Neurophysiological model of tinnitus: Dependence of the minimal masking level on treatment outcome
Transcript of Neurophysiological model of tinnitus: Dependence of the minimal masking level on treatment outcome
ELSEVIER Hearing Research 80 (1994) 216-232
Neurophysiological model of tinnitus: Dependence of the minimal masking level on treatment outcome
Pawel J. Jastreboff a,*, Jonathan W.P. Hazell b, Rena L. Graham b
a University of Maryland School of Medicine, Department of Surgery, 10 South Pine Street, MSTF Building, Room 434F, Baltimore, MD 21201, USA b RNID Medical Research Unit, ILO with the Ferens, University College London, London, UK
Received 8 February 1994; revised 1 August 1994; accepted 14 August 1994
Abstract
Validity of the neurophysiological model of tinnitus (Jastreboff, 1990), outlined in this paper, was tested on data from multicenter trial of tinnitus masking (Hazell et aI., 1985). Minimal masking level, intensity match of tinnitus, and the threshold of hearing have been evaluated on a total of 382 patients before and after 6 months of treatment with maskers, hearing aids, or combination devices. The data has been divided into categories depending on treatment outcome and type of approach used. Results of analysis revealed that: i) the psychoacoustical description of tinnitus does not possess a predictive value for the outcome of the treatment; ii) minimal masking level changed significantly depending on the treatment outcome, decreasing on average by 5.3 dB in patients reporting improvement, and increasing by 4.9 dB in those whose tinnitus remained the same or worsened; iii) 73.9% of patients reporting improvement had their minimal masking level decreased as compared with 50.5% for patients not showing improvement, which is at the level of random change; iv) the type of device used has no significant impact on the treatment outcome and minimal masking level change; v) intensity match and threshold of hearing did not exhibit any significant changes which can be related to treatment outcome. These results are fully consistent with the neurophysiological interpretation of mechanisms involved in the phenomenon of tinnitus and its alleviation.
Keywords: Tinnitus; Neurophysiological model; Psychoacoustics; Treatment
1. Introduction
At the present time we do not have any objective, physical measurement that can be related to the presence of tinnitus. Tinnitus is an auditory phantom perception, and therefore cannot be associated with any sound measurement. Characterization of tinnitus for diagnosis and monitoring of the effectiveness of treatment has been performed mainly by subject interview, and extensive questionnaires have been invented for this purpose (Erlandsson et aI., 1992; George and Kemp, 1991; Kuk et aI., 1990; Hazell et aI., 1985; Wilson et aI., 1991). This approach yielded important epidemiological and demographic data but failed to provide measures useful for predicting the outcome of
* Corresponding author. Fax: (410) 706-4004; e-mail: [email protected]
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treatment and monitoring its progress (Coles et aI., 1993; Stouffer and Tyler, 1990).
At the same time much importance has been attached to the psychoacoustical description of tinnitus (Penner and Bilger, 1992; Kodama and Kitahara, 1990; Penner, 1986; Hazell et aI., 1985; Tyler and ConradArmes, 1984; Penner, 1983b; Tyler and Conrad-Armes, 1983a; Hazell, 1981; Penner, 1988a; Penner, 1988b; Penner, 1983a; Tyler and Stouffer, 1989; Tyler and Conrad-Armes, 1983b; Penner and Klafter, 1992). The expectation was that by evaluating tinnitus pitch, loudness, maskability, and reconstructing the tinnitus sound, different tinnitus categories could be identified for diagnosis and prediction of treatment effectiveness (Douek, 1981). Unfortunately clinical results up to date have failed to find significant correlations between psychoacoustical description of tinnitus and the treatment outcome (Hazell et aI., 1985).
First, it turned out that, paradoxically, patients with
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very low levels of tinnitus loudness, as assessed by psychoacoustical measurements, may have a high level of complaint and distress from their tinnitus, while patients with relatively high levels of loudness might not exhibit distress (Hazell et ai., 1985). Second, psychoacoustical measurements have not been shown to be helpful in predicting the outcome of tinnitus treatments (Scott et ai., 1990; Douek and Reid, 1968). Finally, attempts to relate the subjective improvement of tinnitus to psychoacoustical measurements have not proved successful (Guth et ai., 1990; Hazell, 1990; Kuk et ai., 1989; Hazell et al., 1985; Scott et ai., 1985; Hansen et ai., 1982; Murai et ai., 1992).
The difficulty of making accurate psychoacoustic measurements of tinnitus in a clinical environment has been held partially responsible for the lack of usefulness of the psychoacoustical data. In order to make accurate measurements of tinnitus, as in the matching of two external tones, it is necessary to implement sophisticated and time-consuming methods which preclude them from being used in a clinical environment (Tyler and Conrad-Armes, 1983a; Penner and Bilger, 1992). Assuming that a treatment-induced modification of psychoacoustical characteristics of tinnitus exists, then it might well be concealed by intersubject variability. Since previous efforts have failed to show any treatment-related changes in psychoacoustical measurements, this suggests that these changes are non-existent or in the range of a few dB. Therefore, they would require a large, homogenous population of patients to be detected.
Efforts with the psychoacoustical characterization of tinnitus provided important data showing that tinnitus has clearly different psychoacoustical properties from external sounds (Feldmann, 1988; Feldmann, 1981; Feldmann, 1971; Penner, 1988a; Penner, 1988b; Penner, 1987; Penner, 1986; Penner, 1984; Tyler and Conrad-Armes, 1984; McFadden, 1982; Penner et ai., 1981; Penner, 1993). A number of puzzles have emerged, such as: i) tinnitus does not exhibit phase-related phenomena; ii) masking of tinnitus by external tones is frequency independent, even for tonal tinnitus, which is contrary to the tuned masking of external tones; iii) masking of tinnitus is not proportional to its loudness; iv) contralateral masking can be as effective as ipsilateral masking.
1.1. Psychoacoustical model
A number of theories of the mechanisms of tinnitus have been proposed in the past but until recently they were based on pointing out some localization within the auditory pathways, usually the cochlea or auditory nerve, as a 'tinnitus generator' and treating all the remaining auditory system as a prewired, unchangeable cable transmitting the tinnitus signal originating from
this generator, to the auditory cortex (Tonndorf, 198 I; Tonndorf, 1987; Kiang et ai., 1970; Salvi and Ahroon, 1983; Penner, 1980; M0ller, 1984; Eggermont, 1990). Furthermore, only the auditory system was considered to be relevant to the tinnitus phenomenon and other parts of the nervous system were ignored. This auditory-centered approach encouraged purely psychoacoustical characterization of tinnitus and promoted the idea of the importance of loudness. pitch, and maskability for categorizing tinnitus and predicting the outcome of various treatments (Douek, 1981). Tinnitus masking, employing levels of noise sufficient to make tinnitus inaudible for prolonged periods of time, has been proposed as the effective method of treatment (Vernon and Meikle, 1981; Schleuning et al.. 1980; Vernon and Schleuning, 1978; Vernon, 1977) with stress on selecting optimal spectral parameters of masking sound (Smith et aI., 1991; Terry et aI., 1983), in spite of well established observations that tinnitus masking is to a large extent frequency independent (Penner, 1987; Feldmann, 1971). According to this approach exposing the subject to sound below the level needed for suppression of tinnitus should be without effect. This approach, centered on the tinnitus generator, which confines processes resulting in tinnitus perception to the auditory system, and focuses on the psychoacoustical characterization of tinnitus, will be referred in the remaining part of the paper as 'the psychoacousticaI' model, or approach.
