Eric Daniel Young

It is with great sadness that we heard the news that Eric Daniel Young, the inaugural Editor-in-Chief of JARO (2000–2005), passed away on February 2, 2024. Eric was raised in Nevada on a cattle ranch, but developed an interest in computers at an early age, and left Nevada to purse a degree in engineering at the California Institute of Technology. Subsequently he went to The Johns Hopkins University to earn a PhD in Biomedical Engineering, working with Murray Sachs, and then to a postdoctoral position at the University of Chicago with Jay Goldberg. He then returned to Johns Hopkins as a faculty member in the Department of Biomedical Engineering, where he remained for 40 years until his retirement in 2015. After retirement, he continued contributing his computational skills and extensive knowledge of the auditory system in collaborations on hair cell synaptic transmission.

Eric was known for his rigorous experimental and analytical approaches, extensive quantitative and thoughtful analysis, and cautious interpretation of results. He was a strong proponent of letting the data speak for itself, while also mining the data for clues that could help understand mechanisms and sensory processing feats. He was appropriately skeptical, and always encouraged others to think carefully and deeply about their work and its limitations. As an undergraduate, his work with Roger Sperry and Michael Gazzaniga, led to his first scientific paper on how commissurotomy affects visual processing [1]. His graduate work with Murray Sachs led to a pair of papers in the Journal of the Acoustical Society of America on the recovery of detection thresholds following long pure tones, comparing cat single-fiber recording from the auditory nerve and human psychophysics [2, 3]. As a postdoc in Jay Goldberg’s lab, Eric performed the first detailed study of the responses of vestibular saccular neurons to sound [4], as well as a landmark study on the frequency response areas of dorsal cochlear nucleus (DCN) neurons with Bill Brownell [5]. Upon Eric’s return to Hopkins, he followed three main avenues of research into hearing and hearing loss.

The first avenue was propelled by the observations on the intriguing responses of DCN neurons to tones versus noise in the 1976 paper. In a series of studies between 1980 and 2015 [6–8], he and his colleagues defined much of our current understanding of the functional relationship between DCN fusiform cells and their inputs, and the spectral sensitivity of fusiform cells [9–12], including spectral edges [13]. As a side note, an interesting aspect of this series of studies is that the paper titles never mention cell types by their morphology, but rather refers to the recorded cells by their categorical response properties or as “principal” cells. This choice recognizes a fundamental limitation of these single unit studies, where multiple anatomical cell classes may share aspects of sensory responses, so that the reverse mapping of response classification to cell type is not necessarily one-to-one (e.g., type IV responses may be generated by both fusiform and another large cell type, called giant cells). Nonetheless, through an accumulation of different types of evidence, including pairwise cross-correlation analysis and insightful spectral manipulations of noise bands and tones, this series of studies resulted in the now widely accepted organization of narrow-band inhibition onto fusiform cells that is provided by vertical cells, and wide-band inhibition arising from the D-stellate (radiate multipolar) cells in the ventral cochlear nucleus that impacts both vertical cells and fusiform cells. Detailed analytical studies of the nonlinearities of the principal cell responses ensued, using a variety of approaches in signal processing, including a novel approach with random spectral stimuli [14–16]. From these studies, it became evident that the principal cells have a rather complex and non-linear receptive field structure. Subsequent studies investigated the effects of noise-induced hearing loss, which appears to upset the delicate balance of the synaptic circuitry around the principal cells, and severely distorts their responses to sound [17, 18].

Following the anatomical demonstrations of somatosensory inputs to the granule cell system of the DCN by other groups, Eric’s lab embarked on second set of studies focused on the representation of these somatosensory inputs and their influence on the principal cell responses. This work developed in part around the hypothesis that DCN principal cells are sensitive to spectral shape (including spectral notches and spectral edges, as noted above). This hypothesis was reinforced by measurements of the spectral transform of the pinnae in cats [19, 20], which revealed how the spectral shape of wideband sounds could hold clues regarding sound location relative to the head. This series of studies clarified that one pathway arose from C1 and C2 of the spinal cord, representing peri-aural proprioceptive (but not cutaneous) information about pinna orientation that would be essential to interpret spectral cues [21–24]. In addition, the somatosensory inputs seemed to engage the DCN circuits through multiple pathways, including a circuit deep in the nucleus, as well as the through the granule cell-parallel fiber system in the molecular layer of the nucleus [22]. These studies built a strong foundation for understanding one of the roles that the DCN could play in auditory processing, and also suggested why this multisensory convergence occurs so early in the auditory pathway.

A second major avenue of research was on the population representation of speech sounds in the normal and noise-damaged auditory nerve. This work resulted in a number of key papers in the field attempting to understand how speech might be coded in auditory nerve spike trains at high versus low sound level, via both rate-place coding and phase-locking (temporal) coding [25, 26], and the degradation of his representation by hearing loss [27–30]. Using principally tone-induced hearing loss, these studies revealed a complex set of changes in the nerve’s representation of sounds in ways that are not readily amenable to correction by simple amplification, but indicated that some aspects, such as synchrony capture of the second formant of vowels, may be retrievable by using appropriate spectrally-shaped stimuli. It is also clear when reading these papers that this avenue of research was heavily guided by, and contrasted against, studies of human psychophysical performance in hearing-impaired subjects. This line of work eventually extended into the central nervous system [17, 18, 31, 32], when it was recognized that many of the effects of noise-induced hearing loss on auditory perception could not be adequately explained by the changes in the peripheral representation in the auditory nerve.

