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Hearing Journal:
doi: 10.1097/01.HJ.0000286675.34473.9a
Page 10

Tinnitus: recent insights into mechanisms, models, and therapies

Baguley, David M.

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1 I seem to recall a Page Ten on tinnitus not too long ago. So, why are we returning to this topic so soon? Do you have some news for us?

You're probably thinking of the Hearing Journal special issue on tinnitus in 2001, and, yes, a lot of new things have happened over the past 5 years!

At the moment there seems to be a major resurgence in both clinical and research interest in tinnitus. Evidence of this is the large number of peer-reviewed papers mentioning tinnitus, with about 200 on Medline from 2005 alone! Also, at the recent International Tinnitus Seminar in Pau, France, there was a real spirit of interdisciplinary communication and collaboration, especially between the basic scientists and the clinicians.

Figure. Baguley...
Figure. Baguley...
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2 With all this interest, are we any closer to understanding the mechanisms underlying tinnitus?

Potentially—yes. There are a number of avenues of inquiry that seem very promising.

The first is distinguishing between the ignition site for a tinnitus and physiological mechanisms that then promote that signal in the central auditory system.1,2 Making this distinction allows one to consider these processes, and how they might be influenced to inhibit tinnitus, in individual detail.

Another line of inquiry is looking very carefully at the role of the dorsal cochlear nucleus (DCN) in tinnitus.3,4 The contribution of the DCN has often been overlooked in human audition—indeed, some textbooks consider it to be virtually vestigial.5 But the DCN, though proportionally small, is essentially as complex anatomically in humans as in many of our mammal relatives. In cats, the DCN has been implicated in sound localization6 and in integrating inputs from the auditory and somatic sensory systems, particularly regarding somatic input from the pinna.7

Researchers are considering the idea that the DCN has an inhibiting role in humans with normal hearing, but that when some hearing is lost, this inhibition becomes less effective, thus allowing spontaneous neural activity and noise to progress through the auditory system.3 Interestingly, there are also indications that the DCN is directly influenced by attentional and emotional processes in the human brain.4 Further, it is possible that the DCN may be implicated in one of the oddities of tinnitus—somatically modulated tinnitus.

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3 Somatically modulated tinnitus? What on earth is that?

I'm glad you picked up on it! I have been working with tinnitus patients for 20 years, and for at least the first 10 years if people reported changes in tinnitus when they clenched their teeth, or stroked their face, or moved their neck, I moved quickly on, neither really listening nor understanding.

However, Robert Levine, MD, of the Massachusetts Eye and Ear Infirmary did listen, and his research indicates that 80% of people with troublesome tinnitus find that it is modulated by somatic input from the head or neck.8 Further, he and his colleagues also found that in 60% of people without tinnitus, some tinnitus can be transiently induced by such movements.

It therefore looks as though somatic modulation of tinnitus is a very common phenomenon, and the implication is that some neural pathway connecting somatic sensation with hearing is present in humans. Previous work has already demonstrated such a pathway in cats.7 Once again, the DCN is being suggested as a site where interaction between the somatic and auditory systems can take place.4

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4 Are there any other novel mechanisms?

Indeed. Any audiologist worth his salt reads widely, and last summer I came across a mechanism of tinnitus that was new to me: tinnitus caused by magic! In the book Harry Potter and the Half-blood Prince,10 Harry and Hermione need to talk without being overheard, so they use a tinnitus-inducing spell. Called “muffliato,” it is described as a spell that filled the ears of anyone nearby with an unidentifiable buzzing, so that lengthy conversations could be held in class without being overheard.

Unfortunately, no spell is described that cures tinnitus!

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5 I'm glad you're keeping up with the literature. But how does knowledge of ignition sites and of mechanisms that promote the tinnitus signal help the clinician?

Thank you for raising this point. Your question “But how does this help the clinician?” should be perpetually on the lips of the tinnitus researcher. In fact, this distinction is rather helpful in the clinical setting, and patients quickly understand the generation of their tinnitus and, where possible, the etiology. But they understand also that this ignition of the signal is not sufficient to explain the intrusiveness of the tinnitus signal nor the extent of their distress.