There are a number of implications and predictions of the psychoacoustical approach. According to this approach tinnitus treatment should be aimed at attenuating the tinnitus generator or separating it from the remaining part of the auditory system, e.g. by cutting the auditory nerve. Unfortunately, auditory nerve section is not consistently helpfuL and actually may induces tinnitus in approximately 50% of patients who were without preoperational tinnitus (Berliner et aI., 1992). The psychoacoustical approach also relates the severity of the tinnitus to its loudness and maskability; very loud tinnitus, which is difficult or impossible to mask should be difficult to eliminate, while soft, easily maskable tinnitus should be easily controlled. Improvement in a patients condition should be accompanied by a decrease of tinnitus loudness, paralleled by a decrease in minimal masking level. Categorization of tinnitus cases depending on their audiograms, etiology and type of hearing loss should have a bearing on treatment outcome.
1.2. Neurophysiological model
Analysis of the tinnitus phenomenon from the neuroscience viewpoint led to the development of a new theory of tinnitus, already described in detail Oastreboff, 1990). Only the main ideas of the theory
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are presented here, with their justification and practical implications, as they relate to the results of the present paper in outline. The theory is based on the following basic, well established neurophysiological and psychological principles: i) for each sensory system processing of information occurs on several levels, each contributing to the final signal reaching the cortex; ii) all subsystem within the nervous system, including sensory systems, are strongly interconnected resulting in simultaneous processing of information in a parallel manner, while each system determines the type and extent of specific response evoked by a stimulus; iii) the nervous system exhibits a high level of plasticity, with continuous modification of connections within neural networks resulting in enhancement of significant signals, and a decrease of neuronal response to irrelevant signals; iv) signals which are new, or related to positive or negative reinforcement are treated as significant and evoke an emotional response; repetition of those signals results in enhancement of their perception and in increased resistance to their perception being suppressed by signals from the same or other modality. Repetition of signals not associated with positive or negative reinforcement results in disappearance of any response to their presence, i.e., in habituation; v) detection of sensory information occurs on a pattern-matching principle, allowing for nearly complete perception of a signal even when it becomes highly distorted; (Goldman-Rakic, 1988; Price, 1987; Ito, 1989a; Ito, 1990; Ito, 1984; Konorski, 1948; Thompson and Donegan, 1987; Thompson, 1987; Woody, 1987; Groves and Thompson, 1970; Pribram, 1971; Pribram, 1987; Sejnowski et al., 1988; Churchland and Sejnowski, 1988; el-Kashlan et al., 1993; Gerken, 1993; Gerken, 1991; Aitkin, 1986; Gerken, 1984; Shors et al., 1992; Thompson, 1986; McCormick and Thompson, 1984; Thompson et al., 1963; Thompson, 1989; Ito, 1989b; Brown et al., 1989; Klopf, 1982; Klopf, 1988; Klopf, 1989).
Consequently, the main point of the theory of tinnitus based on these neurophysiological principles is the postulate that all levels of the auditory pathways and several non auditory systems, particularly the limbic system (involved in emotion), are an essential part of each case of tinnitus and contribute in varying degrees in the emergence of tinnitus perception, and determine the level of its annoyance (principles i, and ii). The following scenario of the emergence of tinnitus perception has been proposed (Jastreboff, 1990). Weak initial imbalance of neuronal activity within the auditory system, most frequently related to cochlear damage (McFadden, 1982; Reed, 1960), is detected at low levels in the auditory system, and being a new signal it is further enhanced by subcortical centers, transferred to auditory cortex, and perceived as a sound - tinnitus (principle iv), and is subsequently evaluated. In the majority
of cases the continued presence of tinnitus combined with a lack of any positive or negative associations results in habituation of reaction to the tinnitus signal. Although tinnitus perception may still be possible there is little or no annoyance or discomfort (Hazell et al.. 1985; Jakes et al., 1992) (principle iv). This situation is typical for children, or those leaving a loud concert. who tend to treat tinnitus as a natural event, and tinnitus typically is not annoying them. However, in many cases perception of tinnitus is associated with a negative emotion. Patients treat tinnitus as a signal that something is going wrong with hearing, or with the brain, and as a result start to focus attention on the tinnitus. Quite frequently this is only the result of 'negative counseling' received from professionals, who advise patients to check for brain tumor, indicate that there is a primary psychiatric condition and state that 'nothing can be done with tinnitus' and that the patient has to 'learn to live with it' (Jastreboff and Hazell, 1993). This negative reinforcement of tinnitus perception results in enhancing initial responses of the autonomic nervous system evoked by fear. Moreover since tinnitus is commonly continuously present. and elicits a strong emotional response, this results in tuning of the neuronal networks detecting the tinnitus signal itself (principle iv). This in turn increases the proportion of time an individual is aware of the presence of tinnitus and further enhances the aversive emotional responses of the autonomic nervous system. Notably, the involvement of the limbic system is responsible for the annoyance evoked by tinnitus; the loudness and pitch of tinnitus are of secondary importance and are not normally playing a significant role (Hazell et al., 1985) (principle ii). The approach based on the principles listed above will be referred to in this paper as 'the neurophysiological' model of tinnitus.
1.3. Implications from both models
The psychoacustical and neurophysiological models provide contradictory predictions regarding potential methods of tinnitus treatment and psychoacoustical characterization of tinnitus in patients, showing improvement and non-improvement. First, the psychoacoustical approach predicts that tinnitus can be treated only by attenuating the tinnitus generator, or disrupting the connection of the generator with the cortex. In addition this approach promotes the use of masking by high levels of external noise as providing temporary relief by suppressing tinnitus perception with an external sound. Exposing patients to sound which does not, and cannot mask their tinnitus is considered to be without any beneficial effect, and therefore masking is not used in this group. Observations of short term suppression of tinnitus after masking, so called 'residual inhibition' (Terry et aL, 1983; Vernon and Schleun-
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ing, 1978; Feldmann, 1971), was hoped to lead to a long term solution. This approach was further pursued by attempting to determine the acoustical parameters of the masker sound which might prolong periods of residual inhibition to hours and days (Terry et aI., 1983). The neurophysiological theory explains residual inhibition as a perceptual manifestation of the rebound effect, observed commonly in single cell recordings, which causes temporal detuning of neuronal networks detecting tinnitus-related signal (Jastreboff, 1990). As such it does not have any long-term implications.
1.4. Hahituation-based treatment
In the neurophysiological model treatment is aimed at habituation of both nonspecific reactions induced by perception of tinnitus, and at habituation of the perception of the tinnitus-related signal before it reaches the cortex. Classically habituation is defined as the disappearance of the reaction to a given stimulus, without specifying what part of the reflex arc is responsible for this effect (Green, 1987) (principle iii). In the case of tinnitus the stimulus is an abnormal neuronal activity initiated for the most part in the cochlea or the auditory nerve, resulting, after extensive processing in the perception of phantom sound (tinnitus). In cases where tinnitus induces annoyance, the reaction covers a wide set of nonspecific responses such as fear, anxiety, anger, frustration, and depression. These responses reflect the involvement of the autonomic and limbic nervous systems, which can be activated from subcortical auditory centers (Swanson, 1987; Price, 1987), without perception of tinnitus. The annoyance evoked by tinnitus is dependent on these reactions and not on the psychoacoustical parameters of the tinnitus perception (Hazell et aI., 1985) (principles ii and iv).
