Spontaneous otoacoustic emissions in the barn owl
Introduction
The inner ear is not only a passive organ receiving sound but can itself also produce sound. The notion that frequency-selective elements of the inner ear actively participate in the hearing organ's movement and amplify the displacement is now widely accepted. This concept has been termed the cochlear amplifier mechanism (Davis, 1983). Otoacoustic emissions (OAE) are usually interpreted as a by-product of this active process, whose primary function is to amplify the micromechanical oscillations in the hearing organ and to sharpen the frequency selectivity of the basilar membrane-organ of Corti complex. Although they had been anticipated since 1948 from theoretical considerations about a feedback mechanism between mechano-electrical and electro-mechanical transduction that could account for the high frequency selectivity of the inner ear (Gold, 1948), OAE of the cochlea were not measured until thirty years later (Kemp, 1978). Since then, much research work has focused on the investigation of OAE, which, as a new and non-invasive method has brought new insights into the function of the inner ear.
The various kinds of OAE have been divided into two main categories: spontaneous and evoked emissions (for review see Zurek, 1985; Probst et al., 1991). Spontaneous OAE (SOAE) are narrow-band acoustic signals that are emitted in the absence of any external acoustic stimulation. They originate from spontaneously active hair cells and are primarily found in frequency domains which are perceived with high sensitivity. SOAE have been measured in several mammalian species including man, in frogs (for review see Probst, 1990; Köppl, 1995), in lizards (Köppl and Manley, 1993a, Köppl and Manley, 1993b, Köppl and Manley, 1994; Manley et al., 1996) and preliminary data have also been reported from a bird, the barn owl (Manley and Taschenberger, 1993). The presence of SOAE in all classes of terrestrial vertebrates suggests that the active production of mechanical energy is a primitive property of auditory hair-cell epithelia, perhaps based on a common mechanism (review in Köppl, 1995). Because there are not only a number of anatomical differences between the inner ear of birds and that of mammals, but also numerous structural as well as functional parallels (Klinke and Smolders, 1993; Manley et al., 1989) which suggest that some common mechanisms exist in the function of hair cell populations of both classes of vertebrates, comparative studies on the hearing organ of birds are especially interesting.
The basilar papilla of birds and the organ of Corti of mammals developed independently from the ancestral hearing organ of stem reptiles (Manley, 1990). During evolution, mammalian hair cells differentiated into two morphologically and functionally distinct receptor-cell classes: inner hair cells (IHC) and outer hair cells (OHC) at the neural and abneural position of the hearing organ, respectively. A similar pattern is found in birds and crocodiles, where tall hair cells (THC) on the neural side and short hair cells (SHC) on the abneural side can be distinguished, albeit less clearly. There are several pieces of evidence that argue for functional parallels between THC and IHC on the one hand and SHC and OHC on the other, such as their location on the respective hearing organ and the innervation pattern (Manley, 1990). Similarities are also apparent in their ontogeny. In birds, however, some highly specialized hair cells that were recently designated as SHC in a more narrow sense (Fischer, 1994a, Fischer, 1994b) entirely lack an afferent innervation (Fischer, 1992; Manley and Gleich, 1992). This unique characteristic of the hearing organ of birds makes a detailed investigation of OAE in these animals very relevant to our understanding of the differentiation of hair-cell populations.
One species which is unusual among birds due to several auditory specializations and which has therefore been repeatedly used as a model animal for the investigation of the performance and function of the auditory system (Knudsen and Knudsen, 1990; Konishi, 1993) is the barn owl, Tyto alba. The barn owl localizes sounds extremely accurately (Knudsen and Konishi, 1979; Knudsen et al., 1979; Payne, 1971) and, compared with other birds, shows unusually sensitive high-frequency hearing (Konishi, 1973). Early experiments by Payne (1971)and Konishi (1973)demonstrated that the barn owl can capture its prey purely on acoustic cues.
