The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach

Abstract

The bony labyrinth in the temporal bone houses the sensory systems of balance and hearing. While the overall structure of the semicircular canals and cochlea is similar across therian mammals, their detailed morphology varies even among closely related groups. As such, the shape of the labyrinth carries valuable functional and phylogenetic information. Here we introduce a new, semilandmark-based three-dimensional geometric morphometric approach to shape analysis of the labyrinth, as a major improvement upon previous metric studies based on linear measurements and angles. We first provide a detailed, step-by-step description of the measurement protocol. Subsequently, we test our approach using a geographically diverse sample of 50 recent modern humans and 30 chimpanzee specimens belonging to Pan troglodytes troglodytes and P. t. verus. Our measurement protocol can be applied to CT scans of different spatial resolutions because it primarily quantifies the midline skeleton of the bony labyrinth. Accurately locating the lumen centre of the semicircular canals and the cochlea is not affected by the partial volume and thresholding effects that can make the comparison of the outer border problematic. After virtually extracting the bony labyrinth from CT scans of the temporal bone, we computed its midline skeleton by thinning the encased volume. On the resulting medial axes of the semicircular canals and cochlea we placed a sequence of semilandmarks. After Procrustes superimposition, the shape coordinates were analysed using multivariate statistics. We found statistically significant shape differences between humans and chimpanzees which corroborate previous analyses of the labyrinth based on traditional measurements. As the geometric relationship among the semilandmark coordinates was preserved throughout the analysis, we were able to quantify and visualize even small-scale shape differences. Notably, our approach made it possible to detect and visualize subtle, yet statistically significant (P = 0.009), differences between two chimpanzee subspecies in the shape of their semicircular canals. The ability to discriminate labyrinth shape at the subspecies level demonstrates that the approach presented here has great potential in future taxonomic studies of fossil specimens.

Evolution of locomotion in Anthropoidea: the semicircular canal evidence

“…Beyond recovering new fossils, our understanding of anthropoid locomotor evolution during the Caenozoic will also benefit from further analyses of the canal system, including the introduction of more sophisticated morphometric methods [77,78]. Such an approach will allow for an integrated assessment of functionally relevant aspects, including planar orientation of the canals, which, like arc size, is now known to affect their sensitivity, and may correlate well with locomotor repertoire [8,79,80].…”

Automated analysis of human cochlea shape variability from segmented μ CT images

“…The challenge of cochlear centerline extraction has already been dealt with (Baker and Barnes, 2004;Verbist et al, 2009;Poznyakovskiy et al, 2011;Gunz et al, 2012). A flowchart of the method applied in this study and the results are respectively given on Fig.…”

“…Previous analyses include measurements of the length of the cochlea and the number of cochlear turns (Hardy, 1938;Kawano et al, 1996;Skinner et al, 2002;Escudé et al, 2006;Stakhovskaya et al, 2007;Erixon et al, 2009;Gunz et al, 2012;Shin et al, 2013;van der Marel et al, 2014), measurements of the heights, widths and sectional areas of the scala tympani (Zrunek et al, 1980;Zrunek and Lischka, 1981;Hatsushika et al, 1990;Gulya and Steenerson, 1996;Wysocki, 1999;Thorne et al, 1999;Biedron et al, 2010;Avci et al, 2014), the scala vestibuli (Zrunek and Lischka, 1981;Gulya and Steenerson, 1996;Wysocki, 1999;Thorne et al, 1999;Biedron et al, 2010) and the cochlea (Erixon et al, 2009;Shin et al, 2013), measurements of the radial component of the cochlear centerlines (also called cochlear curvature) (Cohen et al, 1996;Baker, 2008;van der Marel et al, 2014), and studies of the longitudinal component of the centerlines of the scala tympani (Avci et al, 2014) and the cochlea itself (Verbist et al, 2009).…”

“…As important cochlear anatomical structures such as the basilar membrane are not visible in CT imaging, analyses of the cochlea are commonly performed using µCT images (Verbist et al, 2009;Poznyakovskiy et al, 2011;Gunz et al, 2012;Shin et al, 2013;Avci et al, 2014;Ceresa et al, 2014). In order to improve contrast, temporal bone samples can be fixed and stained before imaging (Poznyakovskiy et al, 2011).…”

The labyrinthine morphology of Pronycticebus gaudryi (Primates, Adapiformes)

“…The choice of the threshold value could affect to some extent the reconstruction of the semicircular canals and of the cochlea (Coleman and Colbert 2007). Fortunately, thresholding effects do not affect the location of the lumen centre of the semicircular canals and the cochlea (Gunz et al 2012;Lebrun et al 2010). As such, labyrinthine shape was quantified with 22 landmarks, located at the centres of the lumina of the semicircular canals, of the ampullae, and of the cochlear helix (see Supporting Information Figure S1), following the protocol of Lebrun et al (2010).…”