Postnatal structural development of mammalian Basilar Membrane provides anatomical basis for the maturation of tonotopic maps and frequency tuning

Abstract

The basilar membrane (BM) of the mammalian cochlea constitutes a spiraling acellular ribbon that is intimately attached to the organ of Corti. Its graded stiffness, increasing from apex to the base of the cochlea provides the mechanical basis for sound frequency analysis. Despite its central role in auditory signal transduction, virtually nothing is known about the BM’s structural development. Using polarized light microscopy, the present study characterized the architectural transformations of freshly dissected BM at time points during postnatal development and maturation. The results indicate that the BM structural elements increase progressively in size, becoming radially aligned and more tightly packed with maturation and reach the adult structural signature by postnatal day 20 (P20). The findings provide insight into structural details and developmental changes of the mammalian BM, suggesting that BM is a dynamic structure that changes throughout the life of an animal.

A maturational frequency discrimination deficit may explain developmental language disorder.

“…The basilar membrane remains in our view a good starting point for future inquiry because the deficits we see among some children with DLD are spectral in nature and because the basilar membrane is the seat of tonotopic organization throughout the auditory pathway. We also hypothesized that, given that emilin2 plays an important role in the emergence of the development of the mechanical gradient of the basilar membrane (Amma et al, 2003; Russell et al, 2020; Tani et al, 2021), potential disruption to the expression of this gene might be considered (though we cite the emilin2 literature primarily to emphasize how a genetic abnormality can in principle disrupt the emergence of the mechanical gradient of the basilar membrane). Yet, given the enormous complexity of the auditory pathway, numerous possibilities obviously remain.…”

“…For instance, voiceless fricatives such as/ʃ/, which contain relatively high-frequency components, may stimulate basal regions of the membrane, while vowels such as /ɑ:/, which contain low-frequency components, may stimulate apical regions. Upon the basilar membrane sit a single row of approximately 3,500 inner hair cells, which become selectively responsive to specific frequencies—that is, they are “frequency-tuned”—as a result of their position on the basilar membrane (Sumner et al, 2018; Tani et al, 2021). In turn, inner hair cells are innervated by spiral ganglion neurons, which project to the cochlear nucleus, with this and subsequent innervation conserving tonotopic sensitivity and resulting in the emergence of frequency sensitive “maps” throughout a complex array of subcortical structures of the auditory brainstem and on to the peripheral auditory cortex.…”

“…In turn, inner hair cells are innervated by spiral ganglion neurons, which project to the cochlear nucleus, with this and subsequent innervation conserving tonotopic sensitivity and resulting in the emergence of frequency sensitive “maps” throughout a complex array of subcortical structures of the auditory brainstem and on to the peripheral auditory cortex. The physical properties of the basilar membrane are, therefore, at the heart of frequency sensitivity and acoustic signal decomposition across the auditory pathway, and this itself underpins accurate and efficient speech processing and encoding (Burnham & Mattock, 2014; Echteler et al, 1989; Nuttall et al, 2018; Sumner et al, 2018; Tani et al, 2021). From the third trimester to 6 months of age, structures from the auditory nerve throughout the auditory pathway to the auditory cortex undergo substantial changes in synaptic organization, myelination, and dendritic arborization, and this process of maturation continues through 2 years of age during a typically rich period of language development (Chonchaiya et al, 2013).…”

Full-Range Optical Imaging of Planar Collagen Fiber Orientation Using Polarized Light Microscopy

“…In contrast to QPLM [ 20 , 21 ], CLSM [ 13 , 14 ], or MM [ 15 ], the proposed method does not require any additional equipment such as quarter-wave plates [ 34 , 35 ] and compensators [ 29 – 33 ] which may be difficult or even impossible to be supplemented into some of the microscopes as it was in our case; it is based on light microscopy and requires only two polarizers and a standard rotary table. Thus, the proposed method appears promising thanks to its broad applicability even with the simplest polarized light microscopes.…”

“…In this paper, we present a new method for semiautomatic evaluation of the orientation and dispersion of collagen fibers using PLM within all the 180° range without any additional components. Although this limitation has already been overcome by addition of a universal compensator (two variable retarders) in front of the sample [ 29 – 33 ], or a quarter-wave plate behind it [ 34 , 35 ] in the light path of the polarizing microscope, the presented algorithm is applicable with any polarized light microscope even if this additional equipment cannot be used. We have found another way how to overcome the angular limitation given by the periodicity of light intensity at crossed filters and proposed an automatic algorithm that is capable to evaluate the orientation in each pixel of the micrograph.…”