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Collagen-based mechanical anisotropy of the tectorial membrane: implications for inter-row coupling of outer hair cell bundles.

Gavara N, Chadwick RS - PLoS ONE (2009)

Bottom Line: We found that the TM's large mechanical anisotropy results in a marked transmission of deformations along the direction that maximizes sensory cell excitation, whereas in the perpendicular direction the transmission is greatly reduced.Computational results, based on our values of elastic moduli, suggest that the TM facilitates the directional cooperativity of sensory cells in the cochlea, and that mechanical properties of the TM are tuned to guarantee that the magnitude of sound-induced tip-link stretching remains similar along the length of the cochlea.Furthermore, we anticipate our assay to be a starting point for other studies of biological tissues that require directional functionality.

View Article: PubMed Central - PubMed

Affiliation: Auditory Mechanics Section, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, MD, USA.

ABSTRACT

Background: The tectorial membrane (TM) in the mammalian cochlea displays anisotropy, where mechanical or structural properties differ along varying directions. The anisotropy arises from the presence of collagen fibrils organized in fibers of approximately 1 microm diameter that run radially across the TM. Mechanical coupling between the TM and the sensory epithelia is required for normal hearing. However, the lack of a suitable technique to measure mechanical anisotropy at the microscale level has hindered understanding of the TM's precise role.

Methodology/principal findings: Here we report values of the three elastic moduli that characterize the anisotropic mechanical properties of the TM. Our novel technique combined Atomic Force Microscopy (AFM), modeling, and optical tracking of microspheres to determine the elastic moduli. We found that the TM's large mechanical anisotropy results in a marked transmission of deformations along the direction that maximizes sensory cell excitation, whereas in the perpendicular direction the transmission is greatly reduced.

Conclusions/significance: Computational results, based on our values of elastic moduli, suggest that the TM facilitates the directional cooperativity of sensory cells in the cochlea, and that mechanical properties of the TM are tuned to guarantee that the magnitude of sound-induced tip-link stretching remains similar along the length of the cochlea. Furthermore, we anticipate our assay to be a starting point for other studies of biological tissues that require directional functionality.

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Algebraic decrease of the ratio between displacements and forces as the tip was moved away from the bead.Behavior of Δd/ΔF with increasing bead-tip distances (1//r/). Solid line is the best linear fit, the slope of which yields an elastic modulus (see Table 1). This example graph shows the fit that gives the shear modulus perpendicular to the fiber in the apex of the cochlea. Samples from the same animal and cochlea location were averaged together for a single data point. Data are shown as mean±SE (N being the number of animals used).
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pone-0004877-g005: Algebraic decrease of the ratio between displacements and forces as the tip was moved away from the bead.Behavior of Δd/ΔF with increasing bead-tip distances (1//r/). Solid line is the best linear fit, the slope of which yields an elastic modulus (see Table 1). This example graph shows the fit that gives the shear modulus perpendicular to the fiber in the apex of the cochlea. Samples from the same animal and cochlea location were averaged together for a single data point. Data are shown as mean±SE (N being the number of animals used).

Mentions: For each measurement, the initial indentation was 1 µm and the cantilever was ramped with a sawtooth time pattern an additional micron in the same direction as the initial indentation (Fig. 4 right). Ramping indentations resulted in oscillatory forces with amplitudes ranging 10–120 nN. Consistently, the position of the fluorescent beads also displayed oscillatory movements with amplitudes ranging 20–200 nm (Fig. 3 and 4) at an angle with respect to the direction of the applied force. It should be noted that this angle arose from two different reasons. On the one hand, for certain configurations the Green's tensor predicts a component of displacement perpendicular to the force. On the other hand, small misalignments between the direction of force application and the direction of the fibers also contribute to this perpendicular component (Fig. 3). This angle did not enter into the calculation of the elastic moduli since only the component of displacement in the direction of the applied in-plane force component was required (see Modeling section below). As the tip was moved away from the bead during a set of measurements, forces did not change markedly, but resulting bead displacements were found to decrease. Therefore, was observed to decrease with increasing tip-bead distances. In addition, decreases in were well-fitted by a linear function of 1//r/, indicating strong agreement between our model and the experimental data (see Modeling in the Methods section and Fig. 5). On additional measurements, we verified that the slope of the fit did not depend on the initial indentation (Fig. S1). The slopes of the fits were then used to compute the three elastic moduli. The fiber modulus was found to be on the order of a KPa, whereas the shear moduli were an order of magnitude smaller (Table 1). All elastic moduli displayed larger values at the base of the TM than at the apex.


