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Theory and Treatment of Tinnitus and Decreased Sound Tolerance

Pawel J. Jastreboff and Margaret M. Jastreboff

Tinnitus and decreased sound tolerance are challenging topics in the practice of otolaryngology and audiology, as there is no established standard on how to evaluate and treat these conditions. There is ongoing research aimed at investigation of mechanisms underlying these phenomena and at evaluation of emerging treatments. Substantial progress has been achieved during the last decade in understanding tinnitus, and tinnitus and decreased sound tolerance are treated in an effective manner in an increasing number of centers. This chapter provides an overview of the current status of the field.

Definitions and Epidemiology

Tinnitus, commonly described as a ringing in the ears, can actually be perceived as a wide variety of sounds (e.g., ringing, buzzing, crickets, hissing). It is a phantom auditory perception,¹ that is, while the perception is absolutely real, there is no sound or vibratory activity within the cochlea corresponding to the perception.^2,3 The perception of tinnitus results from the presence of tinnitus-related neuronal activity within the auditory pathways. The prevalence of tinnitus is high. About 10 to 20% of people in the general population can perceive it any time that they focus attention on it,^4,5 but interestingly only about 4 to 8% of the general population is bothered by tinnitus to some extent.^6,7 It is difficult to determine the prevalence of clinically significant tinnitus (i.e., tinnitus that affects people to the extent that they need professional help) because many sufferers with troubling tinnitus cease to believe that something can be done to help them and consequently they no longer seek help. Clinical observations indicate that probably at least 1% of the general population suffers from clinically significant tinnitus and 0.5% are profoundly affected by it.²

Tinnitus has been linked to several medical problems such as conductive hearing loss (e.g., resulting from otitis media, cerumen impaction, ossicular stiffness/discontinuity, otosclerosis); sensory or neural hearing loss (e.g., related to Meniere’s disease, presbycusis, vestibular schwannoma, sudden hearing loss); hormonal changes (e.g., pregnancy, menopause, thyroid dysfunction); and administration of some medications or withdrawal from them.^8,9 Basically, a decrease of the auditory input to higher auditory centers due to any reasons (e.g., medical problem, hearing overprotection, work, or lifestyle) may induce tinnitus.² The classic experiment of Heller and Bergman¹⁰ showed that perception of tinnitus was evoked in 94% of normally hearing people without tinnitus who spent a few minutes in an environment with very low sound level. Recent data confirmed the presence of this phenomenon.¹¹

The prevalence of bothersome tinnitus is associated with the extent of hearing loss and increases with aging until age 65, when it stabilizes, and then decreases after age of 74.⁷ However, when hearing loss is taken into account, the prevalence of tinnitus decreases with age for any given level of hearing loss.⁷ Children experience and have problems with tinnitus to a larger extent than was previously assumed.^12–14 They typically do not complain about tinnitus, considering it a natural experience. When they are bothered by tinnitus, they have the same problems as adults. Unrecognized tinnitus may yield incorrect diagnosis of behavioral or learning problems.

In a psychoacoustic evaluation of tinnitus, its pitch-and- loudness match turned out not to be associated with its severity. Except for low pitch or a roaring tinnitus observed in attacks of Meniere’s disease, these assessment measures are not helpful for diagnosis or treatment planning. A minimal masking level (i.e., a minimal level of white noise that blocks the perception of tinnitus) might provide some indication of how easy it would be to mask tinnitus, when masking therapy is considered.¹⁵ On the other hand, the results reported by Penner and Bilger¹⁶ showed that to sustain masking of tinnitus for a more than a minute, it might be necessary to increase the sound level substantially (even by 40 to 50 dB over a 30-minute period). This observation demonstrates that a minimal masking level can be used only as an indicator of the effectiveness of masking therapy.

Residual inhibition, that is, a decrease of tinnitus loudness after exposure to intensive sound¹⁷ (recommended as 10 dB above minimal masking level) is another measure promoted as a part of tinnitus evaluation.¹⁸ Although there was considerable expectation, this measure never became useful clinically because residual inhibition, if present, typically lasts only seconds or a minute.² Moreover, typically an increase of tinnitus loudness is observed as a result of exposure to loud sound.