It could be argued that this distinction between ignition site and promoting mechanism is implicit within both the Jastreboff Neurophysiological Model10 and the Habituation Model (often called the Psychological Model)11 of tinnitus. But making it explicit facilitates research into these mechanisms in a novel and exciting way.

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6 You mentioned models of tinnitus. Aren't the two models you spoke of completely at odds with each other?

Good question! And the answer is: no, and yes! No, in that there are major areas of convergence between the models. They both pay little attention to the ignition of the tinnitus and more to emotional and behavioral reaction to the tinnitus. In both, the aim of therapy is habituation to the tinnitus. In fact, the main therapy program that derives from the Jastreboff Neurophysiological Model—Tinnitus Retraining Therapy (TRT)—and psychological therapy for tinnitus contain quite similar elements of counseling and sound therapy, though there are differences of style and emphasis.

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7 So, are there really any substantial differences between the models?

There are definitely some significant and important areas of divergence. Specifically, the “directive counseling” used in TRT is one-way and restricted to tinnitus alone, whereas the counseling in a psychological program is more wide-ranging and has, of course, a strong underpinning in psychological practice. Also, the Jastreboff Neurophysiological Model invokes Classical Conditioning theory in explaining the development of persistent troublesome tinnitus.

It has recently been pointed out that there are some potential problems with this, specifically how a sound initially without meaning (i.e., tinnitus) becomes paired with an unconditioned aversive stimulus.

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8 Isn't human learning more complex than simple conditioning?

While people can and do learn by Classical Conditioning, this is neither the most effective nor most common way that human beings learn, and an Evaluative Conditioning process may be more involved in tinnitus.13 In particular, therefore, the Jastreboff Neurophysiological Model does not quite do full justice to these issues and to the role of cognition (belief) in emergent tinnitus distress.

The Habituation (or Psychological) Model has shortcomings also, with a surprising lack of underpinning experimental evidence and the potential overemphasis of the role of emotion and anxiety states in tinnitus.13

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9 Are you suggesting that the truth lies elsewhere?

Perhaps it does. What is evident is that the dichotomy, and controversy, between “Neurophysiological” and “Psychological” models isn't helpful. Put simply, when is tinnitus, which must involve neural activity in the auditory system, not neurophysiological?2 Further, when is troublesome tinnitus, which must involve emotional distress, not psychological? Of course, the answer to both is never.

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10 The idea that tinnitus has a psychological component concerns me as an audiologist. Surely this is going to take me into foreign territory.

It is right to be cautious here, and mindful of boundaries. Flasher and Fogle have very usefully suggested a framework of issues that are “within boundaries” and “beyond boundaries” for non-psychologists who are counseling patients with audiological/vestibular disorders.14

Within boundaries are:

* interviewing the patient/family

* presenting the diagnosis

* providing information about the diagnosis

* discussing interventions for the diagnosis

* dealing with the patient's reaction to the diagnosis

* onward referral as appropriate

* supporting the strengths of the person and the person's efforts to regain function

* supporting the strengths of the family to help them interact optimally with the patient

* creating supportive empowerment for the patient and family to develop the ability to manage their own problems and be independent of the clinician

Beyond boundaries are:

* chemical dependence

* child or elder abuse

* chronic depression

* legal conflicts

* marital problems

* personality disorders

* sexual abuse and sexual problems

* suicidal ideation

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11 I like the boundaries. Do you support them?

Most certainly. Within these boundaries, it is entirely appropriate to deal with tinnitus patients within an audiologist's scope of practice. Indeed, very often it is the audiologist to whom patients with troublesome tinnitus turn first for help. The beyond boundary issues do also present themselves in a tinnitus clinic, however, and the clinician must take care to stay within boundaries, to make appropriate onward referral, and to care for oneself. There is a real risk of clinician burnout, and the need for mentoring, support, and debriefing is high. So, proceed, but with some care.

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12 Many of my patients ask me about the use of complementary or alternative therapies. What exactly is out there in this area?