From the neurophysiological viewpoint tinnitus annoyance results from activity within a reflex arc consisting of stimulus, its detection, and reactions. Habituation, defined as the disappearance of reaction, can result from modification of the reflex arc at two levels: i) at stimulus detection, and ii) between detection and reaction. The second process can occur independently from the first, while habituation occurring at the first level will automatically cause disappearance of reactions. In practice this translates into: j) disappearance of tinnitus perception from the patients consciousness (first mechanism), and consequently disappearance of reactions as well; and ii) tinnitus being still perceived unchanged but not causing annoyance anymore (second mechanism). The detachment of the emotional response from a stimulus is an essential requirement for habituation to occur (principle ii and iv). Therefore, direct counseling of patients aimed at providing them with the hest present knowledge of mechanisms of
tinnitus, to make it familiar, non threatening, and to remove commonly held fears, is an integral part of the treatment protocol. This is in contrast to the psychoacoustical approach in which counseling is ignored or treated as a separate, independent procedure, and where the effects of limited counseling occurring during the process of interaction with the patients are often classified as part of a placebo effect. Counseling alone can be effective in initiating the process of habituation of tinnitus in 20% to 40% of patients (Hazell et aI., 1985; lastreboff et aI., 1994; McKinney and Hazell, 1994; lastreboff and Hazell, 1993).
Once the stimulus looses its emotional significance, by not being reinforced in a positive or negative manner, the reaction initially induced by the stimulus gradually disappears - principle iv. This process can occur over time due to the absence of the stimulus, but is accelerated by repetition of the stimulus in the absence of reinforcement. In the case of tinnitus, removing the negative associations starts the process of habituation, since tinnitus is continuously present but negative reinforcement is absent. In the initial stages of treatment a decrease of autonomic reactions to the perception of tinnitus is frequently observed. This has been described by Hallam and others and is often a final goal in approaches based on cognitive therapy alone, where the aim is to teach patients to cope with their tinnitus (Jakes et aI., 1992; lakes et aI., 1986; Stephens et aI., 1986). The neurophysiological approach (Jastreboff, 1990; lastreboff and Hazell, 1993) has the more specific aim of total removal of the perception of tinnitus by inducing habituation at the perceptual part of the reflex arc.
For habituation to occur at the detection level it is helpful to introduce a low level auditory signal to interfere with the detection of tinnitus-related neuronal activity. The goal is to gradually retrain the neural centers involved in the detection of the tinnitus signal, to filter it out, stopping its passage to the cortical areas. Invoking additional low level, random neuronal activity within the auditory pathways makes it more difficult for neuronal centers to discriminate the tinnitus signal from normal spontaneous and evoked activity, by decreasing the signal to noise ratio. The neurophysiological model requires the tinnitus signal to be detected during this habituation process since it is impossible to retrain the brain reaction to a nonexisting stimulus. For this reason masking of tinnitus is counterproductive for achieving habituation. On the other hand, since there is no requirement to mask tinnitus, patients with unmaskable tinnitus can now be treated effectively. Theoretically, the most effective external sound should induce random activity in as wide a range of auditory neurons as possible and therefore broad-band noise is preferable. Other sounds, including appropriately used environmental sounds, can
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be as effective, and the prediction is that for the final outcome broad-band noise devices and hearing aids should be equally effective in facilitating habituation of tinnitus perception (Sheldrake and Hazell, 1992; Jastreboff et al., 1994), although the time course and speed of recovery is faster for broad band noise. The psychoacoustical model predicts that sounds which are not covering tinnitus are without any effect on tinnitus.
Clinical ouservation that there is only very weak correlation between loudness, minimal masking level and the level of annoyance evoked by tinnitus (Hazen et al., 1985) can not be explained by the psychoacoustical theory. Contrary to this the neurophysiological model states that the level of annoyance depends on the extent of negative emotions induced by tinnitus, which have no direct connection with the psychoacoustical description of tinnitus. Since treatment is aimed at the habituation of tinnitus perception, it is irrelevant what was the exact mechanism inducing abnormal tinnitus-related activity at low levels in the auditory pathways, i.e., if it results from noise-induced hearing loss, exposure to ototoxic drugs, extent and frequency dependence of hearing loss etc. Thus, the threshold and etiology of the hearing loss is irrelevant for prediction of the outcome of habituation-based treatment of tinnitus. Also it is intuitive that the louder the tinnitus and the more difficult to mask, the more resistant it will be to any kind of treatment. The psychoacoustical approach would have the same prediction, and in addition with patients where it is impossible to mask tinnitus, they cannot be entered into therapies based on the masking of tinnitus.
Additionally, contradictive predictions are made by psychoacoustical and neurophysiological theories regarding changes of tinnitus loudness and minimal masking level in patients during the treatment. According to the psychoacoustical approach, masking of tinnitus should not have any long-term effects on tinnitus loudness and maskability, since the tinnitus generator should not be affected by the presence of an external auditory stimulus. In the case of methods aimed at attenuating the tinnitus generator, i.e., by the use of the drugs, the loudness of tinnitus should decrease, followed by a corresponding change in maskability, reflecting the lower level of tinnitus needed to be masked.
The neurophysiological model postulates that a decrease in the level of annoyance can be achieved without any changes in loudness or maskability of tinnitus (habituation occurring at the effector part of the reflex arc). When habituation occurs at the detection part of the arc, the proportion of time when patients are aware of tinnitus should decrease. However during periods when it is perceived, it might have the same loudness and maskability as previously, since the source of tinnitus is not affected by the treatment aimed at
filtering out and stopping transmission of the tinnitusrelated neuronal activity to cortex.
Minimal masking level measures the ability of neuronal networks to detect the tinnitus signal in the presence of additional evoked activity. Since during the process of habituation these neuronal networks will be detuned from recognizing the presence of the tinnitus signal, lower levels of external masking noise should be sufficient to suppress tinnitus detection. Accordingly. the theory predicts that minimal masking level should be the best indicator of changes occurring in the central processing of tinnitus-related neuronal activity, since it reflects the detectability of these signals from the noise of spontaneous and sound-evoked neuronal activity. Perceived tinnitus loudness may still he the same, since once tinnitus is detected and the tinnitusrelated signal is transmitted centrally, its loudness will be evaluated by separate neuronal centers (Phillips, 1987), However initial minimal masking level levels will not be able on their own to predict treatment outcome, particularly.
