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

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 (10^ax - 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.

Figure 1

(A) SR-PCI data of a left human cochlea. 3D Slicer (www.slicer.org, version 4.10.1) was used to create a detailed 3D representation including intra-cochlear soft tissue. The basilar membrane and spiral ganglion were segmented, and the frequency coordinates were calculated using Greenwood’s formula and dendrite tracing. (B,C) For the spiral ganglion, the dendrites were traced from the basilar membrane to make a corresponding frequency map (shown with color scale). Note the angle of dendritic connections are not radial to the mid-modiolar axis in the apical and basal region (denoted by *). (D) Representative tomographic X-ray section showing the segmented round window (red), neural elements (yellow) and basilar membrane (green). GIMP 2 (www.gimp.org) was used to create the figures.

Figure 2

(A) Segmentations of soft tissues from ten cochleae shown in orthographic 3D view. 3D Slicer (www.slicer.org, version 4.10.1) was used to create the 3D representations. Frequency maps of the basilar membrane were developed according to Greenwood. Corresponding dendrites were traced to the spiral ganglion and corresponding octave bands are outlined. Scale bar is 2.5 mm. (B) Average rotational angles for tonotopic frequencies of the BM and SG. Angular rotations are calculated from the mid-point of the round window. Ranges in position of angular rotations are shown with blue arrows. (C) Average length of BM and SG presented against frequency for all cochleae. Values within the color bars represent the mean distance to reach each tonotopic frequency, with values along the top and bottom of the color bars representing the maximum and minimum distances to reach each frequency, respectively.

Figure 3

(A) Basilar membrane length is plotted against diameter A. No correlation was noted between these values (r = 0.18). (B) Table showing mean angular frequencies obtained from ten specimens imaged using synchrotron radiation phase-contrast imaging. (C) Average basilar membrane and spiral ganglion frequencies plotted against cochlear angular depth. This average curve was determined by calculating the mean angular depth of each frequency in all samples. (D) Results of least squares fitting an exponential function to 3D SR-PCI SG tonotopic data. Greenwood’s function for the BM tonotopic distribution is illustrated in green for reference, and the SG function relating proportional length to tonotopic frequency developed herein is illustrated in orange.