E. Christopher Kirk and Ashley D. Gosselin-Ildari
The Anatomical Record
Volume 292, Issue 6, pages 765–776, June 2009
The primate cochlea is a membranous, fluid-filled receptor organ that is specialized for sound detection. Like other parts of the inner ear, the cochlea is contained within the bony labyrinth of the petrous temporal bone. The close anatomical relationship between the bony cochlear labyrinth and the membranous cochlea provides an opportunity to quantify cochlear size using osteological specimens. Although mechanisms of cochlear frequency analysis are well studied, relatively little is known about the functional consequences of interspecific variation in cochlear size. Previous comparative analyses have linked increases in basilar membrane length to decreases in both the high and low frequency limits of hearing in mammals. However, these analyses did not consider the potentially confounding effects of body mass or phylogeny. Here, we present measurements of cochlear labyrinth volume in 33 primate species based on high-resolution computed tomography. These data demonstrate that cochlear labyrinth volume is strongly negatively allometric with respect to body mass. Scaling of cochlear volume in primates is very similar to scaling of basilar membrane length among mammals generally. Furthermore, an analysis of 10 primate taxa with published audiograms reveals that cochlear labyrinth volume is significantly negatively correlated with the high frequency limit of hearing. This result is independent of body mass and phylogeny, suggesting that cochlear size is functionally related to the range of audible frequencies in primates. Although the nature of this functional relationship remains speculative, our findings suggest that some hearing parameters of extinct taxa may be estimated using fossil petrosals.
From the body of the paper:
Use of the cochlear labyrinth to make inferences about mammalian hearing abilities is based on the observation that the gross dimensions of the cochlea and its constituent tissues are correlated with the range of frequencies that can be detected by a species (West, 1985; Echteler et al., 1994). West (1985) demonstrated that the length of the basilar membrane is significantly negatively correlated with both the high and low frequency limits of hearing. In other words, as basilar membrane length increases in mammals, the range of audible frequencies shifts downward into relatively lower frequencies. As a result, mammals with absolutely long basilar membranes tend to have comparatively good low-frequency hearing, while mammals with absolutely short basilar membranes have comparatively good high-frequency hearing. Elephants, for example, have a basilar membrane length of about 60 mm and a range of audible frequencies between 0.18 and 10.5 kHz (West, 1985). By contrast, the house mouse has a basilar membrane length of only 7 mm, and a range of audible frequencies between 2.7 and 79 kHz (West, 1985).
Similar correlations between basilar membrane length and hearing thresholds were reported by Echteler et al. (1994) for mammals with “unspecialized” cochleas. However, these authors also demonstrated that species with substantially nonlinear cochlear frequency-place maps (“hearing specialists”) do not conform to this general mammalian trend (Echteler et al., 1994). From a practical standpoint, these results suggest that the dimensions of the cochlea may be used to estimate the high and low frequency limits of hearing for most mammals (West, 1985; Echteler et al., 1994). By contrast, the hearing abilities of taxa with acoustic foveae (e.g., dolphins and horseshoe bats) and/or substantial discontinuities in basilar membrane dimensions (e.g., mole rats) are more difficult to predict (Echteler et al., 1994). According to the criteria of Echteler et al. (1994), primates may be considered “hearing generalists”. None are known to possess acoustic foveae, none are specialized for echolocation or seismic hearing, and all species that have been studied exhibit typical cochlear frequency-place maps that lack plateaus or discontinuities (Greenwood, 1990). As a result, it is theoretically possible to derive predictions about the hearing abilities of primates based on the anatomy of the cochlea and cochlear labyrinth. Specifically, the findings of West (1985) and Echteler et al. (1994) suggest that increases in the length of the basilar membrane and resulting increases in the size of the cochlea should be correlated with a downward shift in the range of audible frequencies.
Table 1: Cochlear labyrinth volumes in primates
The results of this analysis provide further support for the conclusion that the dimensions of the cochlea influence hearing abilities in mammals. Previous research has shown that basilar membrane length is correlated with both the high and low frequency limits of hearing in mammals with unspecialized cochleas (West, 1985; Echteler et al., 1994). The present analysis demonstrates that cochlear size in primates (as estimated by the volume of the cochlear labyrinth) scales with body mass in a manner very similar to the scaling of basilar membrane length among mammals generally. In the comparative samples used here (Tables 1 and 2), cochlear labyrinth volume and basilar membrane length are each positively correlated with body mass (r = 0.894 and 0.939, respectively). Furthermore, both cochlear variables scale with strong negative allometry relative to body mass. Although cochlear labyrinth volume in primates demonstrates slightly greater negative allometry (RMA slope = 0.36) than basilar membrane length in mammals (RMA slope = 0.44) (Figs. 3 and 4), the RMA regression slope confidence intervals for both variables overlap. These similar scaling relationships support the expectation that cochlear size and basilar membrane length are closely linked. Indeed, it seems reasonable to expect that if selection acts to increase or decrease the length of the basilar membrane, then there should be correlated changes in cochlear volume. While caution in interpreting our data is warranted given the fact that the comparative samples for cochlear labyrinth volume (Table 1; primates) and basilar membrane length (Table 2; mammals generally) include different taxa, these results are consistent with the hypothesis that both cochlear variables should have a similar relationship with hearing abilities.
