T, Matsunaga T, Nageishi Y, Simokochi M. Contingent negative variation enhancement in tinnitus patients. Am J Otolaryngol 1991;12(05):267–271

Publication Dates

  • Publication in this collection
    20 Jan 2023
  • Date of issue
    Oct-Dec 2022

History

  • Received
    24 Dec 2020
  • Accepted
    22 Aug 2021
  • Published
    14 June 2022
Fundação Otorrinolaringologia R. Teodoro Sampaio, 483, 05405-000 São Paulo/SP Brasil, Tel.: (55 11) 3068-9855, Fax: (55 11) 3079-6769 - São Paulo - SP - Brazil
E-mail: iaorl@iaorl.org