1.5. The aim
The purpose of this study was to evaluate the validity of predications of the neurophysiological model by re-examining data obtained in a previous multicenter trial of tinnitus management (Hazell et al., 1985), focusing on alterations in tinnitus maskability in relation to the final outcome of the treatment. In the previous study the effectiveness of a therapeutic masking procedure for tinnitus management was examined. Although patients were instructed to adjust the level of broad band noise to cover their tinnitus, over half of patients used a level of noise BELOW that required to mask their tinnitus. Importantly, these patients exhibited a high level of improvement. This finding, as well as the observation of the high level of effectiveness of hearing aids, which could not be explained by traditional psychoacoustic theory (Coles, 1987; Vernon and Meikle, 1981; Vernon and Schleuning, 1978; Vernon, 1977), has been explained by the neurophysiological model of tinnitus, involving the process of habituation (Jastreboff, 1990).
This paper presents data showing that although the psychoacoustical description of tinnitus, i.e, minimal masking level and intensity match, as well as the threshold of hearing, have no predictive value for treatment outcome, nevertheless, for patients reporting improvement in their tinnitus, the minimal level of wide band noise needed to make tinnitus inaudible decreased, while the opposite occurred in those patients who reported no change or worsening of their tinnitus over the trial period. These findings are in agreement with the predictions of neurophysiological theory of tinnitus (Jastreboff, 1990).
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2. Methods
Data published previously (Hazell et ai., 1985) has been reanalyzed to test the proposed hypothesis. Patient selection and evaluation have been described in detail already (Hazell et aI., 1985), and therefore only a brief outline is provided here. Patients with a primary complaint of tinnitus were selected from Otolaryngology clinics at three hospital centers in the UK: Royal Ear Hospital, London; Royal National Throat Nose and Ear Hospital, London; and General Hospital, Nottingham. Patients came from all over the UK and there were no exclusion criteria, apart from having an adequate understanding of the English language as used in the questionnaires.
472 patients were entered into the trial with 382 reaching the first evaluation period 6 months later. This period only is the subject of the current study, although data collection continued for a further 6 months. The first evaluation period occurred at 9 months for a control group of 69 patients (at the Royal Ear Hospital only) in whom fitting of prosthetic devices was delayed for 3 months in an attempt to measure the effects of the initial counselling sessions alone. A total of 365 patients completed questionnaires and tests in a manner making them suitable for this present study. The first data set referred to as 'before' in this study, is the same as that of the initial data set described in Hazell et al., 1985. The data set referred to as 'after' in this study is the same as that of the first evaluation session of Hazell et ai., 1985.
Of 365 patients, 213 were fitted with maskers, 64 with hearing aids, 74 with combination instruments (combined hearing aids and maskers) and 14 with separate hearing aids and maskers to be used concurrently. In the present analysis, 'ALL' means combined data from all the patients in these 4 groups. For comparisons of masker and hearing aids groups, the results of those fitted with combination instruments and those using maskers and hearing aids concurrently have been excluded. For the purpose of the present analysis the 'tinnitus ear' is defined as the ear in which the tinnitus was heard most prominently (i.e., cases of asymmetrical bilateral tinnitus were included), and the audiometric test results used relate to tests performed on the tinnitus ear alone.
Post aural hearing aids, available under the UK National Health Service at that time, were fitted on ear moulds, with appropriate venting. Wherever possible open moulds were employed leaving the ear canal unoccluded. particularly in normal or near normal hearing subjects. Occlusive moulds were used only where there was a severe hearing loss, and in other cases moulds were vented as widely as was practicable. Masking devices were of two different types, Viennatone AM/Ti and A and M, selected for the stability
and broadband frequency characteristics of the noise they produced, and all were subjected to further quality control by spectral analysis, before use.
The wide band noise use in testing patients was the speech masking noise provided on a Peters AP6 audiometer. This same model of audiometer was used at each center and particular attention was paid to careful and regular calibration. At each center the same audiometer was used for all testing of subjects. Wide band noise intensity match was performed in the following manner: using an ascending procedure (to avoid tinnitus modification), wide band noise was presented through headphones well below the estimated perceived tinnitus loudness, and increased in 5 dB steps. Subjects were asked to indicate the moment when the noise was of equal loudness to the tinnitus and this level expressed as dB HL. Subjects were instructed not to be concerned that the audiometric noise was different in quality to their tinnitus. Minimal masking levels were measured as dB HL in the following manner: wide band noise was presented in a similar manner in ascending 5 dB steps until the subject indicated the first moment that the tinnitus had disappeared, or when the noise first 'covered the tinnitus'.
Counseling of the subjects was minimal, compared to our present clinical approach. Those fitted with maskers were instructed to: a) insert the masker and turn the volume up so that the noise just covers the tinnitus, b) wear the masker as often and for as long as possible, c) understand that the masker will not cure tinnitus but may replace it with a more acceptable sound, and d) expect that short periods of remission from tinnitus may occur (so called 'residual inhibition', (Feldmann, 1988; Vernon and Schleuning, 1978; Vernon, 1977; Feldmann, 1971)).
Although this approach to the use of wide band noise in tinnitus therapy has been superseded by modern techniques of retraining therapy in our practice (Jastreboff and Hazell, 1993), it is important to realize how masking of tinnitus was being implemented by subjects in this study. Subsequent analysis of the data showed that over half the patients were either unable or unwilling to cover their tinnitus with masking noise. Of those whose tinnitus improved during the trial 38% were using a level of noise below that needed to mask their tinnitus, despite instructions to the contrary. In this paper the devices are therefore described as 'noise generators' rather than 'maskers', so that the way in which they are used by patients is not inferred from their name.
3. Data analysis
The analysis in this present study has been performed on the original data maintained in an SPSS
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systems file at University College London. In the past we have attempted to equate various descriptive parameters of tinnitus complaint with psychoacoustical measurements without establishing any clear relationship (Hazell et aI., 1985). In this analysis we have decided to divide all our results into two major categories: i) patients who were reporting an improvement of
any kind (the 'Better' group). ii) patients who reported their tinnitus to be the same
or worse (the 'No-Better' group). Combining 'the same' and 'worse' subgroup into
one 'No-Better' group resulted from the reasoning that both lack of improvement and worsening of the symptoms reflect lack of habituation.
Another grouping was dependant on the type of device used: wide band noise generators, previously referred to as maskers (Hazell et aI., 1985), vs. hearing aids. Consequently, the population of patients was divided into four categories by Better/No-Better, and noise generators/hearing aids divisions.
The following psychoacoustical variables were analyzed: i) minimal masking level; ii) intensity match for wide band noise; and iii) threshold of hearing for wide band noise. We decided against reanalyzing the pitch of tinnitus (or using other measurements dependent on it), since pitch measurement is notoriously unreliable under normal clinical conditions (Penner and Bilger, 1992; Tyler and Conrad-Armes, 1983a) and neurophys-
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The data were analyzed using two approaches. The initial distributions of minimal masking levels, intensity match, threshold of hearing, and their means, for Better/No-Better, ALL, noise generators/hearing aids groups were analyzed by Smirnov test, and ANOV A followed by Student's t-test, for distributions and means respectively. This allowed for assessment of the predictive value of minimal masking level, intensity match, and threshold of hearing for the treatment outcome as well as for checking for potential bias in the initial grouping of subjects. The relation of the effect of treatment with psychoacoustical evaluation has been assessed by the analysis of the distributions of the changes of psychoacoustical parameters evaluated for each individual subject, for various subpopulations of subjects. The majority of subjects were measured before and after the treatment, nevertheless sometimes only one measurement was obtained decreasing the size of some subpopulations.
