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Olson, E. S.

Publications and source records attributed to Olson, E. S..

4 recordsLinked to original sources

Active strains in the basal organ of Corti in gerbil

Optical coherence tomography (OCT) has allowed in vivo recording of sound-induced vibrations of different regions within the organ of Corti complex (OCC), including the basilar membrane (BM), outer hair cell/Deiters cell (OHC/DC) region, and reticular lamina (RL). In the hook region of the gerbil cochlea, where measurements can be made with a substantially transverse optical axis, the three regions have different and characteristic motion responses: The OHC/DC region has greater motions than the other two regions at frequencies below the best frequency (sub-BF); the RL region typically has the greatest BF peak and smallest sub-BF motion. The phase of the OHC/DC-region motion increasingly lags BM motion phase as frequency increases; the RL-region motion phase leads BM, but with a relatively small value. All three regions are compressively nonlinear in the BF peak, but only the OHC/DC region shows sub-BF compressive nonlinearity. In this paper, we describe the strain that exists within the RL and OHC-body regions. These strains are large where the motion varies over short distances, and a region of large strain can be as short as a single 2.7 {micro}m measurement pixel, or extend over several pixels, with the extensive strains appearing more often at 70 than at 50 dB SPL. Beyond the region of large strain, over a distance that can exceed 20 m, the OHC/DC region displays nearly unvarying motion spatially -- this region appears to vibrate as a body. Statement of SignificanceThe sensory tissue of the cochlea responds actively to a sound stimulus: cell-based forces amplify and enhance the vibration of the sensory tissue. Measurements employing optical coherence tomography have identified major vibration patterns along a sensory-tissue-spanning line that includes the active outer hair cells. In this article, we describe the transitional motion between these major vibration regions and the motion strains that exist as vibration morphs from one region to the next. The findings are presented in frequency response curves to convey the frequency tuning and its stimulus-level dependence, and in one-dimensional heat maps to convey the extent of regional motions and strains. These findings fuel and constrain conceptual and physics-based models of cochlear amplification.

biophysics↗

A frame and a hotspot in cochlear mechanics

Auditory sensation is based in nanoscale vibration of the sensory tissue of the cochlea, the organ of Corti complex (OCC). Motion within the OCC is now observable due to optical coherence tomography. In the cochlear base, in response to sound stimulation, the region that includes the electro-motile outer hair cells (OHC) was observed to move with larger amplitude than the basilar membrane (BM) and surrounding regions. The intense motion is based in active cell mechanics, and the region was termed the "hotspot" (Cooper et al., 2018, Nature comm). In addition to this quantitative distinction, the hotspot moved qualitatively differently than the BM, in that its motion scaled nonlinearly with stimulus level at all frequencies, evincing sub-BF activity. Sub-BF activity enhances non-BF motion; thus the frequency tuning of the hotspot was reduced relative to the BM. Regions that did not exhibit sub-BF activity are here defined as the OCC "frame". By this definition the frame includes the BM, the medial and lateral OCC, and most significantly, the reticular lamina (RL). The frame concept groups the majority OCC as a structure that is largely shielded from sub-BF activity. This shielding, and how it is achieved, are key to the active frequency tuning of the cochlea. The observation that the RL does not move actively sub-BF indicates that hair cell stereocilia are not exposed to sub-BF activity. A complex difference analysis reveals the motion of the hotspot relative to the frame.

neuroscience↗

Amplification lags nonlinearity in the recovery from reduced endocochlear potential

The mammalian hearing organ, the cochlea, contains an active amplifier to boost the vibrational response to low level sounds. Hallmarks of this active process are sharp location-dependent frequency tuning and compressive nonlinearity over a wide stimulus range. The amplifier relies on outer hair cell (OHC) generated forces driven in part by the endocochlear potential (EP), the ~ +80 mV potential maintained in scala media, generated by the stria vascularis. We transiently eliminated the EP in vivo by an intravenous injection of furosemide and measured the vibrations of different layers in the cochleas organ of Corti using optical coherence tomography. Distortion product otoacoustic emissions (DPOAE) were monitored at the same times. Following the injection, the vibrations of the basilar membrane lost the best frequency (BF) peak and showed broad tuning similar to a passive cochlea. The intra-organ of Corti vibrations measured in the region of the OHCs lost their BF peak and showed low-pass responses, but retained nonlinearity, indicating that OHC electromotility was still operational. Thus, while electromotility is presumably necessary for amplification, its presence is not sufficient for amplification. The BF peak recovered nearly fully within 2 hours, along with a non-monotonic DPOAE recovery that suggests that physical shifts in operating condition are a final step in the recovery process. SIGNIFICANCEThe endocochlear potential, the +80 mV potential difference across the fluid filled compartments of the cochlea, is essential for normal mechanoelectrical transduction, which leads to receptor potentials in the sensory hair cells when they vibrate in response to sound. Intracochlear vibrations are boosted tremendously by an active nonlinear feedback process that endows the cochlea with its healthy sensitivity and frequency resolution. When the endocochlear potential was reduced by an injection of furosemide, the basilar membrane vibrations resembled those of a passive cochlea, with broad tuning and linear scaling. The vibrations in the region of the outer hair cells also lost the tuned peak, but retained nonlinearity at frequencies below the peak, and these sub-BF responses recovered fairly rapidly. Vibration responses at the peak recovered nearly fully over 2 hours. The staged vibration recovery and a similarly staged DPOAE recovery suggests that physical shifts in operating condition are a final step in the process of cochlear recovery.

systems biology↗

A role for tectorial membrane mechanics in activating the cochlear amplifier

The mechanical and electrical responses of the mammalian cochlea to acoustic stimuli are nonlinear and highly tuned in frequency. This is due to the electromechanical properties of cochlear outer hair cells (OHCs). At each location along the cochlear spiral, the OHCs mediate an active process in which the sensory tissue motion is enhanced at frequencies close to the most sensitive frequency (called the characteristic frequency CF). Previous experimental results showing an approximate 0.3 cycle phase shift in the OHC-generated extracellular voltage relative the basilar membrane displacement that is initiated at a frequency approximately one-half octave lower than the CF are repeated in the present paper with similar findings. This shift is significant because it brings the phase of the OHC-derived electromotile force near to that of the basilar membrane velocity at frequencies above the shift, thereby enabling the transfer of electrical to mechanical power at the basilar membrane. In order to seek a candidate physical mechanism for this phenomenon, we used a comprehensive electromechanical mathematical model of the cochlear response to sound. The model predicts the phase shift in the extracellular voltage referenced to the basilar membrane at a frequency approximately one-half octave below CF, in accordance with the experimental data. In the model, this feature arises from a minimum in the radial impedance of the tectorial membrane and its limbal attachment. These experimental and theoretical results are consistent with the hypothesis that a tectorial membrane resonance introduces the correct phasing between mechanical and electrical responses for power generation, effectively turning on the cochlear amplifier. SIGNIFICANCEThe mechanical and electrical responses of the mammalian cochlea are nonlinear exhibiting up to a thousand-fold difference in gain depending on the frequency and level of sound stimulus. Cochlear outer hair cells (OHC) are broadband electro-mechanical energy converters that mediate this nonlinear active process. However, the mechanism by which the OHC electromotile force acquires the appropriate phase to power this nonlinearity remains unknown. By analyzing new and existing experimental data and using a mathematical model, we address this open issue. We present evidence which suggests that a relatively simple feature, the frequency dependence of the radial impedance of the tectorial membrane, provides requisite mechanics to turn on the frequency-specific nonlinear process essential for healthy hearing.

systems biology↗