Research & Technology Legends | November 2021 Hearing Review

HR interviews a pioneer in the study of the brain and auditory processing disorders

By Karl Strom

“Frank Musiek has been at the forefront of research in neuroaudiology for more than 40 years. His game-changing 1984 paper, co-authored with K. Kibbe and J. Baran, on neuroaudiological findings in split-brain patients originally brought his work to the attention of the research community. Year after year his contributions have broadened to include both behavioral and electrophysiological studies of patients with a variety of central auditory problems. In recent years Dr Musiek, his team, and his former students have brought a sobering rigor to the study of children and adults with auditory processing disorders. Our profession is indebted to this audiological pioneer.”

– James Jerger, PhD

Frank Musiek, PhD, is a renowned audiology researcher, professor, and clinician. His research has contributed to our fundamental understanding of the anatomy, physiology, and neurophysiology of the human auditory system, as well as tests of the auditory brainstem and central auditory pathway, at least three of which are mainstays in today’s clinical test battery. The recipient of the 2007 Jerger Career Award for Research in Audiology, Dr Musiek has published over 180 refereed articles and presented more than 300 invited lectures/seminars and about 400 scientific papers in venues around the world. He has also published 12 books and authored more than 50 book chapters. Dr Musiek is currently a professor in the Department of Speech, Language, and Hearing Sciences at the University of Arizona.


Frank Musiek, PhD

HR:  You have devoted much of your career to the area of neuroaudiology, and some in our field might even say you were among the first to actually popularize the term “neuroaudiology.” Can you tell us a little about this history?

Musiek:  First I wish to thank Jim Jerger for his opening comments. He has been a person I have always admired and certainly has made many significant, groundbreaking contributions to neuroaudiology. 

Historically, the term “neuroaudiology” was used in 1972 by the late George Lynn [a PhD audiologist] and John Gilroy [a neurologist] in an article titled “Neuro-audiological Abnormalities in Patients with Temporal Lobe Tumors.”1 I was aware of this article, but it was more the work from Marilyn Pinheiro, Jim Jerger, and Chuck Berlin who were reporting on patients with central auditory nervous system (CANS) disorders that influenced me early in my career. 

My particular interest was not only in the audiological correlates to CANS disorders but also auditory nerve dysfunction, which is part of the auditory periphery. It made sense to me that the term “neuroaudiology” could encompass audiological correlates to both disorders of the auditory nerve and CANS. This view was bolstered by the fact that I had access to populations with neuroauditory involvement. In addition, I noticed that other disciplines were focusing on the “neuro” aspect of their respective specialty—for example, Neurotology, Neuro-opthamology, Neuropsychology, Neuropharmacology, etc. So, I started using the term Neuroaudiology and encouraged other clinicians and researchers to do so appropriately. 

In terms of orientation we classify CAPD in two types: 1) Learning related, and 2) Neurologically based (which aligns with much of neuroaudiology). 

HR:  You have been a contributor and strong proponent to auditory neuroanatomy and its critical role in neuroaudiology. Can you explain your perspective on this?

Musiek: Well, this started from my experiences with outstanding anatomists and neuroanatomists who profoundly influenced me and instilled the importance of auditory structure and function, diagnostics, and more specifically neuroaudiology. Marilyn Pinheiro, Val Jordan, Kent Morest, and Bill Mosenthal all contributed to my education in auditory neuroanatomy. Marilyn was trained as an audiologist and received post-doc training in neurology. As a mentor, she influenced and instilled in me the importance of auditory neuroanatomy related to audiology. As a doctoral student, I signed up for Val Jordan’s highly regarded temporal bone anatomy course, which grounded me in terms of peripheral auditory and vestibular structures. Kent Morest—considered the father of modern auditory neuroanatomy—profoundly influenced me as a colleague and mentor while I was at the University of Connecticut. In my early years at Dartmouth, Bill Mosenthal provided me with the opportunity in the med school anatomy lab to do a large quantity of human brain dissections while I was helping him teach neuroanatomy. 