The differences of minimal masking levels, intensity match, and threshold of hearing were calculated by subtracting the initial value from the one measured after six months of a treatment. An analysis of distributions of each variable was performed. Since data sets do not fulfill requirement of the normality of the distributions, their analysis was based on the two sample Smirnov test (Conover, 1980). ANOVA and Stu-
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Fig. 1. Characterization of the initial minimal masking level (MML). The minimal masking level values have been categorized depending on treatment outcome (Better - crossed bars and continuous lines; No-Better - open bars and dashed lines), and type of device used (ALL - all devices; NO - noise generators, HA - hearing aids). Bars represent the means with SEM. Other panels show the cumulative distributions of the percentage of patients who had minimal masking level less/equal to a given value on the horizontal axis. Note the lack of difference between Better vs. No-Better groups.
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dent's t-tests were performed as a secondary, when the Smirnov test indicated the presence of differences in distributions, to assess the significance of the changes of means.
4. Results and discussion
4.1. Initial population
A total of 365 patients fulfilled the criteria described in Methods and werc analyzed in this study. There were 128, 85, 34, 30 subjects in noise generators and Bctter, noise generators and No-Better, hearing aids and Better, and hearing aids and No-Better groups, respectively. 88 cases were fitted with combination instruments. or hearing aids and noise generators concurrently. and they are not shown as a separate group, but they are included in the 'ALL' group. This grouping of data has been adopted on the basis of reasoning that the ALL group shows the effect of sound therapy of any kind; noise generators represents the situation with controlled artificial sound; hearing aids therapy is based on the enhancement of the environmental sounds. In the groups with combination instruments or concurrent use of hearing aids and noise generators it is not possible to separate thc effect of artificial noisc and amplificd environmental sounds.
No a priori knowledge was available regarding treatment outcomc, and the approach, i.e., noise generators or hearing aids, was decided on the basis of patient
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evaluation or random allocation (at Royal National Throat Nose and Ear Hospital). As such, the division of the initial patient population into groups depending on the treatment outcome (Better vs. No-Bettcr) should be random. Therefore, initial distributions of minimal masking levels, intensity match and threshold of hearing analyzed before treatment for Bettcr vs. No-Better should bc statistically identical. The results presented in Figs. 1-3 reveal that the means and distributions of the initial values of minimal masking levels, intensity match, and threshold of hearing are statistically indistinguishable for Better vs. No-Bcttcr outcomes.
The data for minimal masking levels before treatment grouped for ALL, noise generators, hearing aids, Bettcr (crossed bars and solid lines), and No-Bettcr (open bars and dotted lines), are presented in Fig. 1. The left top panel shows the mean and SEM values for: ALL group of 344 cases (200 Bettcr vs. 144 NoBetter), 193 with noise generators (! 14 vs. 79), and 60 with hearing aids (32 vs. 28). Thc rcmaining panels show the cumulative distribution of minimal masking lcvel values for ALL, noise generators, and hearing aids groups. As can be secn, these data show no differcncc along aBetter INo-Bctter division. and this is confirmed by statistical analysis.
Analysis of variance showcd that thcrc is a significant difference between noise gencrators and hearing aids (F[I,249] = 6.93, P < 0.01); no difference between Better vs. No-Better groups (F[1.249] = 0.64, P> 0.2); and interaction at the border of significance (F[ 1 ,249] = 3.79, P = 0.(53). The comparison of the individual
% ALL 100
80
60
40
20
OL-~~--~ ______ ~ __ ~~
% 100
80
00
40
cO
()
o 20 40 60
HA
Y (l 20 40 60
go
1M
so 1M
Fig. 2. Characterization of the initial intensity match (1M). All the descriptions as in Fig. I. Note the lack of difference between Better y,.
No-Better groups.
224 P.J. iaSlrcbot( elal. / Hcarinr; Research 80 (1994) 2/6-232
means performed for Better vs. No-Better subgroups show for: ALL group 39.9 and 37.3 dB HL (t[342] =
1.13, P> 0.2); noise generators 33.1 and 33.9 dB HL (t[191] = - 0.26, P> 0.2); hearing aids 46.5 and 35.4 dB HL (t[58] = 2.17, P < 0.05). The analysis of cumulative distribution shows maximal difference between Better vs. No-Better distributions for: ALL group 10.2% (P> 0.2, Smirnov test); noise generators 9.1 % (P> 0.2); hearing aids 38.4% (P < 0.05). The medians for Better vs. No-Better groups were: ALL 37.9 and 33.9 dB HL; noise generators 29.8 and 30.4 dB HL; hearing aids 43.1 and 29.4 dB HL.
Fig. 2 presents intensity match data. Analysis of variance showed a significant dependence from the instrument used (F[I,256] = 18.57, P < 0.001); lack of significance for Better vs. No-Better effect, and for interaction of the main effects (F[I,256] = 0.36, P> 0.2; and F[I,256] = 2.85, N.S.). The comparison of the individual means for Better vs. No-Better subgroups show for: ALL group 25.8 and 24.3 dB HL (t[359] = 0.68, n1 = 216, n2 = 145, P> 0.2); noise generators 18.3 and 19.1 dB HL (t[196] = - 0.32, n1 = 120, n2 = 78, P> 0.2); hearing aids 32.8 and 25.0 dB HL (t[60] = 1.67, nl = 34, n2 = 28, N.S.). The analysis of cumulative distribution shows maximal difference between Better vs. No-Better distributions to be for: ALL group 9.6% (P> 0.2, Smirnov test); noise generators 5.2% (P> 0.2); hearing aids 34.2% (P = 0.055). The medians for Better vs. No-Better groups were: ALL 23.4 and 18.3 dB HL; noise generators 17.5 and 15.6 dB HL; hearing aids 30.6 and 18.0 dB HL.
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Analysis of threshold of hearing for wide band noise is presented in Fig. 3. Analysis of variance showed a significant dependence from the instrument used (F[1,251] = 23.75, P < 0.001); lack of significance for Better vs. No-Better effect, and for interaction of the main effects (F[1,251] = 0.44, P> 0.2; and F[I ,251] =
0.81, P> 0.2). The thresholds for Better vs. No-Better groups were: ALL group II.H and 9.6 dB HL (t[356] =
1.04, nl = 215, n2 = 143, P> 0.2); noise generators 3.5 and 3.2 dB HL (t[I92] = 0.14, nl = 118, n2 = 76, P> 0.2); hearing aids 15.8 and 11.6 dB HL (t[59] = 0.90, n 1 = 33, n2 = 28, P > 0.2). The analysis of cumulative distribution shows maximal difference between Better vs. No-Better distributions for: ALL group 9.0% (P > 0.2, Smirnov test); noise generators 7.4% (P > 0.2); hearing aids 12.2% (P> 0.2). The medians for Better vs. No-Better groups were: ALL 4.6 and 3.9 dB HL; noise generators 0.0 and - 1.0 dB HL; hearing aids 11.3 and 7.0 dB HL.
