Frequency selectivity in Old-World monkeys corroborates sharp cochlear tuning in humans

Abstract

Frequency selectivity in the inner ear is fundamental to hearing and is traditionally thought to be similar across mammals. Although direct measurements are not possible in humans, estimates of frequency tuning based on noninvasive recordings of sound evoked from the cochlea (otoacoustic emissions) have suggested substantially sharper tuning in humans but remain controversial. We report measurements of frequency tuning in macaque monkeys, OldWorld primates phylogenetically closer to humans than the laboratory animals often taken as models of human hearing (e.g., cats, guinea pigs, chinchillas). We find that measurements of tuning obtained directly from individual auditory-nerve fibers and indirectly using otoacoustic emissions both indicate that at characteristic frequencies above about 500 Hz, peripheral frequency selectivity in macaques is significantly sharper than in these common laboratory animals, matching that inferred for humans above 4-5 kHz. Compared with the macaque, the human otoacoustic estimates thus appear neither prohibitively sharp nor exceptional. Our results validate the use of otoacoustic emissions for noninvasive measurement of cochlear tuning and corroborate the finding of sharp tuning in humans. The results have important implications for understanding the mechanical and neural coding of sound in the human cochlea, and thus for developing strategies to compensate for the degradation of tuning in the hearing-impaired.auditory filters | comparative hearing S ound waveforms consist of pressure fluctuations in time and space. In the process of transducing mechanical vibrations into neural signals, the cochlea performs a mechanical frequency analysis that decomposes sounds into constituent frequencies (1, 2). The frequency tuning of the cochlear filters plays a critical role in the ability to distinguish and segregate different sounds perceptually. For example, sounds that radiate from different sources superpose in the air, and are thus "mixed up" before striking the eardrums. Based on the output of the cochlear filters, and by comparing responses from the two ears, the nervous system is capable of disentangling the various sounds, grouping related frequency components to identify auditory objects and localize their sources in space (3). The critical role of peripheral frequency selectivity is perhaps best illustrated by the consequences of damage to the inner ear, which typically leads to a degradation of the cochlear filters. The loss of sharp filtering results in an impaired ability to detect signals in noise and to separate different sounds (4). Frequency selectivity is therefore crucial to everyday human communication.The study of the cochlea is hampered by its fragility and inaccessibility. Direct measurements of mechanical or neural frequency tuning in healthy cochleae are only possible in laboratory animals. To date, measurements of the mechanical vibration of the cochlea's basilar membrane have been largely restricted to the basal high-frequency end of the cochlea, where surgical acce...

Distortion-product otoacoustic emission reflection-component delays and cochlear tuning: Estimates from across the human lifespan

“…The tuning ratio we employed [see Fig. 5(B), inset] represents an average of tuning ratios derived from SFOAE and AN measurements in cat, guinea pig, and chinchilla (Joris et al, 2011). By using the tuning ratio derived from laboratory animals, we assume that r varies relatively little across mammalian species, consistent with previous results .…”

“…5(B) (inset) and a transition frequency CF a|b of 1 kHz, as estimated from the location of the bend in the N R trend. The tuning ratio we employed represents an average derived from SFOAE and auditory-nerve measurements in cat, guinea pig, and chinchilla (Joris et al, 2011). By applying the same tuning ratio for each age group, we implicitly assume that the tuning ratio does not vary systematically with age.…”

“…Consistent relationships between OAE delays and cochlear frequency tuning have been demonstrated in several species (Shera et al, 2002Bergevin and Shera, 2010;Joris et al, 2011). 1 The logic underlying these relationships builds on the observation that cochlear delay and frequency tuning are linked through filter theory, which holds that sharper tuning requires longer delays (e.g., Shera and Guinan, 2003).…”

Measuring stimulus-frequency otoacoustic emissions using swept tones

“…For similar reasons, SFOAEs are also well suited for examining the function of the olivocochlear efferent system (reviewed in Guinan, 2006). In addition, recent theory and empirical evidence suggest that SFOAE delays provide valuable information about cochlear frequency selectivity (e.g., Shera and Guinan, 2003;Shera et al, 2002;Schairer et al, 2006;Shera et al, 2010;Bergevin et al, 2010;Bentsen et al, 2011;Joris et al, 2011). Finally, ongoing efforts to test theoretical models of the cochlea using SFOAEs have provoked years of fruitful debate and refined both theories of OAE generation and our basic understanding of cochlear mechanics.…”

Human neural tuning estimated from compound action potentials in normal hearing human volunteers

“…Comparison of estimated sharpness of neural tuning in human (solid line: mean trend, shaded gray area: range using different conversion functions) with that of single AN fibers in common lab animals (hatched area: outline of different animals; cat data: archival data from our lab., remaining trend data from [14]), macaque monkey (dashed dotted, from [8]) and with that of other indirect measures of human frequency tuning (dotted line: SFOAE from [15]; dashed line: psychoacoustics from [9]; converted from QERB with factor 0.52). 070001-4…”