Strong somatosensory input to the auditory system has been clearly documented recently.19,20 It turned out that the input is both excitatory and inhibitory and that it exists at various levels of the auditory system, including the cochlear nuclei complex. This finding might explain why the majority of patients can modulate their tinnitus by manipulating the head/neck area and why it is possible to induce tinnitus by body manipulation in approximately 30% of subjects without prior tinnitus.²¹ It has been proposed that in some cases the somatosensory system might be responsible for tinnitus.²² So far this hypothesis has not yielded a clinically significant treatment, but the modulation of tinnitus with this manipulation has been used for research purposes.^23–25

In the past, somatosounds, that is, perception of the sound generated by the body,such as sound of blood flow, palatal myoclonus, or spontaneous otoacoustic emissions, were labeled as objective tinnitus and differentiated from subjective tinnitus, for which there was no detectable external sound. This categorization has the intrinsic problem of being dependent not on the mechanisms of tinnitus generation but on the technical ability to detect potential real sound, and it is gradually disappearing from the literature in the context of tinnitus. As it is typically difficult to diagnose somatosounds, their prevalence can be only estimated to be in the range of a few percent of all cases. The most common somatosounds are related to the heart beat, as they reflect changes in the speed of blood flow (e.g., great vessel bruits) or fluctuation of blood or cerebrospinal fluid (CSF) pressure. These sounds are typically perceived as pulsation (thus the name pulsatile tinnitus). Note that pulsation of loudness of tinnitus does not automatically indicate somatosounds. For example, the tinnitus source—which can be, for example, dependent on functional properties of the outer hair cell (OHC) system²—might be affected by CSF pressure, resulting in a fluctuation of tinnitus loudness, still without having any real acoustic signal. There are also nonpulsatile somatosounds, associated for example, with tensor tympani myoclonus, tensor veli palatini myoclonus, eustachian tube dysfunction,^8,26,27 perception of spontaneous oto-acoustic emissions (SOAEs),²⁸ or temporomandibular joint disorder.⁸ Perception of SOAEs is rare, but it is present in a small proportion of patients (typically young women with normal hearing).^29,30 It can be eliminated by administration of aspirin,³¹ which attenuates active properties of OHCs.^32,33 Furthermore, hearing loss or aging eliminates SOAEs due to accumulated OHC damage.

Auditory imagery (i.e., perception of distorted speech or music, sometimes labeled as musical hallucinations) is an interesting case of central tinnitus.³⁴ Although this phenomenon is not related to psychiatric problems,^35–38 it is sometimes confused with landmark hallucinations occurring in schizophrenia. It typically affects elderly women with hearing loss.

Tinnitus frequently is accompanied by decreased tolerance to sounds that would not evoke a similar reaction in the average listener.^8,39,40 Decreased sound tolerance should be taken into consideration when applying a treatment for tinnitus, as it contributes to enhancement of the tinnitus signal and has an impact on the implementation of sound therapy.^2,41 It has been proposed that two components of decreased sound tolerance should be distinguished: (1) hyperacusis and (2) misophonia.^8,39 In hyperacusis, sound-induced neural activity is overamplified within the auditory system, resulting in an abnormally strong reaction to sound occurring within the auditory pathways, and only secondarily affecting the limbic and autonomic nervous systems.⁸ This overamplification might occur inside of the cochlea, for example by too high a level of mechanical amplification being provided by OHCs, or by an abnormally high level of sound-evoked neurotransmitters released from inner hair cells (IHCs). Clinical observations suggest that central mechanisms are more prevalent and hyperacusis might result from an increased sensitivity of neurons in the auditory pathways.^39,42–44 The negative reactions to sound and their strength in hyperacusis depend strictly on the physical characterization of the sound, and reactions are independent of the context in which sound is presented.

Epidemiologic data on hyperacusis in the general population are limited. Nevertheless, a questionnaire study of 10,349 randomly selected people found that 15.3% reported decreased sound tolerance.⁴⁵ A random sample of 3049 subjects in Germany found that 1.72% reported hyperacusis.⁴⁶ Hyperacusis requiring treatment has been reported to accompany tinnitus in approximately 25 to 44%,^40,46,47 and tinnitus was reported to be present in 86% of hyperacusis cases.⁴⁸ On the basis of these numbers, it is possible to estimate that at least 1.5% of the general population has hyperacusis requiring treatment.