The comparison of minimal masking level, intensity match, and threshold of hearing for Better vs. No-Better subgroups shows no statistical significant differences, except borderline tendency for the hearing aids group. It is interesting that minimal masking levels mean and median values were higher for the Better subgroup. Although it could be expected that subjects from hearing aids group have higher minimal masking level values (in dB HL), due to the tendency of fitting subjects with hearing loss with hearing aids, but according to a psychoacoustical model the Better subgroup should have the same or lower value of minimal mask-
% ALL 100
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% HA 100 ... ~
! 20 -;
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Fig. 3. Characterization of the initial threshold of hearing (TH). All the descriptions as in Fig. 1. Note the lack of difference between Better vs. No-Better groups.
p.I. lastreboff et al. / Hearing Research 80 (1994) 216-232 225
ing level than No-Better subgroup. A possible explanation may be that patients fitted with hearing aids and having greater hearing loss benefit more from enhancement of environmental sounds because their auditory systems were deprived of sound to a larger extent than patients with only moderate hearing loss. The use of hearing aids resulted, therefore, in a greater amount of change in neuronal activity within the auditory pathways. Results of threshold of hearing presented in Fig. 3 fully support this explanation. Selection criteria used in this study resulted in fitting patients with significant hearing loss with hearing aids rather than with noise generators. As such, the difference for Better vs. NoBetter groups for hearing aids users can be attributed to selection criteria. The results indicate that patients with larger hearing loss and higher minimal masking level might be more likely to benefit from hearing aids use, nevertheless, since this tendency is not statistically significant it might well reflect a random fluctuation.
The data presented in Figs. 1-3 and their statistical analysis strongly support the postulate that initial psychoacoustic parameters of tinnitus, i.e., its minimal masking level and intensity match, have no value for predicting treatment outcome. Notably, even for high minimal masking level and intensity match some patients got hetter, while other patients with low minimal masking level and intensity match showed no improvement. If there was a relation between the psychoacous-
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tical description of tinnitus and treatment outcome, then the distributions for Better vs. No-Better groups should differ significantly; for example, due to the lack of improvement for patients with high values of minimal masking level or intensity match and the high proportion of patients improving who have low values of these parameters. The fact that the Better vs. NoBetter distributions are statistically indistinguishable (F values from ANOV A close to 1, and probabilities from Smirnov test above 0.5) proves that there is no relation between minimal masking leveL intensity match, threshold of hearing and the treatment outcome. These results argue against a psychoacoustical model, according to whieh the outcome should depend on maskahility and loudness of tinnitus, hut are consistent with neurophysiological theory.
Finally, since these groups were originally statistically indistinguishable, any differences detected after the treatment can be related to its effects, rather than to the initial bias in the data.
4.2. Effects of treatment
The distribution of changes in minimal masking level, depending on the treatment outcome, for ALL patients and for noise generators and hearing aids treatment categories are presented in Fig. 4. The most noticeable point is an opposite direction of change
-40 -20 o 20 40
t..MML
% HA 100
7S
SO
25
~ 0
-40 ·20 o 20 40
t..MML
Fig. 4. Change, of minimal masking levels. The changes have been calculated for individual patients {after value, minus before} and averaged for a given subpopulation of patients. Crossed bars and solid lines represent groups of patients who reported improvement in their tinnitus after 0 months; open hars and dashed lines represent patients who did not report improvement. Note that all treatment subgroups of the Better group show a decrease of minimal masking level (negative change of minimal masking level). About 75% of patients exhibited a negative change of minimal masking level, as shown on the cumulative distrihutions, while patients in the No-Better group exhibited an increase of minimal masking level with an equal number of cases with increased and decreased minimal masking level.
22h P.l. lastrehof( et ill. / Hearing Research 80 (19941216-232
occurring for all Better vs. No-Better subgroups. Minimal masking level decreased in patients who reported improvement in their tinnitus in the course of treatment, while it increased in the No-Better group. The means of changes for Better and No-Better groups were: ALL - 5.3 dB (t[114] = 4.25, P < 0.001, Student's t-test for correlated data) and 4.87 dB (t[94] = 2.30, P < 0.05); noise generators - 6.0 dB (t[67] = 3.20, P < O.OJ) and 3.6 dB (t[48] = 1.14, P> 0.2); hearing aids - 6.3 dB (t[15] = 2.38, P < 0.05) and 6.2 dB (t[18] =
1.13, P > 0.2). Analysis of variance showed highly significant differ
ence for Better vs. No-Better situation (F[1,148] =
11.29, P < 0.001), while both the effect of instruments and the interaction were not significant (F[1,148] =
0.10, P> 0.2; F[1,148] = 0.16, P> 0.2). Direct comparison of changes for between Better vs. No-Better groups shows for : ALL 10.2 dB (t[208] = 4.28, P < 0.001); noise generators 9.6 dB (t[115] = 2.76. P < 0.01); hearing aids 12.5 dB (t[33] = 1.94, P = 0.06).
The cumulative distributions of this data are presented in Fig. 4. Analysis of distribution of changes for all patients revealed that in both Better and No-Better groups there are patients with a maximal shift in minimal masking level of ± 40 dB. The largest number of patients show change of minimal masking level in the range of - 25 dB to + 15 dB. For the ALL group there is a clear shift of the Better group to the left by 8 dB, indicating a larger proportion of patients with decreased minimal masking level after treatment as compared to the No-Better group. 73.9% of the Better group showed the decrease of minimal masking level,
Ll TH dB HL
% ] 00
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60
40
20
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ALL
·20 .] 0
NG HA
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rf~ .j
Il ]Il 20 Ll TH
i.e., negative change of minimal masking level. against 50.5% for No-Better group, which is close to the chance level of 50%. Analysis of cumulative distributions revealed a maximal difference of 27.9%. which is highly statistically significant (z = 2.01, nl = 115, n2 = 95. P
< 0.001, Smirnov test). It is noteworthy that there are 12.3% of cases in the
Better group where improvement was reported despite an increase of minimal masking level by 5-40 dB. Similarly, there are 10.5% of cases in No-Better group where there was no improvement despite a decrease of minimal masking level by 20-45 dB. This suggests that factors other than modification of maskability, for example, influencing the processing of the tinnitus signal by neuronal centers involved in evaluation of the emotional relevance of this signal, as well as temporal variability of the tinnitus signal, are important for the perceived significance of tinnitus. Nevertheless, evaluation of minimal masking level revealed that 73.9% of patients who are showing tinnitus improvement exhibit a decrease in their minimal masking level. Both the importance of central processing and evaluation of tinnitus for its perceived annoyance, and the modification of minimal masking level as an effect of treatment are as suggested by the neurophysiological theory (J astreboff, 1990).
The same trend was observed after extracting from ALL data the noise generators and hearing aids treatment groups (Fig. 4). Interestingly, both the noise generators and hearing aids groups did not differ substantially. As the numbers in the hearing aids group are much smaller than in noise generators, the results
% ALL ] 00
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60
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20
0 -20 -] 0 o 10 20
Ll TH
HA
Insufficient data
Fig. 5. Changes in threshold of hearing. All descriptions as in Fig. 4. Note the lack of difference between Better and No-Better groUpii.
