A behavioral test of presbycusis in the bird auditory system
Introduction
Unfortunately, aging in humans is associated with a gradual deterioration of sensory systems. One of the senses affected is the auditory system which plays an important part in our communication. Presbycusis, i.e. the deterioration of auditory sensitivity with age, may be attributed to changes and deficiencies in the peripheral or in the central parts of the auditory system. Presbycusis can result in an impaired ability for speech recognition and speech discrimination (for a comprehensive overview on psychophysical aspects of presbycusis and speech perception, see Willott, 1991). Not only humans but also other mammals frequently show presbycusis which results from deficits in the auditory periphery. Thus, mammals other than humans have been used as models to provide for a better understanding of the causes of human presbycusis. Once mammals develop hearing deficits they cannot restore auditory function. One reason is certainly that the sensory epithelium of the inner ear shows no regeneration of defects (e.g. Pickles, 1988, Corwin and Oberholtzer, 1997).
In contrast, birds have been shown to regenerate a defective sensory epithelium. This ability was thought to occur only in lower vertebrates (e.g. in fish and amphibians, see Corwin, 1992, Corwin and Oberholtzer, 1997). The remarkable capacity of the bird auditory system was demonstrated in experiments after acoustic trauma or treatment with ototoxic substances (e.g. Cotanche, 1987, Cruz et al., 1987, Corwin and Cotanche, 1988, Ryals and Rubel, 1988; for recent reviews see Cotanche et al., 1994, Cotanche, 1997). The avian cochlea does not only regenerate defective hair cells, auditory function also recovers, although the two processes may not necessarily proceed synchronously (Saunders et al., 1992, Pugliano et al., 1993, Niemiec et al., 1994, Müller and Smolders, 1999; see also reviews in Corwin, 1992, Cotanche, 1997).
The finding that birds show a remarkable ability to regenerate hair cells in their inner ear raises the issue whether they lack the age-dependent hearing loss typically found in mammals. To our knowledge, no long-term investigation has been conducted to study the change of auditory performance in aging birds (for a study of hair cell regeneration in the European starling after administration of ototoxic antibiotics, see Marean et al., 1993, 1998). Despite morphological differences between the mammalian and avian cochlea, both systems exhibit remarkable analogies regarding their auditory function (Manley et al., 1989, Fay, 1992; see also Buus et al., 1995). Thus studies in birds can provide important insights into mechanisms of age-related auditory deficiencies in humans.
Section snippets
Subjects
Subjects were 12 European starlings (Sturnus vulgaris), six of which were 6 to 12 months of age during the experiments (three young males, three young females); the other six birds were 8 to at least 13 years old (three old males, three old females). From two of the old females we have obtained auditory thresholds four times in the course of 11 years. We obtained the starlings between autumn 1985 and autumn 1996; they had lived since then without any obvious health problems in our laboratory
Results
The auditory thresholds obtained from young and old starlings are presented in Fig. 1a,b, respectively. In both age classes, the most sensitive thresholds were found for signal frequencies between 1 and 6 kHz (mean thresholds between 4.2 and 14.8 dB SPL). The audibility functions of the birds can be characterized in terms of seven parameters that allow easy comparison between audiograms (see Dooling, 1980, Dooling, 1992). (1) Best intensity, i.e. the most sensitive threshold of the audibility
Starling auditory sensitivity.
A comparison between thresholds of a large sample of old starlings (N=6; age at least 8 to 13 years) and an equal number of young starlings (age between 6 and 12 months) revealed only small differences between the two age groups. Old birds were on average between 1.5 and 6.1 dB less sensitive for various test frequencies. The size of these differences, however, does not indicate a substantial hearing loss. (The relevance of absolute thresholds for birds in the natural environment is discussed
Acknowledgements
Supported by Grants to G.M. Klump from the Deutsche Forschungsgemeinschaft within the SFB 204 ‘Gehör’ and within the FG ‘Hörobjekte’. Threshold data from 1986 and 1988 were determined in the laboratory of G.M. Klump as part of the Diplom thesis by Elke Maier and Andreas Baur, respectively. We thank Georg M. Klump, Otto Gleich, Christine Köppl and Søren Buus and two anonymous referees for discussion and helpful comments on a previous version of the manuscript.
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Present address: HNO-Klinikum Universität Regensburg, Postfach, D-93042 Regensburg, Germany