Collagen-based mechanical anisotropy of the tectorial membrane: implications for inter-row coupling of outer hair cell bundles.

Gavara N, Chadwick RS - PLoS ONE (2009)

Algebraic decrease of the ratio between displacements and forces as the tip was moved away from the bead.Behavior of Δd/ΔF with increasing bead-tip distances (1//r/). Solid line is the best linear fit, the slope of which yields an elastic modulus (see Table 1). This example graph shows the fit that gives the shear modulus perpendicular to the fiber in the apex of the cochlea. Samples from the same animal and cochlea location were averaged together for a single data point. Data are shown as mean±SE (N being the number of animals used).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2654110&req=5

pone-0004877-g005: Algebraic decrease of the ratio between displacements and forces as the tip was moved away from the bead.Behavior of Δd/ΔF with increasing bead-tip distances (1//r/). Solid line is the best linear fit, the slope of which yields an elastic modulus (see Table 1). This example graph shows the fit that gives the shear modulus perpendicular to the fiber in the apex of the cochlea. Samples from the same animal and cochlea location were averaged together for a single data point. Data are shown as mean±SE (N being the number of animals used).
Mentions: For each measurement, the initial indentation was 1 µm and the cantilever was ramped with a sawtooth time pattern an additional micron in the same direction as the initial indentation (Fig. 4 right). Ramping indentations resulted in oscillatory forces with amplitudes ranging 10–120 nN. Consistently, the position of the fluorescent beads also displayed oscillatory movements with amplitudes ranging 20–200 nm (Fig. 3 and 4) at an angle with respect to the direction of the applied force. It should be noted that this angle arose from two different reasons. On the one hand, for certain configurations the Green's tensor predicts a component of displacement perpendicular to the force. On the other hand, small misalignments between the direction of force application and the direction of the fibers also contribute to this perpendicular component (Fig. 3). This angle did not enter into the calculation of the elastic moduli since only the component of displacement in the direction of the applied in-plane force component was required (see Modeling section below). As the tip was moved away from the bead during a set of measurements, forces did not change markedly, but resulting bead displacements were found to decrease. Therefore, was observed to decrease with increasing tip-bead distances. In addition, decreases in were well-fitted by a linear function of 1//r/, indicating strong agreement between our model and the experimental data (see Modeling in the Methods section and Fig. 5). On additional measurements, we verified that the slope of the fit did not depend on the initial indentation (Fig. S1). The slopes of the fits were then used to compute the three elastic moduli. The fiber modulus was found to be on the order of a KPa, whereas the shear moduli were an order of magnitude smaller (Table 1). All elastic moduli displayed larger values at the base of the TM than at the apex.

Bottom Line: We found that the TM's large mechanical anisotropy results in a marked transmission of deformations along the direction that maximizes sensory cell excitation, whereas in the perpendicular direction the transmission is greatly reduced.Computational results, based on our values of elastic moduli, suggest that the TM facilitates the directional cooperativity of sensory cells in the cochlea, and that mechanical properties of the TM are tuned to guarantee that the magnitude of sound-induced tip-link stretching remains similar along the length of the cochlea.Furthermore, we anticipate our assay to be a starting point for other studies of biological tissues that require directional functionality.

View Article: PubMed Central - PubMed

Affiliation: Auditory Mechanics Section, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, MD, USA.

ABSTRACT

Background: The tectorial membrane (TM) in the mammalian cochlea displays anisotropy, where mechanical or structural properties differ along varying directions. The anisotropy arises from the presence of collagen fibrils organized in fibers of approximately 1 microm diameter that run radially across the TM. Mechanical coupling between the TM and the sensory epithelia is required for normal hearing. However, the lack of a suitable technique to measure mechanical anisotropy at the microscale level has hindered understanding of the TM's precise role.

Methodology/principal findings: Here we report values of the three elastic moduli that characterize the anisotropic mechanical properties of the TM. Our novel technique combined Atomic Force Microscopy (AFM), modeling, and optical tracking of microspheres to determine the elastic moduli. We found that the TM's large mechanical anisotropy results in a marked transmission of deformations along the direction that maximizes sensory cell excitation, whereas in the perpendicular direction the transmission is greatly reduced.

Conclusions/significance: Computational results, based on our values of elastic moduli, suggest that the TM facilitates the directional cooperativity of sensory cells in the cochlea, and that mechanical properties of the TM are tuned to guarantee that the magnitude of sound-induced tip-link stretching remains similar along the length of the cochlea. Furthermore, we anticipate our assay to be a starting point for other studies of biological tissues that require directional functionality.

Show MeSH
Related in: MedlinePlus