There are several therapies that could be considered complementary or alternative for tinnitus.13 Among the more common ones are acupuncture, reflexology, and homeopathy. Others might be the use of gingko biloba extract and hypnotherapy.

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13 How should I advise my patients about these?

Well, for starters, you should know that the use of complementary and alternative therapy is very common. It has been estimated that up to one-third (72 million people) of the US adult population utilized some complementary therapy in 2002,15 and that two-thirds of US adults have used complementary therapy in their lifetime.16 Unfortunately, no complementary therapy has been consistently shown to be effective in reducing either the intensity, awareness, or distress of tinnitus patients, and some could be downright harmful. The most obvious of these is Hopi ear candling,17 which carries a real risk of burns.

A more pernicious risk is that of disappointment, when a patient has placed great hope in a therapy and that hope proves to be forlorn. There is good evidence that such disappointment can compound tinnitus distress.18

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14 What about drug treatments? Are we closer to anything that really is effective?

An effective drug treatment continues to elude us. There are, however, some encouraging recent developments.

The first concerns the use of selective serotonin re-uptake inhibitors (SSRI) in tinnitus patients. These modern antidepressants are widely used in the treatment of depression and anxiety, and increase the extracellullar level of serotonin by inhibiting re-uptake. A recent study has demonstrated a positive effect of sertraline over placebo on reported tinnitus severity, though the study design did not control for depression.19

Disappointingly, a further study that looked at the effect of paroxetine versus a placebo on a group of tinnitus patients who were specifically non-depressed demonstrated no benefit other than in their responses to one question: “How aggravating is your tinnitus?”20 Additional experimental work is needed in this area, as the conceptual argument for serotonin dysfunction being a neurophysiological substrate for tinnitus is strong,21 involving both the relationship between tinnitus and depression and the role of serotonin as a neurotransmitter in the auditory system.

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15 I remember hearing about intravenous lidocaine and tinnitus inhibition. Do we know any more about them?

Indeed we do. It has been known since the 1930s that intravenous infusion of some amine anesthetic agents can transiently inhibit tinnitus in a majority of patients, and that lidocaine is especially effective in this regard.22 This is a perilous procedure though, as there is a risk of respiratory and cardiac arrests at the effective dose. What this does tell us, however, is that there is a mechanism that can inhibit tinnitus, albeit transiently.

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16 So, where is this inhib-itory mechanism? in the cochlea or in the brain?

Indeed, that is the big question. If we ascertain that, we can use other, novel pharmacological agents to influence tinnitus via that mechanism.

A recent study at Cambridge University, England, sought to answer this question by looking at the action of lidocaine upon tinnitus in a group of patients who had previously undergone trans-labyrinthine vestibular schwannoma surgery, during which the cochlear nerve had been sectioned.23 If lidocaine inhibits that tinnitus, then it must be acting in the brain, as the cochlea has been surgically disconnected.

Using a randomized blinded controlled trial paradigm, the Cambridge team was able to demonstrate that lidocaine does inhibit that tinnitus, and so the mechanism is within the brain and may well involve sodium channel modulation in CNS tissue that has undergone plastic reorganization. The urgent search is now on to find drugs that will perform a similar action, but on a longer-term basis and without side effects.

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17 I remember being taught that optimizing hearing with hearing aids can help many people with troublesome tinnitus.

That's correct, and for many patients this, and some simple information, is sufficient. The advances in hearing aid technology have helped us here. Grant Searchfield, PhD, from New Zealand has convincingly summarized the arguments (some of which are longstanding) for hearing aid fitting as an essential element in tinnitus therapy for all patients except that minority with absolutely normal pure-tone audiometry.24 Further, Searchfield calls for the use of low-compression kneepoints to enable the amplification of low-intensity environmental sounds to audible levels without eliciting discomfort to louder sounds.

So, hearing aids remain a powerful tool in the hands of the clinician seeing patients with troublesome tinnitus, even when hearing handicap is not a major issue.

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18 Tinnitus therapy seems very time-consuming. Are there any new approaches to working with tinnitus patients?

