Hair-Bundle Mechanics

Vestibular and non-mammalian auditory hair bundles (left) differ in shape from mammalian cochlear hair bundles (right). (Right) In the mammalian cochlea, the structure of inner-hair-cell bundles (top) differs from outer-hair-cell bundles (bottom).

 
  • The hair bundle is the organelle that converts mechanical input into electrical output for transmission to the brain in the auditory, vestibular, and lateral line systems of all vertebrates 1, 2. We study how a bundle functions as a detector of different types of signals in divergent sensory organs.
  • In response to the quietest sounds we can hear, the hair bundle moves by less than one-billionth of a meter. Hair bundles of many auditory and vestibular organs oscillate spontaneously in the absence of sensory input owing to an active mechanical process. Mathematical modeling predicts that this process can, in some situations, amplify an auditory bundle’s response to periodic stimulation arising from sound and can, under different conditions, allow a vestibular bundle to detect step stimulation owing to head movement3. The mechanosensory function of a hair bundle is controlled by its mechanical environment and can be manipulated in experiments to adjust the bundle’s response to stimulation4,5. Modeling suggests how vestibular systems changed function through evolution to become auditory organs (see figure below). We further propose that despite environmental and developmental variation, a hair-bundle’s function can be ensured by a homeostatic mechanism within sensory organs4. We are presently studying the influence of intrinsic noise on the signal-detection properties of active systems 7, 8.
  • A hair bundle is comprised of a set of stereocilia, hair-like projections extending from the surface of the sensory hair cell. Stereocilia are attached to each other by links that allow the bundle to move as a unit when stimulated. One crucial type of link stems from the interaction between the proteins and lipids coating each stereocilium9. Hair bundles extracted from the auditory systems of mammals do not move cohesively, however, and differ in shape from those in other vertebrate organs (see figure above). To understand how a hair-bundle’s shape contributes to its function, we determined the morphology of a living auditory hair bundle from a mammal for the first time10. How a hair bundle's cohesiveness and shape contribute to its function are topics of current investigation.

The mechanical load on a hair bundle controls its function.

References

  1. A bundle of mechanisms: Inner-ear hair-cell mechanotransduction, Ó Maoiléidigh D and AJ Ricci, Trends Neurosci 42:221 (2019)
  2. 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)
  3. The diverse effects of mechanical loading on active hair bundles, Ó Maoiléidigh D and Hudspeth AJ, Proc Natl Acad Sci USA 109:1943 (2012)
  4. Control of a hair bundle’s mechanosensory function by its mechanical load, Salvi JD†, Ó Maoiléidigh D†, Fabella BA, Tobin M, and Hudspeth AJ, Proc Natl Acad Sci USA 112:E1000 (2015) (†Equal contribution)
  5. Identification of bifurcations from observations of noisy biological oscillators, Salvi JD, Ó Maoiléidigh D, and Hudspeth AJ, Biophys J 111:798 (2016)
  6. Homeostatic enhancement of sensory transduction, Milewski A, Ó Maoiléidigh D, Salvi JD, and Hudspeth AJ, Proc Natl Acad Sci USA 114:E6794 (2017)
  7. Sinusoidal-signal detection by active, noisy oscillators on the brink of self-oscillation, Ó Maoiléidigh D and Hudspeth AJ, Physica D 378-379:33 (2018)
  8. Multiple mechanisms for stochastic resonance are inherent to sinusoidally driven noisy Hopf oscillators, Ó Maoiléidigh D, Physical Review E 97:022226 (2018)
  9. Divalent counterions tether membrane-bound carbohydrates to promote the cohesion of auditory hair bundles, LeBouef AC, Ó Maoiléidigh D, and Hudspeth AJ, Biophys J 100:1316 (2011)
  10. Dimensions of a living cochlear hair bundle, Miller K, Atkinson P, Mendoza KR, Ó Maoiléidigh D, and Grillet N, Front Cell Dev Biol 9:742529 (2021)