The influence of cochlear shape on low-frequency hearing

Abstract

The conventional theory about the snail shell shape of the mammalian cochlea is that it evolved essentially and perhaps solely to conserve space inside the skull. Recently, a theory proposed that the spiral's graded curvature enhances the cochlea's mechanical response to low frequencies. This article provides a multispecies analysis of cochlear shape to test this theory and demonstrates that the ratio of the radii of curvature from the outermost and innermost turns of the cochlear spiral is a significant cochlear feature that correlates strongly with low-frequency hearing limits. The ratio, which is a measure of curvature gradient, is a reflection of the ability of cochlear curvature to focus acoustic energy at the outer wall of the cochlear canal as the wave propagates toward the apex of the cochlea.inner ear ͉ function ͉ mammalian evolution ͉ spiral I t is often thought that mammalian cochleae are coiled to pack a longer organ into a small space inside the skull and that the cochlear coil increases the efficiency of blood and nerve supply through a central shaft (1). Although these spatial advantages of a coiled cochlea have been generally accepted, understanding the effect of shape on hearing itself has been a challenge.Cochlear coiling is absent in reptiles, birds, and monotreme mammals, and it appears to have originated in the marsupial and placental mammal lines (2). Coiling allowed the cochlea to become longer, increasing the potential octave range, whereas uncoiled cochleae have been associated with relatively limited hearing ranges. Earlier studies suggested that the evolution of coiling enhanced high-frequency hearing (3). This suggestion, however, is not wholly satisfactory for several reasons. Above all, increased hearing ranges extended both high-frequency and low-frequency (LF) hearing abilities in mammals compared with birds and reptiles and improved sensitivities compared with even LF specialist fishes (4). Further, the highest-frequency waves are resolved near the base (entrance) before they propagate far enough into the spiral to ''feel'' the cochlear curvature; it is the lowest-frequency waves that propagate along the cochlea's coils.Earlier work on land mammal ear anatomy (5) found a strong correlation between the LF hearing limit of each species and the product of basilar membrane length and number of spiral turns, but did not adduce a mechanistic explanation for this relationship. Other data suggested also that longitudinal curvature of the cochlear duct generates radial fluid pressure gradients (6) and enhances radial movement of hair cells (1, 7).Recently, a new theory proposed that the cochlea's graded curvature actually enhances LF hearing (8), similar to a whispering gallery in which sounds cling to the concave surface of the lateral wall (9). The cochlear spiral shape redistributes wave energy toward the outer wall, particularly along its innermost, tightest, apical turn, and thereby enhances sensitivity to lowerfrequency sounds.In this article, we test this theory morphometrically. W...

Fossil evidence on evolution of inner ear cochlea in Jurassic mammals

“…Elongation of the cochlea with more spiral turns is correlated with increased resolution of sound frequencies [2,8]. The curved gradient of the coiled cochlear canal wall focuses acoustic energy towards the apex of the cochlea, the most sensitive region for the low-frequency sound [9]. The key innovation in the fully coiled cochlea, including its auditory innervation, is correlated with the earliest diversification of metatherians and eutherians in the Cretaceous, and has led to many spectacular functional adaptations in hearing in Cenozoic and living marsupials and placentals [3,5,10 -16].…”

Deep evolutionary roots of strepsirrhine primate labyrinthine morphology

“…Differences in cochlear coiling and in the relative size of the semicircular canals are correlated with differences in auditory capacities (Steele & Zais, 1985;West, 1985) and locomotor behaviour (Matano et al 1985(Matano et al , 1986Spoor et al 1994;Spoor & Zonneveld, 1998), respectively. Specifically, a narrow apical relative to the basal turn of the cochlea is correlated with an extended lowfrequency hearing limit (Manoussaki et al 2008), and relatively large semicircular canals are correlated with fast, jerky styles of locomotion (Spoor et al 2002(Spoor et al , 2007. Because the labyrinth is contained in the densely ossified petrous bone it is often integrally preserved in fossil specimens, which allows inferences on locomotion (Spoor et al 1994(Spoor et al , 2007Spoor & Zonneveld, 1998;Walker et al 2008;Silcox et al 2009) and also on hearing in extinct species (Rosowski & Graybeal, 1991;Ketten, 1992;Meng & Fox, 1995;Fox & Meng, 1997;Manoussaki et al 2008).…”

“…Specifically, a narrow apical relative to the basal turn of the cochlea is correlated with an extended lowfrequency hearing limit (Manoussaki et al 2008), and relatively large semicircular canals are correlated with fast, jerky styles of locomotion (Spoor et al 2002(Spoor et al , 2007. Because the labyrinth is contained in the densely ossified petrous bone it is often integrally preserved in fossil specimens, which allows inferences on locomotion (Spoor et al 1994(Spoor et al , 2007Spoor & Zonneveld, 1998;Walker et al 2008;Silcox et al 2009) and also on hearing in extinct species (Rosowski & Graybeal, 1991;Ketten, 1992;Meng & Fox, 1995;Fox & Meng, 1997;Manoussaki et al 2008). While the functional significance of the primate labyrinth has been investigated in great detail, still relatively little is known about its phylogenetic significance (Spoor, 1993;Hublin et al 1996;Spoor et al 2003).…”

Hydro-Elastic Waves in a Cochlear Model: Numerical Simulations and an Analytically Reduced Model

“…We first assume that the cochlea can be unwound without dramatically affecting its function. It is known that the spiral shape does affect cochlear function at low frequencies [11], however this is more a tuning effect than a dramatic functional effect. We further assume that the fluid effects of the two larger cavities (scala vestibula, scala tympani) dominate those of the third smaller cavity which we neglect.…”