A third avenue of investigation started later in Eric’s career, with a transition to studies of the inferior colliculus, a region often considered a midbrain nexus for auditory processing. These studies largely focused on using sound localization cues (interaural time and level differences, and spectral shape) to probe their representation in spike trains, and integration between cue domains [33–35], in the inferior colliculus and the brachium of the inferior colliculus in marmosets. As with prior work, a panoply of quantitative methods, including the use of virtual stimuli, random spectrum stimuli, and measurement of mutual information, were applied to analyze and compare spike trains and their relationship to the stimuli. One interesting conclusion from this series of studies was that expected patterns of aligned integration based on binaural cue sensitivity (interaural timing and level differences) and likely brainstem sources were not always present in the inferior colliculus, whereas neurons in the brachium of the inferior colliculus seemed to carry more information when these localization cues were aligned [36].

On a personal note, Eric had a tremendous influence on my own interests and approach to studying the auditory system, starting when I was a graduate student. His early work in the DCN [5, 6] initiated questions about the specific circuits of the nucleus and the construction of sensory responses by these circuits that continue to this day. Later, I was privileged to be able to collaborate with Eric through co-mentoring of several graduate students. These collaborations initially formed based on his quantitative approaches to understanding neural function, and focused on the intersection between experimental observations and models [37–39]. In subsequent work, this evolved in to parallel explorations using cellular and systems approaches to understanding multisensory integration in the DCN [40]. Discussions with Eric were always invigorating and often led to reconsideration of hypotheses or thoughts for new experiments.

Upon re-reading many of the papers out of Eric’s lab, it is notable how the discussion sections are carefully crafted and represent a deep and critical coverage of the results in the context of the prior literature. Results are clearly discussed, caveats introduced, and the relationship to prior work is extensively and thoughtfully considered. The discussions pointed out not only the most substantial advances, but equally (and sometimes more) importantly, the reasons that certain issues remained unresolved. These discussion sections also often included a wide-ranging evaluation of the literature, from consideration of cellular mechanisms and limitations of models, through the relationship of the observations to human auditory perception. Indeed, it is clear that trying to reconcile the physiological observations, particularly those associated with sound-induced hearing loss, with the performance of human subjects, presented a multidimensional puzzle in which insights into sensory coding and the amelioration of the consequences of hearing loss could provide important clues to refine hypotheses in both domains, with a long-term goal of ultimately improving the treatment of hearing loss.

In recognition his extraordinary contributions to auditory neuroscience, Eric was inducted into the first class (1996) of College of Fellows of American Institute for Biological and Medical Engineering, received a Claude Pepper Award from NIDCD, and was awarded the ARO Award of Merit in 2007. He was a Fellow of the Acoustical Society of America and served as the Director of the Johns Hopkins’s Center for Hearing and Balance. Eric’s work was primarily supported by an R01 for 38 years, first for studying the cochlear nucleus, auditory nerve and hearing loss, and then transitioning to the inferior colliculus. He was also an investigator on the Hearing and Balance Center’s P60 research training center grant, a co-investigator on other grants, the principal investigator on two training grants from NIDCD.

Although Eric was very focused on his science, he also played a key role in establishing the Journal of the Association for Research in Otolaryngology (JARO), serving both on the publications committee of ARO and then as the founding Editor-in-Chief of the journal [41]. He recruited a premier who’s-who of researchers in otolaryngology and hearing sciences for the first editorial board and initiated and oversaw a rigorous but fair peer-review process. He also chose the original format for the journal cover and manuscript layout. The first issue of the journal was published in August, 2000 (Vol1, Issue1), and had 99 pages with 7 papers. At that time, only 4 issues were published per year. In Eric’s opening Editorial, he laid out the rationale for the journal, set the scope of the work that the journal would consider, emphasized that all papers would be reviewed by at least 2 reviewers (in practice, at least 2 and often 3), and gave credit to the key players that enabled the journal to be established: Ed Rubel, then ARO president; Art Popper and Gerald Popelka, key members of the publications committee. Eric started the journal in the paper age, when manuscript submission was by mail (although a 3.5 floppy or Zip-100 disk was required to be submitted as well), review was by e-mail, and proofing was done with mark-up on a paper copy. The transition to electronic manuscript handling did not happen until Ruth Anne Eatock became Editor-in-Chief. Eric also instituted a preprint server in early 2005, that put papers on-line once they were accepted, but before they had gone through the production stage, complete with a DOI number. This was certainly a forward-looking move!

Eric was an exceptional mentor and collaborator, and many of his students and postdoctoral trainees have continued to work and extend his scientific ethos to push the boundaries of knowledge in the auditory system. His lasting impact on our understanding of how the auditory system functions and encodes sound lives on with those who worked with him, and those who were influenced by his approach to science and his insights into auditory sensory processing.

Paul B. Manis

JARO Editor-in-Chief, 2011–2022

Funding

No funding was received to assist with the preparation of this manuscript.

Declarations

Competing Interests

The author reports no competing interests.