Evolutionary Biology of Hearing

 

For well over 100 years, investigators have pondered questions regarding the evolutionary origin of the vertebrate ear and about how the ear evolved from its most primitive form to that found in modern mammals. The earliest ideas for the origin of the ear, called the acousticolateralis hypothesis, suggested that the ear evolved from the lateral line (reviewed in Popper et al., 1992). A variety of studies suggested a series of evolutionary changes from the primitive ear to that of modern mammals (see van Bergeijk, 1967). More recent investigators, and particularly those using modern anatomical and physiological methods, now suggest that while the ear and lateral line may share a common ancestor, these are two distinct systems that are unrelated in terms of one giving rise to the other (see Popper et al., 1992). Moreover, as pointed out by Wever (e.g., 1974), we must now question whether there was a steady sequence in the evolution of the vertebrate ear, or whether, in fact, the ear, and regions of the ear, evolved multiple times in the course of vertebrate history, much as very similar ears evolved multiple times in the evolution of invertebrates (e.g., Budelmann, 1992; Hoy, 1992; Popper and Fay, 1997; Fay and Popper, 2000).

The diversity of ear structures and auditory systems among vertebrates is extraordinarily large, and very few data are available even now that help us answer questions related to the evolution of the auditory system. At the same time, it is likely that we may learn more about evolution of sensory systems from studying the auditory system than from any other sensory system. The reason for this is simple. There is a potential wealth of information about evolutionary changes in the ear lying in the fossil record - something that is not available for any other vertebrate sensory system (e.g., Clack, 1997). Moreover, the striking comparative material available for each of the different levels of the vertebrate auditory system (from periphery to CNS) is far richer than for any other sensory system. In essence, the very fact that the ear may have evolved multiple times (see Fritzsch, 1992, p.790) provides a rich body of comparative data upon which to evaluate evolution of the ear.

Why comparative hearing and evolution

Unique and important information about the basic mechanisms of hearing come from research using diverse species. Often specific questions regarding human auditory function can be approached and answered by selecting a species for study that allow exploration of the auditory system in ways that are not easy to accomplish in humans. Clearly, the science of hearing and auditory neuroscience has benefited greatly from the comparative approach and from viewing animals in the context of their evolutionary relationships.

Using but a few examples from work of TP faculty, studies by Carr on the auditory system of owls has provided insight into time coding in the auditory system (Carr et al., 2001), whereas work on ferrets by Shamma and his colleagues provide for a deeper understanding of cortical processing (Fritz et al, 2007). A better understanding of hair cell regeneration and post-embryonic proliferation comes from work on fish by Popper (Kwan et al., 2006), whereas Dooling and colleagues have used birds to explore issues of recovery of hearing after hair cell regeneration (Dooling et al, 2006).

Other examples of basic research in non-mammalian species that have driven the field include: (1) The study of nucleus laminar in birds has improved understanding of MSO function, and helps explain how and why localization of low-frequency sounds is not easy for patients with a single cochlear implant (see Middlebrooks et al., 2005); (2) The finding that interrupted or altered auditory feedback slows the degradation of birdsong leaves no doubt about the importance of auditory feedback in speech production (see Mooney, 2004); (3) The finding that hair cells regenerate in birds opened the possibility that hair cells can be made to regenerate in mammals (reviewed in Meyer & Corwin 2008; Oesterele & Stone 2008); (4) The clear and easily defined repertoire of songbirds has allowed investigation into the role of how neurons reflect auditory experience in sleep (e.g., Konishi, 2004); (5) Studies on turtles, frogs, and birds have formed the basis for understanding the biophysics of hair cells because their hair cells survived more easily in vitro than mammalian hair cells (e.g., Gillespie and Hudspeth 1991); (6) The biophysics of hair cells has in turn led to an understanding of how loud noise can damage them (e.g., Henderson et al. 2008; Saunders & Salvi 2008); and (7) Mice and zebrafish are the major models for studying the genetics of hearing loss (e.g., Shalit & Avraham 2008)

Studies of comparative and evolutionary biology of hearing at UM

Our group is composed of laboratories studying hearing using different animal groups and different experimental paradigms. This diversity enables our faculty and students to appreciate the value of a comparative approach in modern biology, to address questions that cannot be studied using human models, and to select model systems that also provide insight into the evolution of the vertebrate auditory system (e.g., Popper's work on evolution of hair cells – Coffin et al. 2004; Carr's work on evolution of the auditory CNS – Carr & Edds-Walton 2008; and Dooling's studies related to hearing in dinosaurs – Gleich et al. 2005). We encourage selection of model systems that promote understanding of broad issues in hearing, and aid in uncovering mechanisms involved in human hearing disorders.
Beyond providing very intensive training in auditory neuroscience, our TP emphasizes two separate, but closely related, issues: comparative auditory function and structure, and the evolution of the auditory system.