P.l. lastreboJJ et at. / Hearing Research SO (]994) 216-232 227
for the ALL group were dominated by the noise generators group. Accordingly, in the noise generators group 75% of subjects showed decrease of minimal masking level in the Better vs. 55.1% in the No-Better group. The Smirnov test revealed a significant difference between distributions (maximal difference 26.7%, Z =
1.43, n I = 68, n2 = 49, P < 0.05). The medians are - 6.7 and - 0.6 dB for Better and No-Better groups respectively. In the hearing aids group the difference between Better and No-Better groups is even more pronounced, with 81.3% showing a decrease of minimal masking level in Better vs. 47.4% in the No-Better group. The difference between the Better and No-Better group is statistically significant (maximal difference 47.4%, z =
1.40, nl = 16, n2 = 19, P < 0.05). The results for minimal masking level show that
when the population of patients is divided into two sets, on the basis of the simplest classification of treatment outcome, into Better INo-Better categories, minimal masking level in patients with improvement tends to decrease, while in patients whose tinnitus remained the same or worsened, minimal masking level increased. Since distributions of minimal masking level before treatment did not exhibit significant differences. these changes may be related to treatment.
Evaluation of changes of the intensity match of tinnitus did not reveal the presence of any significant change (Fig. 5). The following mean changes were observed for Better vs. No-Better: ALL 1.4 vs. 1.4 dB (t[112] = 0.01, P> 0.2); and noise generators l.5 vs. l.2 (t[71] = 0.l2, P> 0.2). The hearing aids group was too small to allow for analysis. A comparison of distribu-
tl 1M dB HL
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tions of changes of intensity match revealed that they are statistically indistinguishable: ALL maximal difference 9.9% (z = 0.52, n1 = 65, n2 = 49, P> 0.2); noise generators maximal difference 12.7% (z = 0.10, nl = 47, n2 = 26, P > 0.2).
To assess possible changes in hearing during the treatment period, which might affect minimal masking level and intensity match measurements, we analyzed threshold of hearing in the same way as with minimal masking level (Fig. 6). Comparisons of the means of change showed for Better vs. No-Better subgroups: ALL 1.7 vs. 1.2 dB (t[149] = 0.25, P> 0.2); and noise generators 2.3 vs. 1.4 dB (t[86] = 0.42, P> 0.2). The hearing aids group was too small to allow for analysis. Comparison of the cumulative distributions indicate that the distribution of changes for Better vs. No-Better groups are statistically indistinguishable: ALL maximal difference 4.5% (z = 0.26, n 1 = 85, n2 = 66, P> 0.2); noise generators maximal difference 6.5o/r. (z =
0.30, n1 = 53, n2 = 35, P> 0.2). All of the above results fail to show any significant change in threshold within 6 months of treatment. This argues against the interpretation that observed changes in minimal masking level during the treatment are contaminated by changes in the subjects' hearing.
4.3. General discussion
Three main findings emerged from this study. Firstly, the outcome of treatment was not related to initial values of psycho acoustical parameters describing tinnitus or to subject hearing loss, i.e .. minimal masking
% ALL 100
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HA
Insufficient data
Fig. 6. Changes in intensity match. All descriptions as in Fig. 4. Note the lack of difference between Better and No-Better groups.
P.1. ./astrebojf er al./ Hearing Research SO (191.)41 210-232
level, intensity match, and threshold of hearing. Secondly, minimal masking level exhibited significant changes during the treatment period and, depending on the outcome of treatment, decreased for the group showing improvement and increased for the group with tinnitus remaining the same or getting worse. Thirdly, the type of device used, i.e., noise generators or hearing aids, was irrelevant for final outcome, and changes in minimal masking level were similar for both treatments.
The observation that there is no relation between the initial value of tinnitus intensity match and minimal masking level is counter-intuitive. A reasonable expectation is that if tinnitus is louder and its minimal masking level is high, then it will be more difficult to relieve patients from its effects. This reasoning is based on the psychoacoustical approach to tinnitus as a phenomenon contained within the cochlea, which might be alleviated by masking the tinnitus generator. Consequently, louder tinnitus would be more difficult to mask, and the probability of relieving patients from tinnitus should be smaller, or nonexistent for patients with tinnitus which cannot be masked at all.
Contrary to this model, the neurophysiological approach to tinnitus postulates that processing of the tinnitus signal by the nervous system plays a dominant role in its detection, perception and evaluation, with the strength of a cochlear tinnitus generator being of secondary importance in tinnitus intrusiveness (Jastreboff, 1990; lastreboff and Hazell, 1993). Furthermore, habituation should occur even in the presence of a relatively strong peripheral signal, as factors not related to tinnitus psychoacoustic characterization (i.e., extent of the threat created by tinnitus, general stress level, and temporal variability of the tinnitus signal) will determine the presence and extent of the habituation process.
Accordingly, initial values of minimal masking level, intensity match, and threshold of hearing are of secondary importance compared to these factors and do not have a decisive influence on the treatment outcome. It must be stressed therefore that they should not be used for determining the suitability of any treatment or predicting its outcome. Results presented in Figs. 1-3 and their analysis fully support this postulate.
While the initial psychoacoustical characterization of tinnitus is not helpful in predicting the treatment outcome, it can be useful in monitoring the process of recovery for a group of patients when combined with subjective evaluation of changes in tinnitus intrusiveness (J astreboff and Hazell, 1993), and can provide the means for more objective monitoring of the effectiveness of treatment. The authors are not aware of any other data from such a large population of patients providing a strong link between outcome of treatment
and psychoacoustical description of tinnitus. The~c
changes are significant for the group when described a~ a difference over the duration of the treatment period for a given patient. The changes are small, averaging a few dB, as compared with the larger absolute value .... for minimal masking level.
These changes are too small to have an impact on the subjective evaluation of tinnitus by an individual patient, but they can be used for evaluating the effectiveness of various new treatments on a group of patients. This concept is strengthened by the fact that in both Better and No-Better groups we have changes of minimal masking level ranging from - 50 to + 50 dB disregarding the treatment outcome. Some patients exhibiting a large reduction of minimal masking level of up to 50 dB were not experiencing improvement of tinnitus, while other patients on whom we measured a significant increase in these parameters, nevertheless reported an improvement in their tinnitus. This observation is in total agreement with the theoretical predictions and everyday clinical practice, and stresses the importance of other factors being decisive for the process of tinnitus habituation Uastreboff, 1990; lastreboff and Hazell, 1993). Nevertheless, observation of change in the minimal masking level related to treatment is important because it provides us with insight into the changes that are occurring in the auditory system during the course of treatment and allow for validation of different theories of the mechanism of tinnitus and its therapy. Assuming that the tinnitus generator is not being significantly affected by the use of noise generators or hearing aids, which is supported by unchanged intensity match, then a decrease in minimal masking level would indicate that the same tinnitus related signal is not detected as easily as it was before (J astreboff, 1990; lastreboff and Hazell, 1993).
The data presented here are in total agreement with the prediction of the neurophysiological model, showing that patients who reported a subjective improvement in their tinnitus exhibited a clear and statistically significant decrease in their minimal masking level. Significantly, the patients from the No-Better group show an increase of their minimal masking level, suggesting that detection of the tinnitus signal has been enhanced during the unsuccessful treatment period. This is in agreement with the concept of habituation, and the importance of aversive components in tinnitus perception, with failure of treatment adding to the negative qualities associated with tinnitus. Once a threatening connection has been established. the detectability of the tinnitus pattern should further increase due to its everyday presence. Dynamic aspects of processing and filtering of an auditory signal by the nervous system act against stable, unchangeable situations; i.e., signals are either habituated or their detectability increases (Lara and Arbib, 1985).