The hearing organ of the barn owl is one of the most complex among birds with a length of 11 mm and a total number of 16 300 hair cells (Fischer et al., 1988). It also has an unusually large number of afferent fibres in the auditory nerve (>31100; Köppl, 1997b). In the apical third, the innervation pattern of the hair cells is similar to that of other birds. However, in the basal part of the Papilla basilaris, which perceives high frequencies, the number of afferent nerve terminals per receptor cell is strongly increased for neurally located hair cells. Whereas about two afferent synapses per hair cell are usually observed in other bird species, in the barn owl up to 20 afferent fibres terminate on a single hair cell. This is close to the situation of mammalian IHC (Fischer, 1994a, Fischer, 1994b). For lower frequencies, the frequency map on the Papilla basilaris of the barn owl is similar to what is known from other birds. The highest octave of the owl's hearing range (5 to 10 kHz), however, shows greatly expanded frequency mapping. This expanded spatial representation of the animal's upper hearing range has been termed an auditory fovea (Köppl et al., 1993). Although several morphological specializations of the auditory system have already been demonstrated in this species, and almost every step in acoustic processing up to the owl's midbrain has been investigated physiologically, relatively little is known about the peripheral processing of sound by the barn owl.
The aim of the present study was to obtain more information about the preneural and mechanical elements in the barn owl's basilar papilla. The sound field in the external ear canal was investigated, in order to describe the characteristic features of the SOAE and their responses to changes in body temperature and to applied external pure-tone stimuli.
Section snippets
Materials and methods
The measurements were carried out on 19 adult barn owls (Tyto alba guttata) from our own breeding colony. The experiments were non-invasive; however, a light anaesthesia was necessary to ensure that the animals did not move. The animals were anaesthetized by an initial i.m. injection of xylazine (3 mg/kg, Rompun, Bayer), followed 5 min later by ketamine (4 mg/kg, Ketavet, Parke-Davis). Light anaesthesia was maintained by administering half of the respective initial doses after every 30 to 100
Results
Within the averaged spectrum, SOAE were evident as signals with a very narrow bandwidth. Peaks in spectra were accepted as SOAE if they were gradually and reversibly suppressible by suitable external tones. For further analyses, a standard spectrum of the subjectively `best' screening day in terms of SOAE number and amplitude of each ear was selected.
Seventeen of 19 barn owls investigated (89.5%) showed clear SOAE with a level of at least 1.5 dB above noise (i.e., with an amplitude greater than
Discussion
SOAE have been reported for all classes of terrestrial vertebrates: from mammals including humans (reviews in Zurek, 1985; Probst, 1990; Köppl, 1995), anuran amphibians (Genossa et al., 1989; Palmer and Wilson, 1982; Van Dijk et al., 1989; Wilson et al., 1990), reptiles (lizards: Köppl and Manley, 1993a, Köppl and Manley, 1993b; Manley et al., 1993) and a bird (Manley and Taschenberger, 1993and this report). Considering the large differences in inner-ear morphology between amphibians, reptiles,
Acknowledgements
This work was supported by a grant to G.A. Manley from the Deutsche Forschungsgemeinschaft within the program of the SFB 204 `Gehör'. We thank A. Kaiser and C. Köppl for comments on an earlier version of the manuscript.
References (73)
- et al.
Spontaneous otoacoustic emissions in chinchilla ear canals: correlation with histopathology and suppression by external tones
Hear. Res.
(1984) An active process in cochlear mechanics
Hear. Res.
(1983)Quantitative analysis of the innervation of the chicken basilar papilla
Hear. Res.
(1992)Quantitative TEM analysis of the barn owl basilar papilla
Hear. Res.
(1994)- et al.
The basilar papilla of the barn owl Tyto alba: a quantitative morphological SEM analysis
Hear. Res.
(1988) - et al.
First appearance and development of electromotility in neonatal gerbil outer hair cells
Hear. Res.
(1994) Otoacoustic emissions, travelling waves and cochlear mechanisms
Hear. Res.
(1986)Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system
Hear. Res.
(1986)- et al.
Performance of the avian inner ear
Progr. Brain Res.
(1993) - et al.
Spontaneous otoacoustic emissions in the bobtail lizard. I: General characteristics
Hear. Res.
(1993)