I recently had the opportunity to do an email “interview” with Robert (Bob) Burkard, PhD, a professor at the University at Buffalo in Buffalo, New York. His most recent project caught my attention at the American Auditory Society meeting in March 2019, and he agreed to take some time and answer a few questions on his work. Dr. Burkard’s voluminous list of publications fills 13 pages of his curriculum vitae and spans 39 years.
Dr. Burkard, thank you for taking time out of your schedule to answer a few questions for Audiology Today. Can you highlight some of your favorite lines of study over your career?
I see my research as one main line of research that has focused on the effects of various stimulus manipulations to elicit the auditory brainstem response (ABR), which has over time involved different collaborators (including students) and animal species. I have, on occasion, veered off my ABR path and done some auditory steady-state-evoked response (ASSR) studies, but those (in my view) are just overlapping ABRs at the high modulation rates I have typically focused on. I have also had the opportunity to collaborate in a few functional imaging studies and some vestibular/balance work.
Taking a primacy and a recency perspective, I will bookend my research career to date and pick my doctoral research and my current bottlenose dolphin research as my favorite lines of research.
I went to the University of Wisconsin-Madison for my master’s and PhD in audiology. I received an amazing education in Madison. Bob Goldstein taught me about auditory-evoked potentials. Terry Wiley gave me a firm foundation in instrumentation and acoustic-impedance measures and Ray Karlovich taught me acoustics. I still use this foundational knowledge in my research efforts. They gave me the tools I needed to have a research career.
I also interacted with the faculty in engineering and neurophysiology and prominent hearing scientists (e.g., Bill Rhode, Dan Geisler, John Brugge) took the time to educate me in areas such as auditory physiology and signals and systems. They taught me what I needed to pursue a career in auditory physiology and, without that knowledge, I would have been severely limited in establishing a research program.
After beginning my PhD program, a young pediatric neurologist (Kurt Hecox) took me under his wing and I was tasked with setting up a laboratory and beginning to do experiments in normal-hearing young adults studying the ABR. My dissertation work was studying human ABRs in response to stimulus manipulations including click rate, background masking noise level, and using high-pass subtractive masking to limit where in the cochlea the ABR could arise.
This was one of my favorite times in my career because Kurt Hecox gave me the responsibility of putting together a laboratory, an experience that has helped me set up laboratories as I have changed jobs. In addition, he set me on the path of studying the ABR to various stimulus manipulations that I have continued over the last nearly 40 years.
That takes me to my other favorite line of research—the one I am involved in currently. I’m investigating (mostly) the ABR in the bottlenose dolphin (Tursiops truncatus) to similar stimulus manipulations as performed in my human (and other terrestrial mammal) research. To me, the important part of a research program is the experimental questions asked, the animal species involved, and the folks you are working with.
I think the dolphins are interesting. The technical challenges of experiments with the underwater speakers and microphones—and the dolphins—are substantial. Finally, the people I am working with are great scientists and amazing human beings. The fact that this line of research gets me out of Buffalo to San Diego and I get to spend a few days on San Diego Bay is icing on the cake.
I thoroughly enjoy talking science with the people I’m working with, whether that takes place early in the morning while eating breakfast burritos, during data collection, or later in the afternoon over a beer. My San Diego collaborators have reminded me why I originally fell in love with doing research—it is about both the experimental question AND the collaborators.
It sounds like you were fortunate to have not just one, but a few, important mentors early on who helped shape your career. Who would have known that path would lead to work with marine life? Escaping to San Diego periodically to work with dolphins certainly sounds appealing. I know very little about the dolphins’ auditory system, except that they use echolocation. What are the similarities and the differences between the dolphin and human auditory system?
Both species are mammals, and the cochlea and auditory nervous system appear quite similar. I say appear, as bottlenose dolphins (like humans) are protected from invasive experimentation. What we know about their auditory system is limited, compared to what we know about mice and rats.
The neocortex (including the auditory cortex) of bottlenose dolphins is quite different from that of humans. Cortical differences are, no doubt, in part due to a very long evolutionary timeline separating the two species, as well as the fact that dolphins echolocate and humans do not.
When our mammalian ancestors came out of the ocean, the outer and middle ears evolved for hearing in air, rather than in water. The transfer function of the middle ear attempts to compensate from the ~30 dB loss in acoustic input when going from the low impedance medium of air to the high impedance medium of water.
When cetaceans decided that it was time to return to the sea, the outer and middle ears were not useful for underwater hearing. Thus, in dolphins, there is no external pinna, the ear canal is atrophic, and the middle ear is vestigial. The lateral aspect of the jaw appears to connect to the inner ear via fat pads, but this transmission pathway is not completely understood.
The nominal frequency range of hearing in humans is from 20–20,000 Hz. This, of course, depends on age and how intense the sound can be at the hearing extrema, not to mention that vibrotactile thresholds may likely be below several hundred Hz.
Bottlenose dolphins hear up to ~140 kHz and behavioral studies have shown responses below 1000 Hz. The dolphin inner ear is acoustically isolated from the rest of the skull. If I had to hazard a guess, I would suggest that the dolphins’ high-frequency hearing and the acoustic isolation of the cochlea evolved to enhance echolocation function.
I would imagine, then, that the dolphins’ evoked potentials may be similar, but not exactly the same, as humans. What does a dolphin’s evoked potential waveform look like in comparison to a human’s evoked potential waveform?
The human ABR is a series of five vertex-positive peaks with approximately 1 ms between peaks (e.g., a 4 ms I-V interwave interval). Waves II and IV are often challenging to identify, so we mostly look at waves I, III, and V. Perhaps because of our fat heads, thick skulls, or because we do not hear very well in the high frequencies, the human ABR peak amplitudes are typically less than 1 µV.