P.l. lastreboff et al. / Hearing Research SO (1994) 216-232 229
During the treatment period there are no significant changes in threshold of hearing to wide band noise. In addition, frequency-specific evaluation of hearing (not shown) did not reveal the presence of changes in hearing threshold. These observations show that minimal masking level and intensity match measurements were not affected by a threshold shift. Lack of changes in threshold of hearing further argues against any progressive cochlear pathology occurring during the treatment period, induding eventual noise-induced hearing loss resulting from the everyday use of noise generators or hearing aids. Absence of any relation of the treatment outcome to threshold of hearing further argues against the simplistic association of tinnitus with cochlear pathology without induding the effects of tinnitus signal processing by the nervous system.
The loudness data did not show the presence of any treatment-related changes. The cochlear theory requires that changes in minimal masking level and intensity match are positively correlated, since the same physical locus, the cochlear tinnitus generator, is modified. Neurophysiological analysis predicts weak, if any, correlation, since different centers are involved in the threshold of signal detection - minimal masking level, vs. evaluation of its loudness - intensity match. Thus changes in minimal masking level and intensity match are not necessarily correlated, as minimal masking level is directly related to the ability of the system to habituate to the tinnitus signal while intensity match is of significance only in extreme cases. The data presented in Figs. 4 and 5 fully support the neurophysiological approach and are contrary to the prediction of the cochlear model, since minimal masking level has changed significantly in a manner related to the treatment outcome, while analysis of intensity match did not reveal the presence of any clear changes.
The comparison of the effectiveness of noise generators and hearing aids as treatments revealed that both are equally effective on properly selected subpopulations of patients (Fig. 4). This observation is difficult to explain on the basis of a psychoacoustical approach to tinnitus, which would suggest the need for the masking sound to have similar frequency to the tinnitus, and thus emphasize the importance of specific frequency characteristics of the masking sound. According to the neurophysiological approach, the frequency spectrum of an additional external sound is secondary; any stable sound with a sufficient wide spectrum should be equally effective. This postulate results from the reasoning that to induce and further facilitate the process of habituation of tinnitus perception, it is necessary to: i) detach perception of tinnitus from aversive associations, which prevent habituation from occurring, by directive counseling (cognitive therapy as a part of the treatment); and ii) provide the auditory system with an additional signal, which will interfere with the detection, percep-
tion and evaluation of the tinnitus-related signal (Jastreboff, 1990; lastreboff and Hazell, 1993). The important aspects of this interfering signal are: i) a wide band of frequency aimed at providing a mild stimulation of the entire population of neurons within the auditory pathways; ii) a sound which should not evoke negative, aversive reactions, which would prevent habituation; iii) a sound which should not mask tinnitus, since making tinnitus inaudible would prevent retraining of the centers involved in tinnitus detection, and would therefore hinder the process of habituation; iv) the sound should not fluctuate, which would attract the subject's attention and induce aversive reactions. This signal can be provided by a wide band of noise of the type emitted by tinnitus maskers or by appropriately amplifying sufficiently rich environmental sounds with hearing aids.
There are a number of other tinnitus puzzles which have been explained by the neurophysiological model, such as the rapid onset of tinnitus but its much slower attenuation, the variable effectiveness of contralateral masking, tinnitus masking by tones from a wide range of frequencies, its resistance to masking (Jastreboff, 1990), but since they are not directly related to material presented in this paper, they are not elaborated here.
In the past, a number of specific theories have been proposed. These theories focus on potential processes which might generate a tinnitus signal c.g. dctachment of hair cell cilia from the tectorial membrane (Tonndorf, 1981), cross talk between auditory nerve fibers (M0ller, 1984; Eggermont, 1990), enhancement of activity due to the edge effect (Kiang et al., 1970; Salvi et al., 1983; Salvi and Ahroon, 1983; Penner, 1980) and the theory based on the analogy of tinnitus with pain (Tonndorf, 1987). These theories might be completely correct in terms of initiating a number of events leading to perception of the tinnitus sound, and do not in any way contradict the neurophysiological model. This model is invariant from the specific process initiating tinnitus, but stresses the importance of processing the initial tinnitus signal and the involvement of other neuronal systems outside the auditory pathways for the perception of tinnitus and the level of annoyance induced by tinnitus.
Recently, the significance of central processing of tinnitus has been pointed out by other authors (M0l1er et al.. 1992b; M0ller, 1992; Pujol, 1992; Romand, 1992; Dupont et aI., 1992). In his recent theory M0I1er emphasized the role of the extralemniscal pathways, and multisensory system integration in tinnitus emergence (M0I1er, 1992). He argued that the extralemniscal pathways are involved in tinnitus emergence based on the following observations. First, recordings of compound action potentials directly from an exposed intracranial part of the VIII nerve did not show any difference
2-'0 P..l. .Iaslrehoff ('I ell. / Hearing Research SO (19941210-232
between groups of tinnitus and non-tinnitus patients, which argue against abnormal signals within the auditory nerve (M011er, 1992; M0ller et aI., 1992a). Second, latencies of peak V were slightly shorter in tinnitus patients, suggesting an area of termination of the laterallemniscus in the Ie. Interestingly, our work on the objective method of detecting tinnitus in humans by mathematical analysis of ABR, revealed shortening of the latency of peak V in tinnitus patients as well as changes in potentials with even longer latencies (Jastreboff et aI., 1992). Third, somatosensory stimulation of tinnitus patients resulted in changes in their tinnitus which can be mediated only through the extralemniscal system or association cortex, where interaction of auditory and somatosensory information occurs (M011er, 1992). The frequency dependence of observed effects up to 10Hz argues against the possibility of the involvement of the association cortex (M011er, 1992). Therefore the subcortical extralemniscal structures, predominantly the external nucleus and the dorsal cortex of the IC, are primary candidates to be investigated for involvement in processing of the tinnitus-related signal. Several other authors have stressed that tinnitus perception may persist even after the disappearance of peripheral tinnitus-related activity due to permanent modification of the central auditory pathways (Pujol, 1992; Romand, 1992; Dupont et aI., 1992; Attias et aI., 1993). Notably, recording of the auditory event related potentials (Nl, P2, P300) from tinnitus and matched non-tinnitus subjects revealed significant suppression of the amplitude of those potentials in tinnitus patients, supporting the postulate of limbic system and central processing involvement in tinnitus (Attias et aI., 1993)
In conclusion, the results presented in this paper show that although a psychoacoustical description of tinnitus does not possess predictive value for the outcome of the treatment, minimal masking level can be useful in monitoring the progress of treatment. Most notably, the results are consistent with the neurophysiological interpretation of mechanisms involved in phenomenon of tinnitus and its alleviation.
Acknowledgements
The work has been supported by NIH/NIDCD grant DC00299 (PJJ); the Royal National Institute for Deaf People grant 621-089 (JWPH); and a grant from the Hearing Research Trust 089:FER:JH (RLG).
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