Introduction
The osseous spiral lamina (OSL) is a bony structure inside the cochlea that projects from the modiolus from base to apex, separating the cochlear canal into the scala vestibuli and the scala tympani. Despite being described as early as 1851 [
1], misconceptions regarding its anatomy [
2‐
4] and mechanical behavior are only now being corrected. The advent of technologies such as scanning electron microscopy combined with 3D reconstructions has improved the understanding and visualization of inner ear anatomy. Additionally, recent findings suggesting a cribriform structure of the OSL plates gave rise to the hypothesis that its mobility may influence air and bone conductive hearing [
5‐
7]. As anatomically revealing as scanning electron microscopy is, the need for tissue preparation, potential for introduction of artifacts, and typical anisotropic resolution (0.5 × 0.5 × 100 µm) make this technique suboptimal for cochlear investigation.
To overcome these limitations, non-destructive imaging modalities based on computed tomography and magnetic resonance are well-established to meet the varying levels of resolution required for pre-clinical and clinical applications. For instance, clinical computed tomography is available with an isotropic resolution of 500 µm or less and magnetic resonance of 300 µm at 7 Tesla. For pre-clinical purposes, these same imaging modalities usually provide isotropic resolution typically at levels of 10 to 100 µm [
8‐
10]. Laboratory-based micro-computed tomography (microCT) is an imaging technique that is increasingly applied for research in biomedical and life sciences. MicroCT was introduced to complement histological evaluations, as a non-destructive, three-dimensional imaging technique at a microscopical level. At the same time, high-intensity synchrotron radiation has enabled better visualization and contrast of the soft structures inside the cochlea [
11]. Unfortunately, most microCT studies either use animal models or are restricted to the oval and round windows [
11,
12]. Meanwhile, other anatomical structures of cochlea remain subdued [
13,
14]. Given the bony morphology of the OSL microCT is therefore well-suited for generating images up to single-digit micron resolutions enabling detailed 3D reconstructions to be created for the first time.
Although inconsistent with the classical concept of a rigid OSL, this structure was described as porous in early anatomical studies, but not visually demonstrated [
1‐
4,
15,
16]. The radial length and porosity can explain the observed movement of the OSL in response to sounds in human cadaveric temporal bones, as described by Raufer et al. [
5]. Even though its function remains undetermined, it is known that the OSL can have an impact on sound response and the motion of the cochlear partition (CP) [
6,
17]. The higher repercussion relies on bone-conducted sound stimulation. The compression and expansion vibrations of the otic capsule create a vibrational response on the basilar membrane [
18], and no difference between air conduction and bone conduction mechanisms was found in experiments using cadaveric fresh-frozen human temporal bones [
7]. Bone conduction sound transmission is considered to be based on inertial effects [
19,
20]. In this context, the inertial vibration of the OSL may have a partial impact on the overall response of basilar membrane vibrations to sound, especially at high frequencies [
7]. All these previous theoretical descriptions corroborate the idea of a flexible OSL. However, the current models of the cochlea assume that the OSL is rigid. The findings presented in this study can be utilized to integrate a flexible OSL into future cochlear models. Moreover, to the best of our knowledge, there has so far been no detailed visualization of its morphological characteristics.
The aim of this pilot study is to present a detailed 3D reconstruction of the osseous spiral lamina, which has not been previously studied in such depth. By gaining a better understanding of the OSL, we can further advance our knowledge of the mechanisms of hearing and increase the reliability and efficiency of cochlear models.
For this purpose, we measured the width and thickness of the human OSL by microCT using increasing nominal resolutions (14.0-, 13.0-, 4.5-, 2.5-µm voxel size).
Additionally, a porosity distribution study of the individual plates at the basal and middle turns and the apex was conducted. Furthermore, the 3D reconstruction allowed the bony pillars (BP) that lie between the OSL plates to be observed in great detail.
Discussion
The cochlea is a small, spiral bone structure in the inner ear that plays a critical role in hearing. It contains three types of bones: (1) the petrous portion of the temporal bone, which is the trabecular bone that houses the cochlea; (2) the modiolus, which is the central conical axis of trabecular bone; and (3) the osseous spiral lamina (OSL), which is a thin layer of bone composed of two plates of compact bone that protrudes from the modiolus and separates part of the two fluid-filled canals that run through the cochlea, the scala vestibuli, and the scala tympani, which, like the canals, makes two and three-quarter turns around the modiolus [
23,
24].
The bony structures of the inner ear were superficially described in early anatomical studies, but imaging demonstration has only been possible more recently [
1,
2,
16]. Anatomical descriptions of the bony inner ear are usually restricted to the modiolus [
16,
25] and use histopathological techniques. Although histopathology remains the gold standard for cytological evaluation, the specimen preparation process involves the physical destruction of the specimen and creates typical anisotropic resolution (0.5 × 0.5 × 100 µm) if translated into 3D [
26‐
28].