It's true that one-to-one tinnitus therapy takes time. Practitioners may spend an hour or more with a new patient, and have several 45-minute follow-up appointments. For many practitioners, this may not be feasible. There are indications, however, that tinnitus services can be delivered effectively in a group context, which may be more suitable for busy clinicians.25

There is also some exciting research from Sweden demonstrating the impressive efficacy of psychological therapy for patients with troublesome tinnitus. It is provided via the Internet following an initial face-to-face consultation.26 While this strategy for delivering services to tinnitus patients is not yet ready for wider use, it does represent an innovative approach that may be of great benefit to patients who live where there is no local tinnitus service.

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19 If tinnitus therapy can be delivered via the Internet, what are the pros-pects for self-help treatment?

There is a very significant role for self-help in the management of tinnitus. Both the American Tinnitus Association (www.ata.org) and the British Tinnitus Association (www.tinnitus.org.uk) offer up-to-date and authoritative information to people with troublesome tinnitus, as do a number of independent web sites (e.g., www.tinnitus.org). The peer support and message of hope communicated in this way are extremely valuable. But patients do sometimes need a professional to guide them through the information that is available and help identify what is valid and appropriate.

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20 What then are your real hopes for the future?

The history of research into tinnitus therapy shows that progress has been made, even though a truly effective treatment for inhibition of tinnitus—the heart's desire of our patients—continues to elude us. The present situation shows real signs of progress, however, with renewed interest from basic scientists and clinicians, and some signposts to a brighter future.

There are few things related to ears and hearing that have been discussed and debated as much as tinnitus. That's partly because it is so widespread. The American Tinnitus Association estimates that more than 50 million Americans experience tinnitus to some degree, about 12 million have it severely enough to seek medical attention, and about 2 million patients are so seriously debilitated by their tinnitus that they cannot function “normally” on a day-to-day basis.

While published reports of this auditory perception go back centuries, research interest remains high. A quick PubMed search shows a match for “tinnitus” with over 5000 articles. And, if you have a little more time on your hands, you might want to check out the nearly 10 million matches listed by Google. There are tinnitus courses, specialists, clinics, associations, organizations, self-help groups, and help lines. There are treatments, therapies and many alleged “cures.” You can even read about animals or famous people who have tinnitus.

We've had several discussions about tinnitus at the Journal too, and, in fact, we devoted a special issue to the topic in 2001, edited by Richard Tyler, PhD. But that was 5 years ago, and things change. So, it's time to bring in another tinnitus expert, this one from across the Atlantic.

David Baguley, PhD, is director of audiology, Addenbrooke's Hospital, Cambridge University Hospitals, where he has worked for the past 20 years. His main clinical focus is on tinnitus in both adults and children, in particular synthesizing the perspectives of different disciplines on tinnitus and considering the implications of this for therapy. Dr. Baguley, who is internationally known for his work in tinnitus, has received the Shapiro Tinnitus Research Award from the British Tinnitus Association. Last month, the American Academy of Audiology presented him with its International Award in Hearing. Look for the book he recently co-edited: Tinnitus: A Multidisciplinary Approach.

David's hobby is listening to loud indie-rock music, so one has to wonder if his favorite band is the emerging group from Portsmouth named—you guessed it—Tinnitus! Unfortunately, the Portland, Oregon indie-rock band Hazel is no longer performing, but David probably owns the group's CD, which includes the hit Ringing in My Ears.

This is probably not the first article you've read on the topic of tinnitus, but I think you'll enjoy the excellent update that Dr. Baguley has provided. As he points out, we continue to learn more about this intriguing auditory perception, and make progress in its treatment and management.

Gus Mueller

Page Ten Editor

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REFERENCES

1. Eggermont JJ: Cortical tonotopic map reorganization and its implications for tinnitus. In Dauman R, Bousceau-Faure F, eds. Proceedings of the VIIIth International Tinnitus Seminar. Acta Otolaryngol Supplementum, in press.

2. Baguley DM: What progress have we made on tinnitus? The 2005 Tnndorf Lecture. In Dauman R, Bousceau-Faure F, eds. Proceedings of the VIIIth International Tinnitus Seminar. Acta Otolaryngol Supplementum, in press.