Hyperacusis has been linked to a number of medical problems, such as Bell’s palsy, Lyme disease, Williams syndrome, Ramsay Hunt syndrome, stapedectomy, perilymphatic fistula, head injury, migraine, depression, withdrawal from benzodiazepines, increased CSF pressure, and Addison’s disease^48,76–88 Treatments of these medical problems may help with hyperacusis; for example, treating Lyme disease or implementing gradual withdrawal from benzodiazepines can be effective.^2,49

Misophonia, the dislike of sound, is the second component of decreased sound tolerance and reflects conditioned negative reactions to sound.^8,39 It is a relatively new concept that originated from our observation that many patients were avoiding and disliking sounds, while not necessarily being afraid of them. A variety of negative emotions are involved in misophonia. Phonophobia is considered to be a specific case of misophonia when fear is the dominant emotion.

Considering the mechanisms involved, misophonia can be defined as abnormally strong reactions of the autonomic and limbic systems resulting from enhanced connections between the auditory and limbic systems. These connections encompass both a high cortical level loop with involvement of cognition, as well as subconscious connections, most probably involving the link between the medial geniculate body and amygdala.^50–52 The functions of these connections are governed by the principles of conditioned reflexes. Note that in case of pure misophonia the auditory system is not overactivated and it acts within normal limits.

With misophonia, the strength of a patient’s reaction depends to a large extent on the context in which sound appears, and is only partially linked to the physical characteristics of the sound. A patient’s previous evaluation, experience with a particular sound, and beliefs linked to it (e.g., a belief that the sound is a potential threat or can be harmful) are very important. One’s psychological profile also plays a role in the response to sound.

Misophonia is practically always evoked by significant hyperacusis, but can be present independently as well. Approximately 60% of our patients exhibit misophonia requiring specific treatment.40 Note that decreased sound tolerance and its components are related neither to hearing loss nor to recruitment.^2,39

Models and Mechanisms

There are a variety of models of tinnitus. The commonly accepted notion that tinnitus is a problem only when it is perceived encouraged a search for mechanisms and development of models of tinnitus generators and strongly focused on the auditory system, particularly the cochlea.^53–59 Within this approach there is lately a shift from focusing on peripheral mechanisms toward mechanisms involving processing information within the central auditory pathways.^60,61 Emphasis is placed on the perception of tinnitus, removing this perception, and achieving silence as an ultimate cure for tinnitus. Attention is focused on potential mechanisms responsible for generating the tinnitus signal, and consequently treatments of tinnitus aim at removing these specific generators.

Various classifications of tinnitus have been introduced. Division of tinnitus into objective and subjective gradually disappear, and objective tinnitus became commonly labeled as a somatosound, whereas the term tinnitus is reserved for subjective auditory phantom perception.² Another classification was based on anatomy, specifically peripheral versus central auditory pathways. Furosemide, a diuretic acting presumably on the cochlea, was proposed as a test method to determine if tinnitus is peripheral or central. The hypothesis was that if tinnitus improves after furosemide administration, it is peripheral; if it doesn’t, it is central.⁶²

Another classification assumed specific mechanisms of tinnitus generation. In this respect several mechanisms responsible for the emergence of tinnitus-related neuronal activity have been proposed: (1) abnormal coupling between neurons causing synchronization of neuronal discharges⁵⁷; (2) local decrease of spontaneous activity enhanced by the lateral inhibition^63,64; (3) unbalanced activation of type I and type II auditory nerve fibers⁵³; (4) abnormal neurotransmitter release from IHCs⁶⁵; (5) decreased activity of the efferent system⁶⁶; (6) mechanical displacement within the organ of Corti⁶⁷; (7) abnormalities in transduction processes⁶⁵; (8) abnormal calcium homeostasis⁶⁸; (9) physical or biochemical factors affecting the auditory nerve⁵⁷; (10) enhanced sensitivity of the auditory pathways after decreased auditory input¹; and (11) discordant damage or dysfunction of OHCs and IHCs^1,2,2,3 Most of these hypotheses provided an indication of how to treat tinnitus,and some of these methods have been applied in clinical practice, for example, microvascular decompression,^69,70 calcium channel blockers,⁷¹ or infusions of drugs affecting transduction function within the cochlea.^72,73

