Unraveling the labyrinth of our balance system: Visualizing bony otolith organ structure through novel 3D modeling

Abstract

The organs of balance, the semicircular canals (SCCs) and otolith organs (utricle and saccule) of the inner ear labyrinth, are essential to basic human movement and function. While the SCCs (both external and internal structure) are well visualized and understood, the seemingly vague bony structure of the utricle and saccule remains largely unexplored. Consequently, relationships between this bony structure and the internal otolith organs themselves remain unknown. As a result, a comprehensive understanding of the morphology of our balance organs and relationships to function has eluded us.As a first step to understand the relationships of the utricle and saccule (that is the membranous otolith organs responsible for detecting linear motion) to their external bony coverings, we have developed a morphometrically‐based modelling system to visualize bony otolith organ structure. The indeterminate shape of this capsule has precluded a standard metric approach to capture such relationships. Our method combines osmium tetroxide contrast enhanced micro‐computed tomography (μCT) imaging of human temporal bones (n=13), digital visualizations, and landmark‐based 3D shape analyses of bony and membranous structure. This was done in order to: 1) test the hypothesis that the bony form surrounding the otolith organs covaries with internal membranous anatomy (including the utricle and saccule); and 2) pinpoint specific arrangements of landmarks on the bone that best reflect the internal structure of the utricle and saccule. This approach allows us to extract the bony otolith organ structure from an otherwise nebulous bony form.Tests of integration on 3D shape data between bony and membranous tissue demonstrate a significant association between the hard and soft tissues of the otolith organs (p<0.05). Relative orientation of the otolith organs also significantly correlates with surrounding bony structure (p<0.005). These data support our initial hypothesis and inform the creation of our 3D visualization of human otolith organ structure, establishing the configuration of the otolith organs to bony structure of the labyrinth. Furthermore, this model enhances our understanding of spatial relationships between the otolith organs and cranial structure and provides the foundation to assess the evolution of a prime sensory system essential for providing a gravitational frame of reference for all vertebrate life.