The relationship between neuroanatomy and neuroaudiology is perhaps best exemplified by some recent research on patients with schizophrenia and auditory hallucinations, and our paper “Auditory Hallucinations: An Audiological Horizon?2 This research highlights probable relationships between changes in the structure of the auditory cortex, auditory hallucinations, and central auditory function. Though more research is needed, it appears that decreases in volume of the auditory cortex in those with schizophrenia is correlated with the occurrence and severity of auditory hallucinations. These individuals also perform poorly on tests of central auditory function—especially dichotic listening. The pursuit of these kinds of relationships between functional neuroanatomy and auditory assessment is a prime example of neuroaudiology.

HR:  As the title of your paper suggests, this really does seem to be a ripe area for audiology. What other things excite you about the future of neuroaudiology?

Musiek: Frankly, that would lead to an exhaustive list, because it’s really any disorder that can affect the CANS or auditory nerve that could relate to, or be an aspect of, neuroaudiology. However, there are a few that are especially noteworthy because they are often overlooked or not sufficiently evaluated. 

One of these is multiple sclerosis (MS). As you know, MS is a demyelinating disease often affecting young adults. Any anatomical region of myelinated nerves can be affected by MS, including the auditory system. There are 1 million people with MS in the United States. A number of studies have shown more than half show abnormal findings on behavioral or electrophysiological central auditory tests, and anywhere between 4-40% will relate audiological symptoms. 

Tests of the auditory brainstem response (ABR) and dichotic listening can be very revealing in terms of auditory system involvement. Due to the heavy myelination of the auditory brainstem pathway and corpus callosum, these tests [ABR and dichotic testing] have been proven to be highly dependent on proper function and integrity of these structures, and thus sensitive to compromise. 

Also of interest is head trauma— especially blast injuries in our military veterans. This is a clinical population that demands in-depth neuroaudiological assessment and review.3 Erik Gallun and his colleagues at the Portland VA have shown the value of tests, such as gap detection and dichotic listening, in defining auditory deficits in this clinical population.4 It should be remembered that in head injury, central and/or peripheral auditory function can be compromised. 

Another population of high interest are individuals with vascular disorders, such as strokes or diabetes, affecting the CANS. These patients are often overlooked in terms of their auditory difficulties, as demonstrated by the excellent report from Edwards et al.5 This is despite tens of articles showing good central auditory test efficacy in revealing what is often major central auditory deficits in these patients. 

Another neurological population with auditory involvement is one of the most interesting and striking: those people who have undergone hemispherectomy or temporal lobectomy. This surgery is often performed on young children with intractable epilepsy. With this surgery done early in life, these children often do amazingly well—but they do have a variety of deficits including those of central auditory function. A well-selected central auditory test battery utilized on these individuals can reveal a myriad of audiological deficits of varying degrees. With this information, counseling and rehabilitation procedures can be initiated, which often prove most helpful to these patients.

Interestingly, one of the commonalities of these aforementioned neuroaudiological disorders is a normal pure-tone audiogram. Pure-tone thresholds will do little to define the auditory deficits in these neurologically-based hearing problems. 

Also of note is the misconception that these neurologically based hearing deficits are rare entities. While it is true that perhaps MS, temporal lobectomies, and hemispherectomies (TLH) have a low-incidence, their prevalence is growing. This is because both MS and TLH occur relatively early in life, and many individuals with these diagnoses live near-normal life spans. This means that every year, the prevalence of the individuals not seen for proper audiological evaluation and treatment increases, and over many years, the prevalence becomes significantly high, despite the low-incidence.  

Another misconception that I commonly hear is that these neuroaudiological evaluations are used to make a diagnosis of these disorders and pale in comparison to modern imaging techniques. This premise is wrong. What we are mostly interested in these patients is not the diagnosis of the disorder, but to determine the integrity of the CANS and the entire auditory system. This in turn allows us to: 1) Make a proper referral when necessary; 2) Properly counsel the patient about their hearing difficulties;  3) Initiate a suitable rehabilitative program, and 4) Provide critical information to other professionals with regard to the nature of the auditory problem associated with the disorder. 

