Mammalian behavior and physiology converge to confirm sharper cochlear tuning in humans - PubMed (original) (raw)

Mammalian behavior and physiology converge to confirm sharper cochlear tuning in humans

Christian J Sumner et al. Proc Natl Acad Sci U S A. 2018.

Abstract

Frequency analysis of sound by the cochlea is the most fundamental property of the auditory system. Despite its importance, the resolution of this frequency analysis in humans remains controversial. The controversy persists because the methods used to estimate tuning in humans are indirect and have not all been independently validated in other species. Some data suggest that human cochlear tuning is considerably sharper than that of laboratory animals, while others suggest little or no difference between species. We show here in a single species (ferret) that behavioral estimates of tuning bandwidths obtained using perceptual masking methods, and objective estimates obtained using otoacoustic emissions, both also employed in humans, agree closely with direct physiological measurements from single auditory-nerve fibers. Combined with human behavioral data, this outcome indicates that the frequency analysis performed by the human cochlea is of significantly higher resolution than found in common laboratory animals. This finding raises important questions about the evolutionary origins of human cochlear tuning, its role in the emergence of speech communication, and the mechanisms underlying our ability to separate and process natural sounds in complex acoustic environments.

Keywords: auditory nerve; cochlear tuning; frequency selectivity; otoacoustic emissions; psychoacoustics.

Copyright © 2018 the Author(s). Published by PNAS.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Three different ways of estimating cochlear tuning used in ferrets. ANFs, threshold levels (gray line) for a response are fit with a filter model (red line), from which the ERB (dashed gray line) is calculated. OAEs, the mean phase gradient of OAEs (red line) is used to estimate filter sharpness, QERB (=f/ERB), using the approximate species invariance of the tuning ratio. PSY, the behavioral detection of a pure tone in the presence of two bands of noise, separated by varying spectral distances. ERB (blue dashed line) is estimated by fitting a filter model to the detection thresholds. ANF data from ref. .

Fig. 2.

Fig. 2.

Three measures of frequency selectivity agree. (A) Filter sharpness from PSY-F agrees closely with ANF and OAE measurements. Tuning in individual nerve fibers (gray points), psychophysical forward masking (blue points), and a loess trend and its bootstrapped 95% CI for the otoacoustic emissions measurements. Dashed lines indicate bootstrapped 95% CIs for the data. (B) Forward masking (PSY-F; blue points, n = 8) yields a better match to auditory nerve tuning than simultaneous masking (PSY-S; magenta points, n = 22). In B, auditory nerve data are shown as the area within the loess (

SI Appendix, Experimental Methods

) trend 95% CI. ANF data from ref. .

Fig. 3.

Fig. 3.

Comparing different measures of frequency resolution in the ferret, independently of the effect of signal frequency. (A) The different tuning measurements as a fraction of the mean ANF tuning at a given frequency. Dashed red lines show excluded OAE outliers (see

SI Appendix, Experimental Methods

). (B) Statistical comparison of the different measures of tuning. Horizontal bars show the mean of each measure as a fraction of auditory nerve tuning and also as effect size (relative to ANF tuning). Asterisks next to data points indicate significant differences compared with auditory nerve tuning. *P < 0.05; **P < 0.01; ***P < 0.001.

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