Three-dimensional tonotopic mapping of the human cochlea based on synchrotron radiation phase-contrast imaging

Hao Li,Sumit Agrawal,Hanif M Ladak,Ning Zhu,Luke Helpard,Seyed Alireza Rohani,Jonas Ekeroot,Helge Rask-Andersen

doi:10.1038/s41598-021-83225-w

Abstract

The human cochlea transforms sound waves into electrical signals in the acoustic nerve fibers with high acuity. This transformation occurs via vibrating anisotropic membranes (basilar and tectorial membranes) and frequency-specific hair cell receptors. Frequency-positions can be mapped within the cochlea to create a tonotopic chart which fits an almost-exponential function with lowest frequencies positioned apically and highest frequencies positioned at the cochlear base (Bekesy 1960, Greenwood 1961). To date, models of frequency positions have been based on a two-dimensional analysis with inaccurate representations of the cochlear hook region. In the present study, the first three-dimensional frequency analysis of the cochlea using dendritic mapping to obtain accurate tonotopic maps of the human basilar membrane/organ of Corti and the spiral ganglion was performed. A novel imaging technique, synchrotron radiation phase-contrast imaging, was used and a spiral ganglion frequency function was estimated by nonlinear least squares fitting a Greenwood-like function (F = A (10ax − K)) to the data. The three-dimensional tonotopic data presented herein has large implications for validating electrode position and creating customized frequency maps for cochlear implant recipients.

Highlights

The human cochlea transforms sound waves into electrical signals in the acoustic nerve fibers with high acuity
Synchrotron radiation was used by Vogel, the absorption-based contrast did not provide adequate soft tissue discernment in structures such as the basilar membrane (BM)
The ability to discern structures with staining was a significant improvement, the round window (RW) and OW were opened during sample preparation, and artefacts have been reported to arise from the staining of soft tissues[6,21]

Summary

Introduction

The human cochlea transforms sound waves into electrical signals in the acoustic nerve fibers with high acuity This transformation occurs via vibrating anisotropic membranes (basilar and tectorial membranes) and frequency-specific hair cell receptors. The delicate tissue and sensory cells responsible for this mechanoelectrical transduction in the inner ear are at a high risk of damage, which can lead to sensorineural hearing loss. Stakhovskaya et al.[8] published histologically-derived SG tonotopy measurements, which have become the most widely accepted and utilized information for SG frequency mapping This previous work was based on two-dimensional histological sections and has not been validated in three-dimensions. The first detailed three-dimensional (3D) measurements of the BM and SG are presented using synchrotron radiation phase-contrast imaging (SR-PCI) This imaging technique has the advantage of simultaneous bone and soft tissue visualization without the need for sectioning and staining[9]. The objective of the present work is to use manual dendrite tracing in SR-PCI data to determine accurate 3D tonotopic coordinates of the human SG

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Conclusion