Although there is a consensus that a neuronal activity is responsible for tinnitus, there is still no agreement on the type of neuronal activity related to tinnitus. An increase of spontaneous neuronal activity within the nervous system seems to be a dominant theory.^74–76 Synchronization of the activity between neurons as the basis for tinnitus has been suggested as well⁷⁷; however, subsequent research failed to validate this hypothesis.^78,79 Finally, modification in temporal patterns of discharges, including bursting, an epileptic-type of activity, has been proposed,⁷⁴ and preliminary data support this hypothesis.^2,74,80,81

Psychological models of tinnitus represent the other approach. Commonly it is postulated that patients have problems with tinnitus because they have some psychological or psychiatric problem.⁸² The auditory system is ignored or its role downplayed and coexistence of hyperacusis with tinnitus is neglected. The brain is typically approached as “A black box” (i.e., a device or theoretical construct with known or specified performance characteristics but unknown or unspecified constituents and means of operation”⁸³), and psychological models tend to be oriented toward empirical observation of behavioral reactions, with less attention paid to specific physiological mechanism underlying tinnitus. Treatments based on these models typically focus on improving coping with tinnitus^84,85 and they can provide help in some cases as they are effective in changing the patient’s thinking about tinnitus and reversing the consequences of negative counseling. Cognitive-behavioral therapy seems to be the most effective in this category of treatments.⁸⁶

The neurophysiological model of tinnitus, described first in 1990,¹ combines auditory and other systems in the brain that are involved in the perception of, and reactions to, tinnitus, and considers the issue of decreased sound tolerance.^{2,3,8,39,41,52,87} This model challenges the common belief that to evoke a reaction to tinnitus it is necessary to perceive it. Although it is obvious that the perception of tinnitus can induce negative reactions, it is possible to develop reactions to tinnitus-related neuronal activity without tinnitus perception, just as it is possible to learn to create conditioned reflexes, and to have reactions to stimuli that are not consciously perceived.^88–91 Therefore, reactions to tinnitus can be evoked via conscious and subconscious pathways.^2,41

Tinnitus-related neuronal activity, referred to later as the tinnitus signal, is basically the same in people who only experience tinnitus and those who actually suffer because of it. In the majority of cases, this neuronal activity is a side effect of the attempt of the auditory system to compensate for a dysfunction within the auditory periphery. In people with clinically significant tinnitus, however, this neuronal activity inappropriately activates the limbic and sympathetic part of the autonomic nervous system (Fig 36–1),^1,2,41 resulting in a series of behavioral responses and consequences, such as problems with attention, decreased ability to enjoy one’s activities, interference with work, problems with sleep, impaired social interactions (including interactions with family), anxiety, depression, increase of one’s general stress level, and panic. It is possible to identify the particular systems in the brain and the specific physiological mechanisms responsible for each of these responses.

The auditory system has direct subcortical and subconscious connections from the medial geniculate body to the lateral nucleus of the amygdala,^50,51 a part of the limbic system, which controls emotional expression, memory storage and recall, motivation and mood, seizure activity, and exerts an important influence on the endocrine and autonomic motor systems.⁹²

The limbic system is directly connected with the autonomic nervous system, which consists of two mutually antagonistic parts: the parasympathetic, which prepares the organism for feeding, digestion, rest, and relaxation,⁹³ and the sympathetic, which has the opposite effect, preparing the body for action (e.g., inhibiting the digestive system, stimulating the heart, dilating the bronchi, contracting the arteries) and, in the extreme, the “fight or flight” reaction. Overactivation of the sympathetic part leads to behavioral reactions that match those reported by patients with clinically significant tinnitus: anxiety,problems with sleep, problems with concentration, panic attacks, and decreased ability to enjoy life activities. It is known that various stimuli can cause overactivation of the limbic and autonomic nervous systems, such as high stress levels, significant problems at work or at home, chronic pain, or the effects of even weak sensory stimuli over which we do not have control. Note that reactions depend on what is being activated (e.g., sympathetic versus parasympathetic nervous system) and are not specific to a type of sensory stimulus (e.g., sound or light).94 For example, anxiety can be induced by hearing a voice of an enemy or by seeing a gun pointed at us, and relaxation can be induced by hearing a voice of a friend or seeing smiling people around us. A variety of signals (e.g., tinnitus, work environment) could evoke the same reactions.