It is also true that the audiologist may be the first heathcare provider to see these kinds of patients. Defining the problem with appropriate testing from the start can be a critical component for proper and timely referral.

HR:  I get the feeling most of these disorders are overlooked or not pursued by audiologists. Do you think this is the case, and, if so, why?    

Musiek: Well, that’s not always the case, but it’s often true. There are likely a number of reasons for this notable gap in audiology services, and they cannot all be mentioned here. However, there are a few that are foremost in my view.

One is our history. Audiology has in many ways been an outgrowth of otology. Dating back to Carhart, otologic relationships with audiology have been there from the beginning. The disorders we have been trained to deal with are essentially otological in nature. Many audiologists work with otologists and, of course, see mostly otologic disorders in their practice. Therefore, it is easy to understand why a lot of audiologists are strongly oriented and feel comfortable with seeing otologic problems. This certainly is not a bad thing, but what is forgotten (perhaps in some cases purposefully) is that neurological problems can also affect hearing processes. Remember, we hear with our brains not our ears! With this history of otological relationships, it is easy to understand why audiologists are otologically, and not neurologically, oriented.

Another reason is our education and training. Though there certainly are exceptions, audiologists generally do not receive sufficient training in the anatomy and physiology of the CANS, disorders that can affect the CANS, or auditory processing assessment/rehab. Although this educational shortcoming is improving, in many programs these topics are superficially covered or simply not addressed. In addition, few professors are well grounded in these areas of knowledge. Processes that deal with the complexity of the brain demand considerable training, yet as audiologists we receive comparatively little.

A third reason is a weak relationship with clinical neuroscience. To see patients with neurologically based auditory problems, neurologists and neurosurgeons need to understand more about audiology and vice versa. Speaking from personal experience, once this happens, more patients from these clinicians will make their way to the audiologist. This, of course, assumes that once these patients are referred, audiologists can appropriately evaluate them. Generating knowledgeable communication with neurologists and neurosurgeons about neuroauditory disorders will foster trust and enhance relationships. Education is key, and a good avenue for enhancing this is attending and contributing to neurology and neurosurgery grand rounds or similar venues. 

A final possible explanation is reimbursement. This indeed is an important and contemporary issue; however, it should not outweigh the importance of properly evaluating and managing the patient in the best possible manner. Reimbursement is something for which the national societies must champion and strategically campaign. However, on the individual level, there are some strategies that can help. Ian Windmill and Barry Freeman6 have argued that writing to third-party payers to cover additional tests can be successful. Explaining why additional testing was needed and that “best practices” were followed can yield increases in reimbursement. This must be done with consistency and certainly some tenacity.

HR: It definitely is fascinating territory and would appear to be one of the most-fertile areas of future development for hearing healthcare. Are there any specific cases that stick in your mind as being particularly revealing scientifically or that really piqued your interest and led you down new pathways in neuroaudiology? 

Musiek:  Well, there is no question that some of the most interesting cases come from neuroaudiology/CAPD. Among the most interesting, as Dr Jerger pointed out, were the split-brain patients.7 These were mostly research cases that we saw at Dartmouth in the 1980s when it was essentially the only place in the world where the surgery was performed [surgically sectioning the corpus callosum for those with intractable epilepsy] and extensive research conducted. These patients had normal hearing sensitivity and essentially performed normally on most central auditory tests—except dichotic listening and pattern perception. On these procedures, performance was essentially at chance levels for the left ear on dichotic tests and bilaterally for frequency patterns. These findings were consistent with the absence of interhemispheric transfer of auditory information which, as we learned, these tests required. 