These expectations are largely borne out by our analysis of the relationship between cochlear labyrinth volume and hearing abilities in primate species with published audiograms (Heffner, 2004). Although cochlear labyrinth volume is not significantly correlated with either the best frequency of hearing (=frequency with lowest absolute detection threshold) or the total hearing range (= range of audible frequencies at 60 dB SPL), cochlear labyrinth volume is significantly negatively correlated with both the high and low frequency limits of hearing (Figs. 5a and 6a). In other words, as cochlear size increases, the range of audible frequencies shifts downward. These results are robust: even with the relatively small samples considered here, cochlear labyrinth volume alone can explain 61% of the variation in high frequency limit and 63% of the variation in low frequency limit. In this respect, our findings for cochlear size in primates closely match the results reported by West (1985) and Echteler et al. (1994) for basilar membrane length in a comparative sample of 9 mammalian species.
One potential criticism of the analyses presented by West (1985) and Echteler et al. (1994) is that both failed to address the influence of body mass and phylogeny. Indeed, it has been known for decades that high frequency limit is correlated with head and body size (Masterton et al., 1969; Heffner and Heffner, 1992, Heffner, 2004). This correlation has typically been explained as a result of selection for efficient sound localization at different head sizes. According to Heffner:
"Mammals with small heads (or, more precisely, short travel times for sound as it travels from one ear to the other) hear higher frequencies than mammals with large heads. The explanation for this relationship does not lie in the physical scaling of the auditory bulla and cochlea, with smaller middle and inner ears being associated with better high frequency hearing and larger ears being associated with better low-frequency hearing… In the case of high-frequency hearing, the explanation for the close correlation with head size… is that being able to detect high frequencies allows mammals to localize sound using pinna cues and spectral differences between the ears." (p. 1115; Heffner, 2004)
If this scenario is correct, then the size of the cochlea and length of the basilar membrane have no functional relationship with high frequency limit per se. In this case, the significant negative correlations between cochlear size variables (Table 1; West, 1985; Echteler et al., 1994) and high frequency limit would be the spurious byproduct of independent correlations between cochlear size, high frequency limit, and head/body size. The results of the present analysis, however, do not support this conclusion. While cochlear labyrinth volume and high frequency limit are both significantly correlated with body mass (Figs. 3 and 5b), the correlation between high frequency limit and cochlear volume (r = −0.78; P = 0.0074; Fig. 5a) is stronger than the correlation between high frequency limit and body mass (r = −0.68; P = 0.0321). Furthermore, the relationship between cochlear labyrinth volume and high frequency limit remains significant when independent contrasts are used to minimize the influence of phylogenetic effects. By comparison, independent contrasts of body mass and high frequency limit are not significantly correlated. More importantly, when a partial correlation analysis is used to hold the effects of body mass constant, cochlear labyrinth volume remains significantly correlated with high frequency limit (Fig. 7a). These results indicate not only that high frequency limit decreases with increasing absolute cochlear size, but that species with relatively large cochleas for their body size also have relatively low high frequency limits. In other words, at a given body size, species with smaller cochleas tend to have better high frequency hearing than species with larger cochleas.
The case for a functional relationship between cochlear size and low frequency limit is less convincing than that for high frequency limit. Although cochlear labyrinth volume is significantly negatively correlated with low frequency limit (r = −0.79; P = 0.0186), the correlation between body mass and low frequency limit is stronger (r = −0.84; P = 0.0089) (Fig. 6a,b). Furthermore, when a partial correlation analysis is used to hold body mass constant, cochlear labyrinth volume is no longer significantly correlated with low frequency limit (Fig. 7b).
These differences in the results for high frequency limit and low frequency limit beg the question of precisely how cochlear size might influence hearing abilities in mammals. Passive frequency analysis in the cochlea is generally attributed to the existence of a resonance gradient along the length of the basilar membrane, with the basal region of the basilar membrane having a higher resonant frequency than more apical regions (Echteler et al., 1994; Purves et al., 2008). This resonance gradient is thought to be largely dependent on variation in the mass and stiffness of the basilar membrane, leaving the mechanical significance of variation in basilar membrane length or the absolute size of the cochlea unclear. Although it is tempting to speculate that the mass of the cochlear fluids might also have a resonant effect on cochlear tuning, a great many factors influence cochlear mechanics (Dallos et al., 1996; Gummer, 2003) and a discussion of their potential relationship to cochlear size is well beyond the scope of the present analysis. Accordingly, while our data show a robust negative correlation between cochlear volume and high frequency limit in primates that is independent of body mass and phylogeny, the precise mechanism (or mechanisms) responsible for this relationship remains unknown.
It is also not immediately evident how interspecific variation in the high and low frequency limits of hearing influence primate ecology. Although the demands of sound localization are doubtless important (Masterton et al., 1969; Heffner and Heffner, 1992, Heffner, 2004), variation in habitat acoustics, diet, predation, and intraspecific communication may also exert a selective influence on hearing abilities (Morton, 1975; Waser and Brown, 1986; Zimmerman et al., 1995; de al Torre and Snowdon, 2002; Brumm and Slabbekoorn, 2005). Although these ecological relationships remain to be elucidated, the results of the present analysis suggest that the evolution of primate hearing abilities can be studied through an examination of the bony cochlear labyrinth. Cochlear labyrinth volume, in particular, can be used to estimate the high frequency limit of hearing. Similarly, Coleman and Boyer (2008) have recently reported that the length of the cochlea  can be used to estimate low frequency sensitivity in euarchontans. These analyses hold out the possibility that some parameters of the audiogram can be reconstructed for fossil species with suitably preserved bony labyrinths. Ultimately, such conclusions may be linked to differences in auditory ecology, as with divergent cochlear specializations for echolocation in odontocetes and low frequency communication in mysticetes (Fleischer, 1976; Ketten, 1992; Luo and Eastman, 1995; Geisler and Luo, 1996; Luo and Marsh, 1996).