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ARTICLE, Behavioral/Systems

Internal Shearing within the Hearing Organ Evoked by Basilar Membrane Motion

Anders Fridberger, Jacques Boutet de Monvel and Mats Ulfendahl
Journal of Neuroscience 15 November 2002, 22 (22) 9850-9857; DOI: https://doi.org/10.1523/JNEUROSCI.22-22-09850.2002
Anders Fridberger
Department of Physiology and Pharmacology, Karolinska Institutet, SE-171 76 Stockholm, Sweden
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Jacques Boutet de Monvel
Department of Clinical Neuroscience and Center for Hearing and Communication Research and
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Mats Ulfendahl
Department of Clinical Neuroscience and Center for Hearing and Communication Research and
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    Fig. 1.

    Schematic drawing of the insertion of the perfusion tube into the scala tympani (ST) of the basal turn (left). Fluid flowed continuously through the scala tympani to exit through the helicotrema (small arrows). An increase in scala tympani pressure shifted the organ in the direction of the scala vestibuli (SV;large arrow). Fluid compartments filled with perilymph are dark gray; endolymphatic compartments arelight gray. Right, Anatomical structures visible in subsequent figures are indicated in this schematic drawing of a cross section of the organ of Corti in the apical turn.BM, Basilar membrane; DC, Deiter cell;OP, outer pillar cell; TC, tunnel of Corti; IP, inner pillar cell; IHC, inner hair cell; TM, tectorial membrane; OHC, outer hair cell; HC, Hensen cell; RM, Reissner's membrane. The asterisk indicates a nerve fiber crossing the tunnel of Corti to reach the outer hair cells.

  • Fig. 2.
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    Fig. 2.

    A, Confocal view of the hearing organ in the apical turn. Red staining originates from the membrane dye RH795, and green stain originates from the cytoplasmic dye calcein. B, Merged image of the organ at two different pressure levels. The image was generated through averaging the red and green channels of the RGB image shown inA to form a single-channel grayscale image. This grayscale image was subsequently given a pink color. Similar averaging was applied to an image acquired at a different pressure level, and that image was coded green. Thus, structures that overlap each other in the two images will appeargray, and structures that moved will be eitherpink or green. Note the relatively small motion in the inner hair cell region and the graded increase in amplitude that occurred when moving to the right part of the image. The scale bar applies to both panels.

  • Fig. 3.
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    Fig. 3.

    A, High-magnification view of the tunnel of Corti region. B, Merged RGB image of the same part of the organ, generated by applying the same scheme as in Figure 2B (image at high pressure,pink; image after decrease in pressure,green). The scale bar applies to bothpanels.

  • Fig. 4.
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    Fig. 4.

    Top left, Confocal micrograph showing the difference in intensity values between the frames corresponding to the two maximum displacements of the cycle toward the scala vestibuli and toward the scala tympani, respectively.Bright and dark pixels correspond to significant displacements, whereas absence of motion appears in amedium green-gray color. The trajectories of different points along the reticular lamina (a–d), on the hair cell bodies (e–h), and on the inner and outer pillar cells (i–l) are shown, as measured from the optical flow computation. Bottom, Details of optical flow trajectories of points on the reticular lamina (a–d), at the cell bodies below (e–h), and along the inner (i–k) and outer (l) pillar cells. The initial position (indicated by a star) was taken as the origin for each trajectory. The final position was marked by a × symbol. Note the large displacement in the negative direction (i.e., when the cochlear partition is biased toward the scala tympani) and the difference in orientation of the trajectories obtained at the bottom and top parts of the inner pillar cells. IHC, Inner hair cell;OHC, outer hair cell; IP, inner pillar cell; OP, outer pillar cell. Top right, Plot of the trajectory amplitudes in micrometers for 15 points along the reticular lamina (from the inner hair cell to the third-row outer hair cell) as a function of the distance from the inner hair cell apex. Note the clear linear growth of the amplitude, reflecting a rigid motion of the reticular lamina. The dashed line is a best linear fit to the set of data points. RL, Reticular lamina.

  • Fig. 5.
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    Fig. 5.

    Deformations of the projected profile of the inner hair cell. A contour delimiting the profile of the cell was drawn by hand for the first frame of the sequence shown in Figure 4 and was left to evolve according to the measured displacements between successive frames. The image is a merged view of the two maximum displacements of the inner hair cell toward the scala vestibuli and scala tympani, respectively, with the corresponding profiles superimposed. Only the channel corresponding to the RH795 dye (Fig. 4A,red) is displayed. The length of the cell was measured as the distance from point A to point C, and its width was measured as the distance from B toD. (A′–D′ are the corresponding points in the second frame.)

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    Fig. 6.

    Determination of the effective pivot axis of the reticular lamina. Results are shown for two different experiments (A, B). For each experiment, a least-squares estimation of the reticular lamina pivot axis was performed using three different series of time points, corresponding to different angular displacements of the reticular lamina: 0, The full series of 13 frames (maximum angular displacements of 3.4 and 2.7° for experimentsA and B, respectively); 1, a medium subseries (maximum angular displacements of 3.0 and 1.9° forA and B, respectively); and2, a small subseries (maximum angular displacements of 1.1 and 0.95° for A and B, respectively). Displayed in each case are the image difference between the two frames corresponding to the maximum displacements upward and downward, together with the estimated pivot axis, and a sample of gridlines showing intermediate positions of the reticular lamina. Note how the location of the pivot axis changes with angular displacement in each of the two experiments, moving toward the apical pole of the inner hair cell for smaller displacements. The profile of the inner hair cell is outlined in blue.

  • Fig. 7.
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    Fig. 7.

    Movement of different points along the pillar cells and sensory cells accompanying basilar membrane displacements. Pivot axes are shown for the inner and outer pillar cells and for the outer hair cells. The estimation was performed for a subseries of the full sequence corresponding to small angular displacements of the structures in the organ. (One of the pivot axes,R1, was estimated outside the frame of the image, as shown by the asterisk.) The difference in the location of the pivot axes for the basal and apical parts of the inner pillar cell indicates cellular deformation. Note that because of the nonrigidity of the outer hair cell bases and of the inner pillar cell, different parts of these cells move around different instantaneous axes of rotation. Therefore, pointsR1–R6 actually represent averaged pivot axes for the corresponding lines highlighted on the cells. PointsR1–R4 carry more information than points R5 and R6 , however, because the inner and outer pillar cells were seen to be less amenable to deformation than the outer hair cell bodies.

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The Journal of Neuroscience: 22 (22)
Journal of Neuroscience
Vol. 22, Issue 22
15 Nov 2002
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Internal Shearing within the Hearing Organ Evoked by Basilar Membrane Motion
Anders Fridberger, Jacques Boutet de Monvel, Mats Ulfendahl
Journal of Neuroscience 15 November 2002, 22 (22) 9850-9857; DOI: 10.1523/JNEUROSCI.22-22-09850.2002

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Internal Shearing within the Hearing Organ Evoked by Basilar Membrane Motion
Anders Fridberger, Jacques Boutet de Monvel, Mats Ulfendahl
Journal of Neuroscience 15 November 2002, 22 (22) 9850-9857; DOI: 10.1523/JNEUROSCI.22-22-09850.2002
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Keywords

  • cochlear mechanics
  • basilar membrane
  • outer hair cells
  • cellular bending
  • pressure changes
  • mechanical properties

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