Surrounded by the dense cochlear bone, under around 2.5-µm resolution microCT, a trabecular looking modiolus stands in the middle of the cochlea, projecting itself to form the two bony plates that determine the shape of the OSL. Although the OSL consists of two plates of compact bone, the porous nature of these plates and the presence of numerous bony pillars make it more similar as a whole to a trabecular bone. In fact, trabecular bone is by definition a hierarchical, spongy, and porous lattice structure that provides the framework for the soft, highly cellular bone marrow filling the intertrabecular spaces. At a microstructural scale, trabecular bone architecture is organized to optimize load transfer [
29]. Similarly, the OSL system as a whole can be thought of as trabecular bone, with two individual plates connected by bony pillars on the inside and the habenular openings at its end. The OSL plates have a lace-like appearance enfolding the fibers that will later form the cochlear nerve. The radial middle portion of the basal turn of the OSL (both plates) has a more porous appearance than its edges, similarly to Raufer’s description [
6]. This surface reduction is congruent with the sparse distribution of the bony pillars in the middle of the OSL. Although habenular openings were described by Küçük et al. [
15] as tunnels, internal inspection of the structure indicates that the openings do not behave like tunnels. On the contrary, they convey the impression of a cave and appear to have a structural support function, joining the plates together on the lateral end, at the insertion point of the bridge and limbus regions. The bony pillars could have a similar support function, keeping the plates together while providing stability that can have a potentially significant influence on the spread of excitation during its vibration. However, more investigation on this possibility is needed.
The lace-like appearance of the OSL plates turns out to be a common characteristic, and it was observed in the measured specimens. Porosity analysis demonstrated a considerable higher percentage of pores on both vestibular plate VP and tympanic plate TP on the basal turn if compared to previous study [
6]. Unlike the work of Raufer et al. [
6], which was limited to considering different portions of the basal turn and suprabasal turn (between 1 and 12 mm of longitudinal distance from the base), in this study, we also calculated porosity relative to the middle turn and the apex. In these cases, we found a constant presence of porosity in both TP (mid, 61%; apex, 56%) and VP (mid, 50%; apex, 61%). Moreover, while the TP appears to be more porous than VP in the basal and middle turns, although this difference is less pronounced than in previous descriptions [
6], in the apex, we find more porosity in VP than in TP (61% vs. 56%). With regard to our study results, we believe that the volumetric reconstructions used in our measurements provide a more realistic depiction of the OSL anatomy. Since 3D investigation provides more information than conventional 2D studies, this technique seems to be more suitable for demonstrating the porosity of the structure. The difference in methodology can also be responsible of the main differences found in the analysis of OSL width compared to previous studies as described in Fig.
10. The major discrepancy was found at the basal turn where, besides the use of different methodologies, both studies lack in samples group size (our pilot study
n = 2; previous study
n = 1). Further investigation will have to be carried out to provide reliable statistics especially on distances closer to the base. The combination of a highly porous trabecular bone and the fluid filled cochlea creates a new approach for hearing mechanical studies. Evidently, future kinetic cochlea studies must consider the OSL and the cochlear partition as one mobile structure, the differences in porosity from base to apex, and the effects of the fluid dynamics in their vibration analysis calculations. This modeling work can help support recent theories regarding the influence of different material properties on the motion of the cochlear partition and contribute to the understanding of low-frequency and bone conductive hearing [
30]. As a result, it will be useful in the development of clinical interventions for the preservation of hearing.
Another possible clinical consequence of the OSL’s porosity is that it can potentially play a role in manufacture of new implant technology, direct inner ear drug delivery, and stem cell delivery. Secondary to hair cell loss, spiral ganglion’s neuron degeneration is one of the major causes of sensorineural hearing loss. The use of perilymph as carrier for inner ear drug delivery is common, but it is inefficient due to the difficulty in reaching stable therapeutic concentrations throughout the cochlea [
31‐
37]. The spiral ganglion’s neurons are located in Rosenthal’s canal which runs along the OSL, and there is increasing evidence of their permeability to small molecules and neurotrophic genes [
38‐
42]. The difficulty of drugs in crossing the blood–labyrinth barrier has been reported [
33,
43,
44]. In the future, drug-eluted cochlear implants could potentially take advantage of the OSL’s porosity to enable drug distribution directly to the spiral ganglion [
45].
Geometrical reconstruction of the OSL revealed a cantilever structure that should be considered in future mathematical models for studying hearing mechanics. Although it should be noted that the voxel size used in this pilot study may be considered relatively large to obtain accurate measurements, especially in the OSL thickness range, the thickness and width we measured are consistent with previous studies [
6,
7]. However, in contrast to earlier findings [
6], our porosity measurements demonstrated the presence of pores in both VP and TP (up to 69%), as well as random bony pillars distribution throughout the cochlea in both radial and longitudinal directions. Additionally, it was possible to observe the habenular openings through a new perspective; rather than the previously described “tunnel”, our study showed a “cave”. Furthermore, the connection between the cochlear partition and the OSL that we have demonstrated in 3D should encourage others to consider that they possess a “one flexible structure” morphology. In this article, we present three of four factors (i.e., geometry) to be considered in future studies of hearing mechanics: the width, thickness, and stiffness (porosity) of the OSL. The inter-plate bony pillars (including its thickness and related stiffness) should also be considered as a factor and added to the mathematical models. Gathering information on these variables by applying 3D methodology described here to a larger sample size will provide a better understanding of hearing mechanics.
Conclusion
A combination of surgical dissection techniques with microCT allowed, for the first time, an isotropic volumetric study of the human OSL. Our study demonstrated the porosity of both plates (VP and TP) and the presence of bony pillars in the middle of the OSL. It also enabled a flight through the habenular openings and throughout the whole cochlea. The microCT technique emerges as a valuable imaging option in hearing research, providing a detailed anatomical 3D-reconstruction of the ear. Furthermore, visualizing the anatomical details of an intact cochlea at the micrometer level, with high resolution, and in 3D provides valuable new information for application to future anatomical, physiological, and mathematical studies.
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