Dimensions of a Living Cochlear Hair Bundle
Front Cell Dev Biol
2021; 9: 742529
The hair bundle is the mechanosensory organelle of hair cells that detects mechanical stimuli caused by sounds, head motions, and fluid flows. Each hair bundle is an assembly of cellular-protrusions called stereocilia, which differ in height to form a staircase. Stereocilia have different heights, widths, and separations in different species, sensory organs, positions within an organ, hair-cell types, and even within a single hair bundle. The dimensions of the stereociliary assembly dictate how the hair bundle responds to stimuli. These hair-bundle properties have been measured previously only to a limited degree. In particular, mammalian data are either incomplete, lack control for age or position within an organ, or have artifacts owing to fixation or dehydration. Here, we provide a complete set of measurements for postnatal day (P) 11 C57BL/6J mouse apical inner hair cells (IHCs) obtained from living tissue, tissue mildly-fixed for fluorescent imaging, or tissue strongly fixed and dehydrated for scanning electronic microscopy (SEM). We found that hair bundles mildly-fixed for fluorescence had the same dimensions as living hair bundles, whereas SEM-prepared hair bundles shrank uniformly in stereociliary heights, widths, and separations. By determining the shrinkage factors, we imputed live dimensions from SEM that were too small to observe optically. Accordingly, we created the first complete blueprint of a living IHC hair bundle. We show that SEM-prepared measurements strongly affect calculations of a bundle's mechanical properties - overestimating stereociliary deflection stiffness and underestimating the fluid coupling between stereocilia. The methods of measurement, the data, and the consequences we describe illustrate the high levels of accuracy and precision required to understand hair-bundle mechanotransduction.
View details for DOI 10.3389/fcell.2021.742529
View details for PubMedCentralID PMC8657763
- A Bundle of Mechanisms: Inner-Ear Hair-Cell Mechanotransduction Trends in neurosciences 2019; 42: 221-236 Hide
- Bilateral spontaneous otoacoustic emissions show coupling between active oscillators in the two ears Biophysical Journal 2019; 116: 2023-2034 Hide
Multiple mechanisms for stochastic resonance are inherent to sinusoidally driven noisy Hopf oscillators.
Physical Review E
2018; 97: 022226
To ensure their sensitivity to weak periodic signals, some physical systems likely operate near a Hopf bifurcation. Many systems operating near such a bifurcation exhibit stochastic resonance, but it is unclear which mechanisms for resonance are inherent to the bifurcation. To address this question, we study the sinusoidally forced dynamics of noisy supercritical and subcritical Hopf oscillators. We find four qualitatively different mechanisms for stochastic resonance and determine the conditions for each type of resonance.
View details for DOI 10.1103/PhysRevE.97.022226
- Sinusoidal-signal detection by active, noisy oscillators on the brink of self-oscillation Physica D 2018; 378-379: 33-45 Hide
Homeostatic enhancement of sensory transduction.
Proceedings of the National Academy of Sciences of the United States of America
2017; 114 (33): E6794-E6803
Our sense of hearing boasts exquisite sensitivity, precise frequency discrimination, and a broad dynamic range. Experiments and modeling imply, however, that the auditory system achieves this performance for only a narrow range of parameter values. Small changes in these values could compromise hair cells' ability to detect stimuli. We propose that, rather than exerting tight control over parameters, the auditory system uses a homeostatic mechanism that increases the robustness of its operation to variation in parameter values. To slowly adjust the response to sinusoidal stimulation, the homeostatic mechanism feeds back a rectified version of the hair bundle's displacement to its adaptation process. When homeostasis is enforced, the range of parameter values for which the sensitivity, tuning sharpness, and dynamic range exceed specified thresholds can increase by more than an order of magnitude. Signatures in the hair cell's behavior provide a means to determine through experiment whether such a mechanism operates in the auditory system. Robustness of function through homeostasis may be ensured in any system through mechanisms similar to those that we describe here.
View details for DOI 10.1073/pnas.1706242114
View details for PubMedID 28760949
- Mechanical Transduction Processes in the Hair Cell Understanding the Cochlea Springer International Publishing. 2017: 75–111 Hide
Identification of Bifurcations from Observations of Noisy Biological Oscillators.
2016; 111 (4): 798-812
Hair bundles are biological oscillators that actively transduce mechanical stimuli into electrical signals in the auditory, vestibular, and lateral-line systems of vertebrates. A bundle's function can be explained in part by its operation near a particular type of bifurcation, a qualitative change in behavior. By operating near different varieties of bifurcation, the bundle responds best to disparate classes of stimuli. We show how to determine the identity of and proximity to distinct bifurcations despite the presence of substantial environmental noise. Using an improved mechanical-load clamp to coerce a hair bundle to traverse different bifurcations, we find that a bundle operates within at least two functional regimes. When coupled to a high-stiffness load, a bundle functions near a supercritical Hopf bifurcation, in which case it responds best to sinusoidal stimuli such as those detected by an auditory organ. When the load stiffness is low, a bundle instead resides close to a subcritical Hopf bifurcation and achieves a graded frequency response-a continuous change in the rate, but not the amplitude, of spiking in response to changes in the offset force-a behavior that is useful in a vestibular organ. The mechanical load in vivo might therefore control a hair bundle's responsiveness for effective operation in a particular receptor organ. Our results provide direct experimental evidence for the existence of distinct bifurcations associated with a noisy biological oscillator, and demonstrate a general strategy for bifurcation analysis based on observations of any noisy system.
View details for DOI 10.1016/j.bpj.2016.07.027
View details for PubMedID 27558723
View details for PubMedCentralID PMC5002087
Control of a hair bundle's mechanosensory function by its mechanical load.
Proceedings of the National Academy of Sciences of the United States of America
2015; 112 (9): E1000-9
Hair cells, the sensory receptors of the internal ear, subserve different functions in various receptor organs: they detect oscillatory stimuli in the auditory system, but transduce constant and step stimuli in the vestibular and lateral-line systems. We show that a hair cell's function can be controlled experimentally by adjusting its mechanical load. By making bundles from a single organ operate as any of four distinct types of signal detector, we demonstrate that altering only a few key parameters can fundamentally change a sensory cell's role. The motions of a single hair bundle can resemble those of a bundle from the amphibian vestibular system, the reptilian auditory system, or the mammalian auditory system, demonstrating an essential similarity of bundles across species and receptor organs.
View details for DOI 10.1073/pnas.1501453112
View details for PubMedID 25691749
View details for PubMedCentralID PMC4352782
- Vibrational Modes and Damping in the Cochlear Partition MECHANICS OF HEARING: PROTEIN TO PERCEPTION 2015; 1703 Hide More
Books & Chapter Reviews
Mechanical transduction processes in the hair cell
Corey D, Ó Maoiléidigh D, and Ashmore J
Understanding the Cochlea, Springer Handbook of Auditory Research
Manley GA, Gummer AW (Eds.), Springer (2017)
The interplay between active hair bundle mechanics and electromotility in the cochlea
Ó Maoiléidigh D and Julicher F
Concepts and challenges in the biophysics of hearing, p451, World Scientific Publishing (2009)