3. Kaltenbach JA, Zhang J, Finlayson P: Tinnitus as a plastic phenomenon and its possible neural underpinnings in the dorsal cochlear nucleus. Hear Res 2005;206(1–2):200–226.

4. Kaltenbach JA: The dorsal cochlear nucleus as a participant in the auditory, attentional and emotional components of tinnitus. Hear Res 2006;Feb 7 (E-pub ahead of print).

5. Webster DG: Neuroscience of Communication. San Diego: Singular, 2nd ed., 1995.

6. Nelken I, Young ED: Why do cats need a dorsal cochlear nucleus? J Basic Clin Physiol Pharmacol 1996;7:199–220.

7. Kanold PO, Young ED: Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 2001;21(19):7848–7858.

8. Levine RA, Abel M, Cheng H: CNS somatosensory-auditory interactions elicit or modulate tinnitus. Exper Brain Res 2003;153(4):643–648.

9. Rowling JK: Harry Potter and the Half-Blood Prince. London: Bloomsbury, 2005:224.

10. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge: Cambridge University Press, 2004.

11. Hallam RS, Rachman S, Hinchcliffe R: Psychological aspects of tinnitus. In Rachman S., ed., Contributions to Medical Psychology, Vol. 3. Oxford: Pergamon Press, 1984: 31–53.

12. McKenna L: Models of tinnitus suffering compared and contrasted. Aud Med 2004;2:41–53.

13. Andersson G, Baguley DM, McKenna L, McFerran D: Tinnitus: A Multidisciplinary Approach. London: Whurr, 2005.

14. Flasher LV, Fogle PT: Counseling Skills for Speech-Language Pathologists and Audiologists. New York: Thomson, Delmar Learning, 2004.

15. Tindle HA, David RB, Phillips RS, Eisenberg DM: Trends in use of complementary and alternative medicine by US adults: 1997–2002. Altern Ther Health Med 2005;11(1):42–49.

16. Kessler RC, Davis RB, Foster DF, et al.: Long-term trends in the use of complementary and alternative medical therapies in the United States. Ann Int Med 2001;135:262–268.

17. Shenk HL, Dancer J: Ear candling: A fool-proof method, or proof of foolish methods? Audiology Online 2005 http://www.audiologyonline.com/articles/article_detail.asp?article_id=1538.

18. Andersson G: Prior treatments in a group of tinnitus sufferers seeking treatment. Psychother Psychosomatics 1997;66:107–110.

19. Zoger S, Svedlund J, Holgers KM: The effects of sertraline on severe tinnitus suffering: A randomized, double-blind, placebo-controlled study. J Clin Psychopharmacol 2006;26(1):32–39.

20. Robinson SK, Viirre ES, Bailey KA, et al.: Randomized placebo-controlled trial of a selective serotonin reuptake inhibitor in the treatment of nondepressed tinnitus subjects. Psychosom Med 2005;67(6):981–988.

21. Simpson JJ, Davies WE: A review of evidence in support of a role for 5-HT in the perception of tinnitus. Hear Res 2000;145:1–7.

22. Barany R: Die beeinflussing der Ohrensausens durch intravenous injequierte lokalanaesthesia. Acta Otolaryngol 1935;23:201–203.

23. Baguley DM, Jones S, Wilkins I, et al.: The inhibitory effect of intravenous lidocaine infusion upon tinnitus following translabyrinthine removal of vestibular schwannoma: A double blind placebo control crossover study. Otol Neurotol 2005;26(2):169–176.

24. Searchfield GD: Hearing aids and tinnitus. In Tyler RS, ed., Tinnitus Treatment: Clinical Protocols. New York: Thieme, 2005: 161–175.

25. Newman CW, Sandridge SA: Incorporating group and individual sessions into a tinnitus management clinic. In Tyler RS, ed., Tinnitus Treatment: Clinical Protocols. New York: Thieme, 2005: 187–197.

26. Andersson G, Kaldo-Sandström V: Internet-based cognitive behavioral therapy for tinnitus. J Clin Psychol 2004;60(2):171–178.

© 2006 Lippincott Williams & Wilkins, Inc.

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