Another informative case was of a young woman who while driving suddenly lost her hearing on the left side. And this was accompanied by tinnitus and some imbalance. Within the next couple of days of onset, these conditions improved, and when we saw her, she still had a moderate, flat, sensorineural hearing loss. The initial thoughts by both otology and audiology were that she had Meniere’s disease. However, we decided to pursue an ABR which showed a clearly abnormal response on the left side. An MRI was then pursued, which showed plaques in the left brainstem auditory pathway and, in turn, led to the diagnosis of MS. Sudden hearing loss linked to MS was and is unusual, and this case was noteworthy in alerting the medical community that this can happen.8

The third and final case I should mention was of a woman in her 50s who lost her job as a secretary because of hearing difficulties. Upon exam, she revealed only mild, bilateral, sensorineural hearing loss, but her speech recognition score rolled over at high intensities, bilaterally. This prompted an ABR which was totally absent bilaterally. Central tests, including masking level difference (MLD) and dichotic tests, were abnormal bilaterally. This led to a referral to Neurology who found, after much testing and history pursuits, that she had Charcot Marie Tooth (CMT) syndrome. We published this case in 1982,9 and to our knowledge it is one the first cases reported linking CMT to abnormal neuroaudiological test results. Now, CMT is considered one of the disorders classified as a true auditory neuropathy.

HR: It’s apparent your clinical and basic science investigations have made a significant impact on the field. What would you say about Neuroaudiology and the future of audiology? 

Musiek: Neuroaudiology has gained some ground recently, but it is still underplayed and often misunderstood. Certainly, it is not for everyone, but currently I fear many individuals needing it are underserved by the present audiology community. Patients with real auditory complaints and normal audiograms should be further evaluated—just as Carhart conveyed over 50 years ago!

Neuroaudiology/CAPD is demanding and requires training beyond what is obtained in most universities, and those wishing to seriously pursue this area must realize that. Many have pursued further education and training by reading, attending workshops, etc. In my opinion, more graduate and post-grad education must be made available focusing on normal and abnormal structure and the function of the CANS. 

Neuroaudiology/CAPD represents a great opportunity and frontier for audiologists interested in higher auditory function. There will be many exciting breakthroughs in our knowledge of this topic in the future. Cultivating a practice in this area is a fascinating pursuit and provides an important service to perhaps the most underserved clinical population in audiology. In addition, there is an abundance of valued tools presently available to both evaluate and help manage individuals with central, neurologically based hearing problems. 

Neuroaudiology presents a challenge, but one worth undertaking not only to enhance our field but to better serve our patients.


Karl Strom is editor of The Hearing Review and has been reporting on hearing-related issues for over 25 years.

CORRESPONDENCE can be addressed to HR at: [email protected] or Dr Musiek at: [email protected]

Citation for this article: Strom K. Neuroaudiology: An interview with Frank Musiek. Hearing Review. 2021;28(11):24-26.

 

References

  1. Lynn GE, Gilroy J. Neuro-audiological abnormalities in patients with temporal lobe tumors. J Neurolog Sci. 1972;17(2):167-184.
  2. Musiek FE, Morris S, Ichiba K, Clark L, Davidson AJ. Auditory hallucinations: An audiological horizon? J Am Acad Audiol. 2021;32(03): 195-210.
  3. Strom KE. Veterans with hearing loss: Unique needs and audiological considerations. https://hearingreview.com/resource-center/white-papers/special-report-veterans-with-hearing-loss-unique-needs-and-audiological-considerations. Published September 21, 2019.
  4. Gallun FJ, Lewis MS, Folmer RL, et al. Implications of blast exposure for central auditory function: A review. J Rehabil Res Dev. 2012;49(7):1059-1074.
  5. Edwards DF, Hahn MG, Baum CM, Perlmutter MS, Sheedy C, Dromerick AW. Screening patients with stroke for rehabilitation needs: Validation of the post-stroke rehabilitation guidelines. Neurorehabil Neural Repair. 2006;20(1):42-48.
  6. Windmill I, Freeman B. Medicare payments for hearing care procedures: A 14-year review. Hearing Review. 2021;28(3):12-18.
  7. Musiek FE, Kibbe K, Baran JA. Neuroaudiological results from split-brain patients. Semin Hear. 1984;5(3):219-229.
  8. Musiek FE, Baran JA, Pinheiro ML. Neuroaudiology: Case Studies. 1st ed. Singular Publishing Group;1994.
  9. Musiek FE, Weider DJ, Mueller RJ. Audiologic findings in Charcot-Marie-Tooth disease. Arch Otolaryngol. 1982;108(9):595-599.