The prominent dolphin ABR peaks include positive waves P1, P3, and P4, as well as negative wave N5. The P1–P4 interwave interval to a click is on the order of 2 ms. Dolphin ABR peaks to higher-level click stimuli are typically several µV in amplitude, and may exceed 5 µV.
There appears to be one less positive peak in dolphins than humans, the interwave interval is smaller in dolphins than humans, and the amplitude of the dolphin ABR is larger than in humans.
It would be difficult to imagine that this line of research would have direct clinical applications. However, there are a few “animal electrophysiology” courses that focus on measuring thresholds, particularly in canines. There are also many occurrences of marine life, such as whales and dolphins, that beach themselves for unknown reasons, which some hypothesize could be attributed to sonic interference. How will your findings affect the field of audiology or zoology?
I try to do research that I find interesting and rewarding based on the scientific questions asked, not necessarily because the experimental results will ever be clinically relevant. I use my experience with human ABRs (and those of other terrestrial mammals) to guide some of the experimental questions I ask.
The results of these marine mammal studies are likely not generalizable to humans, but do inform us about the unique auditory system of the bottlenose dolphin. Our results address how to optimize hearing testing of toothed whales (a dolphin is a toothed whale). These stimulus optimizations in bottlenose dolphins include the use of chirps and optimal rates that can be used to obtain ABRs at a specified signal-to-noise ratio in the least amount of time.
There is interest in obtaining audiometric information on marine mammals in the wild (perhaps even stranded animals) to assess the possible consequences of man-made noise on their hearing abilities (and behavior). This would be difficult, if not impossible, using behavioral methods (it is way too time consuming to train the animals). In fact, there is now an American National Standards Institute (ANSI) standard related to performing hearing assessment using the ASSR (I wanted this to be ABR, but I lost that battle) titled “Procedure for determining audiograms in toothed whales through evoked potential methods.”
For audiology, where do you think the next new ideas or “breakthroughs” are going to come from, or where is the biggest knowledge gap?
There is nothing rarer in a scientific field than a new idea. What usually drives a field forward is the development of a new experimental technique that lets you study something that was previously very difficult (or impossible) to study. The ABR was a tool that allowed us to see the auditory periphery and brainstem in a new way. Otoacoustic emissions gave us a window into looking at cochlear micromechanics. Functional imaging made it possible to investigate (non-invasively) the brain’s response to sound.
On the physiological side of things, it would be great if we could find a technique to identify inner hair cell and type I afferent function and separate that from outer hair cell loss and strial changes resulting in a degradation of the endolymphatic potential. It would be game changing if we could record single-unit responses to sound, in the eighth nerve and central auditory nervous system, non-invasively.
I think we have a much better understanding of the auditory system than the vestibular system and hope that techniques are developed and refined allowing us to better diagnose end-organ-specific otolith and canal disorders. I like the emerging body of work on listening effort, as it gets us away from defining hearing loss on the threshold audiogram and moves us into the suprathreshold domain.
Pupillometry is proving useful for the study of cognitive effort and it will be interesting to see where that line of research leads us. Finally, the body of work on acoustic absorbance has led to the possibility of separating incident from reflected sound waves in a sound cavity, with the incident wave being quantified as forward sound pressure.
Coupler measurements of sound pressure ignore individual differences in the acoustics of the outer ear. Currently, there is nothing real about real-ear measures, as those measurements reflect the incident and reflected sound waves at the location of microphone placement, and that may (or may not) faithfully represent the sound pressure at the plane of the tympanic membrane.
The development of replicable measures of forward sound pressure paves the way for true real-ear measurement of sound pressure, which might lead to less variability (across normal hearing young adult subjects) in threshold and could make the audiogram a more sensitive measure of the true sensitivity of the auditory system.
Those are all interesting points to ponder. I hope our readers are encouraged to pursue some of them. To answer some of these questions and move the field further, we need inquisitive minds in people with grit and fortitude. Finally, do you have any advice to new researchers?
Do research on a topic that interests you. It is often challenging to get an experiment to work, to get a grant funded, and/or to get that article published. Unless you are passionate about doing your research, you will have trouble seeing the work through to completion.
Your collaborators are as important as your research question. It is often not possible to do research in isolation and, if you cannot do it yourself, you will need to find collaborators. Sometimes those can be students and hired technicians who will basically do as you say. If you are working with other scientists, they will have their own views on an area of investigation, rules of publishing, and their own scientific and personal strengths and weaknesses.
Pick collaborators whose skill set complements your skill set. If you find yourself working with one or more collaborators and you are unhappy with that collaboration, communicate your reasons for your unhappiness. If you cannot work out your disagreement, end that collaboration and find some new folks to work with.
Periodically change the direction of your research. I am not talking about going from studying the ABR to working in aerospace medicine, but change things up. For example: change jobs, change the animal model you are using, change from normal-hearing to hearing-impaired subjects, or change collaborators.
Change is scary, but often rewarding. It is hard to be innovative after 20 or 30 years of studying exactly the same thing.
At the beginning of this interview, I mentioned some of the many mentors who helped me with my research career. Once you have begun your research career, and achieved some success, serve as a mentor for those with less experience than you.
These could be your own graduate students (if you are in academia) and this could also be someone you ran into at a meeting who was having some career challenges. You can listen and offer advice. The American Speech-Language-Hearing Association MARC (Mentoring Academic-Research Careers) program pairs graduate students, post-docs, and young faculty with more senior faculty. I have served as a MARC mentor and found it personally gratifying.