Exactly the same stimulus can induce diametrically opposite reactions depending on past experience shaping present associations. The same principle applies to tinnitus: if there are not negative associations linked to the perception of tinnitus, then conditioned reflexes linking the auditory with the limbic and autonomic nervous systems do not develop, and the tinnitus signal does not evoke any behavioral reactions. However, when negative associations develop as a result of a general fear of the unknown, low tolerance to a lack of control over one’s environment, or negative counseling, then conditioned reflex arcs are created and the tinnitus signal causes activation of the limbic and autonomic nervous systems, with consequent negative behavioral reactions.

The functional connections linking the auditory and the limbic and autonomic nervous systems are governed by conditioned reflexes and it is possible to identify two categories of connections: (1) conscious, which involves perception, recognition, evaluation, attention, and other cognitive processes, and occurs at the cortical level; and (2) subconscious (Fig 36–1). Notably, there is no need for a causal link between a stimulus and reactions to create a conditioned reflex, and if tinnitus perception is associated with a high level of emotional distress, the connections are created, causing the tinnitus-related neuronal activity (conditioned stimulus) to evoke activation of the limbic and autonomic nervous systems (conditioned reactions).^2,41

Figure 36–1 The neurophysiological model of tinnitus. (From Jastreboff PJ, Jastreboff MM. Tinnitus and hyperacusis. In: Snow JB Jr, Ballenger JJ, eds. Ballenger’s Otorhinolaryngology Head and Neck Surgery, 16th ed. Hamilton, Ontario, Canada: BC Decker, 2003:456–475. Reprinted with permission.)

Reinforcement is necessary to initiate creation of the reflex arc, and several scenarios are observed in the case of tinnitus. Most frequently a negative emotional state is evoked by negative counseling; for example, patients are told unpleasant, threatening news about their tinnitus such as that it might indicate the presence of a tumor, or that something is wrong with the brain, or that tinnitus lasts forever and nothing can be done so “you have to learn to live with it.” Such information, particularly coming from a medical professional, frequently has a devastating effect on the patient and leads to strong activation of the limbic and autonomic nervous systems and furthermore evokes survival reflexes. A negative emotional state occurs in cases of the rapid emergence of tinnitus or an increase in preexisting tinnitus (e.g., in the case of sudden hearing loss, exposure to an explosion or gunfire, head trauma etc.). Created reflex arcs undergo further enhancement in a vicious-cycle scenario, which works at the conscious and subconscious levels.⁴¹ Note that this reflex has a strong tendency to become stronger as the signal (tinnitus) is continuously present and the effect of the activation of the limbic and autonomic nervous systems acts as the reinforcement. Thus, both the signal and the reinforcement are continuously present. This situation corresponds to a situation of continuous training, and consequently enhances the strength of the reflex.

At the initial stage of development of tinnitus as a problem, the conscious path is essential and plays a dominant role. Once tinnitus acquires negative connotations, the subconscious conditioned reflex is automatically created and becomes equally important as the conscious path, or even dominant. Sustained enhanced activation of the sympathetic part of the autonomic nervous system is responsible for behaviorally observed problems. Once the tinnitus signal acquires a high level of negative associations and is classified as creating a potential threat to patients’ quality of life, then patients respond by going into an alert mode, with their survival reflexes activated. The dominant, subconscious survival mechanism decreases their ability to enjoy life, pushing patients into anxiety and depression.²

To appreciate the widespread occurrence of the role of habituation, it is important to note certain significant characteristics of brain function that have a major impact on tinnitus patients. It has been firmly established that we cannot perform more than one task involving full cognitive attention at a given time. Performing several tasks can be done by quickly switching from one activity to the other.^95,96

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