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Probing cochlear tuning and tonotopy in the tiger using otoacoustic emissions

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Abstract

Otoacoustic emissions (sound emitted from the ear) allow cochlear function to be probed noninvasively. The emissions evoked by pure tones, known as stimulus-frequency emissions (SFOAEs), have been shown to provide reliable estimates of peripheral frequency tuning in a variety of mammalian and non-mammalian species. Here, we apply the same methodology to explore peripheral auditory function in the largest member of the cat family, the tiger (Panthera tigris). We measured SFOAEs in 9 unique ears of 5 anesthetized tigers. The tigers, housed at the Henry Doorly Zoo (Omaha, NE), were of both sexes and ranged in age from 3 to 10 years. SFOAE phase-gradient delays are significantly longer in tigers—by approximately a factor of two above 2 kHz and even more at lower frequencies—than in domestic cats (Felis catus), a species commonly used in auditory studies. Based on correlations between tuning and delay established in other species, our results imply that cochlear tuning in the tiger is significantly sharper than in domestic cat and appears comparable to that of humans. Furthermore, the SFOAE data indicate that tigers have a larger tonotopic mapping constant (mm/octave) than domestic cats. A larger mapping constant in tiger is consistent both with auditory brainstem response thresholds (that suggest a lower upper frequency limit of hearing for the tiger than domestic cat) and with measurements of basilar-membrane length (about 1.5 times longer in the tiger than domestic cat).

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Notes

  1. We were unable to measure the lengths of the external ear canals in the tigers studied here. Using a 7-cm estimate obtained previously from one specimen, and assuming an upper bound of 25 % on the tiger-to-tiger variability, yields a corresponding uncertainty of less than 0.1 ms in the round-trip emission delay. At 10 kHz, this corresponds to an uncertainty of about 1 period in N SFOAE, or about 5 %. This 5 % uncertainty carries over to our estimate of Q ERB.

  2. OAEs have been suggested to be of value in clinical veterinary contexts (e.g., McBrearty and Penderis 2011).

  3. The ERB is a parameter-free measure of tuning bandwidth commonly adopted in the psychophysical literature. For any filter, the ERB is the bandwidth of the rectangular filter with the same peak response that passes the same total power when driven by white noise (Shera et al. 2010).

  4. Several studies examining the mammalian tonotopic map have suggested that it can deviate from a simple exponential form at frequencies below about a few hundred Hz (Greenwood 1990), potentially facilitating sensitivity and selectivity across frequency (Lepage 2003; Vater and Kössl 2011). However, deviations from an exponential map appear not to occur in several small mammals such as guinea pig (Tsuji and Liberman 1997), mouse (Müller et al. 2005), and chinchilla (Müller et al. 2010). It is not known whether significant deviations from an exponential map are present in the tiger cochlea, or if tigers can be considered ‘auditory specialists’ (Vater and Kössl 2011) for other reasons (Walsh et al. 2011a). While a transition in cochlear processing between the base and apex (e.g., loss of scaling invariance) occurs in the mammalian cochlea (Shera and Guinan 2003; Temchin et al. 2008; Shera et al. 2010), the existence of the transition has not been shown to correlate with deviations from an exponential tonotopic map.

Abbreviations

ABR:

Auditory brainstem response

BM:

Basilar membrane

DPOAE:

Distortion-product otoacoustic emission

ERB:

Equivalent rectangular bandwidth

OAE:

Otoacoustic emission

SFOAE:

Stimulus-frequency otoacoustic emission

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Acknowledgments

The support, advice, and assistance of the veterinarians and staff of the Henry Doorly Zoo were invaluable to the completion of this study. All procedures were approved by the Institutional Animal Care and Use Committee. We thank Sebastiaan Meenderink and John Rosowski for helpful comments on the manuscript. The work was supported by the National Science Foundation (grants 0823417 and 0602173), the Howard Hughes Medical Institute (grant 52003749), and the National Institutes of Health (grants R01 DC003687 and P30 DC05209).

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Authors and Affiliations

  1. Department of Otolaryngology/Head and Neck Surgery, Columbia University, 630 W. 168th St., P&S 11–452, New York, NY, 10032, USA

    Christopher Bergevin

  2. Boys Town National Research Hospital, 555 North 30th Street, Omaha, NE, 68131, USA

    Edward J. Walsh & JoAnn McGee

  3. Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA, 02114, USA

    Christopher A. Shera

  4. Department of Otology and Laryngology, Harvard Medical School, Boston, MA, 02115, USA

    Christopher A. Shera

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  1. Christopher Bergevin
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  2. Edward J. Walsh
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  3. JoAnn McGee
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  4. Christopher A. Shera
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Correspondence to Christopher Bergevin.

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Bergevin, C., Walsh, E.J., McGee, J. et al. Probing cochlear tuning and tonotopy in the tiger using otoacoustic emissions. J Comp Physiol A 198, 617–624 (2012). https://doi.org/10.1007/s00359-012-0734-1

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  • DOI: https://doi.org/10.1007/s00359-012-0734-1

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