The major goal of our program is to produce auditory neuroscientists who understand the diversity of hearing mechanisms and the evolution of the auditory system so that they are able to identify appropriate models to ask questions of fundamental importance central to the function of the auditory system in health and in disease. Examples include understanding of hair cell repair and regeneration using fish and birds; (e.g., Dooling and Popper labs); developing new types of hearing aids using information learned from insects and frogs (e.g., Yager lab); understanding mechanisms of sound source localization using bats (e.g., Moss lab), birds (Carr and Dooling labs), or fish (Popper lab); and exploring aging in the auditory system (e.g., Gordon-Salant).

Our theme of the comparative and evolutionary biology of hearing follows naturally from the work of our Core Faculty.

References

Carr, CE and Edds-Walton, P. (2008) Vertebrate Auditory Pathways. In: Handbook of the Senses Volume 1. Audition. Eds. Hoy, R, Dallos, P and Oertel, D (eds) Elsevier, Oxford.

Carr CE, Soares D, Parameshwaran S, Perney T. (2001) Evolution and development of time coding systems.Curr Opin Neurobiol. 11:727-33.

Coffin, A., Kelley, M., Manley, G.A., and Popper, A.N. (2004). Evolution of sensory hair cells. In: Evolution of the Vertebrate Auditory System (eds. G.A. Manley, A.N. Popper, and R.R. Fay). Springer-Verlag, New York, 55-94.

Costello, L. C., Franklin, R. B., and Ashe, W. K. (1994). Black physiologists: Where are they? The Physiologist 37:284-286.

Dooling RJ, Ryals BM, Dent ML, Reid TL. (2006) Perception of complex sounds in budgerigars (Melopsittacus undulatus) with temporary hearing loss. J Acoust Soc Am. 119:2524-32.

Fields, C. D. (1998). Trouble along the science pipeline. Black Issues in Higher Education, March 19, 1998, pp. 14-15.

Fritz JB, Elhilali M, David SV, Shamma SA. (2007) Auditory attention--focusing the searchlight on sound. Curr Opin Neurobiol. 17:437-55.

Gillespie, P.G. and Hudspeth, A. J. (1991). High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J. Cell Biol. 112: 625-640.

Gleich, O., Dooling, R. J., and Manley, G. A. (2005). Audiogram, body mass and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenshaften, 92, 595-598.

Harvey, William. (2001). Eighteenth annual status report on minorities in higher education. Washington, DC: American Council on Education.

Henderson, D., Hu, B., and Bielfeld, E. (2008). Patterns and mechanisms of noise-induced cochlear pathology. In Auditory Trauma, Protection, and Repair, eds. Schacht, J. Popper, A. N., and Fay, R. R. Springer Science + Business Media, New York, pp. 195-218.

Konishi M. (2004) The role of auditory feedback in birdsong. Ann N Y Acad Sci. 1016:463-75.

Kwak SJ, Vemaraju S, Moorman SJ, Zeddies D, Popper AN, Riley BB. (2006) Zebrafish pax5 regulates development of the utricular macula and vestibular function. Dev Dyn. 235:3026-38.

Ma, J. (2005). Trends and issues: Recruiting and retraining female and minority faculty. TIAA-CREFInstitute. http://www.tiaa-crefinstitute.org/research/trends/docs/Tr070105c.pdf

Meyer, J. R. and Corwin, J. T. (2008). Morphological correlates of regeneration and repair in the inner ear. In Hair Cell Regeneration, Repair, and Protection, eds Salvi, R. J., Popper, A. N., and Fay, R. R. Springer Science + Business Media, New York, pp. 39-76.

Middlebrooks, J. Arenberg Bierer, J., and Snyder, R. L. (2005). Cochlear implants: the view from the brain. Curr. Opinion. Neurobiol. 15:488.493.

Mooney R. (2004) Synaptic mechanisms for auditory-vocal integration and the correction of vocal errors. Ann N Y Acad Sci. 1016:476-94.

Oesterele, E. C. and Stone, J. S. (2008). Hair cell regeneration: Mechanisms guiding cellular proliferation and differentiation. In Hair Cell Regeneration, Repair, and Protection, eds Salvi, R. J., Popper, A. N., and Fay, R. R. Springer Science + Business Media, New York, pp. 141-198.

Saunders, J. C. and Salvi, R. J. (2008). Recovery of function in the avian auditory system. In Hair Cell Regeneration, Repair, and Protection, eds Salvi, R. J., Popper, A. N., and Fay, R. R. Springer Science + Business Media, New York, pp. 77-116.

Shalit, E. and Avraham, K. B. (2008) Genetics of Hearing Loss. In Auditory Trauma, Protection, and Repair, eds. Schacht, J. Popper, A. N., and Fay, R. R. Springer Science + Business Media, New York, pp. 9-48.