Mechanical Control of Sensory Hair-Bundle Function

Author

Joshua D. Salvi

Date of Award

2015

Document Type

Thesis

Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Hudspeth Laboratory

Abstract

Hair bundles detect sound in the auditory system, head position and rotation in the vestibular system, and fluid flow in the lateral-­‐‑line system. To do so, bundles respond to periodic, static, and hydrodynamic forces contingent upon the receptor organs in which they are situated. As the mechanosensory function of a hair bundle varies, so too do the mechanical properties of the bundle and its microenvironment. Hair bundles range in height from 1 μμm to 100 μμm and in stiffness from 100 μμN·∙m-­‐‑1 to 10,000 μμN·∙m-­‐‑1. They are composed of actin-­‐‑filled, hypertrophic microvilli—stereocilia—that number from fewer than 20 through more than 300 per bundle. In addition, bundles may or may not possess one true cilium, the kinocilium. Hair bundles differ in shape across organs and organisms: they may be isodiametric, fan-­‐‑shaped, or V-­‐‑shaped. Depending on the organ in which they occur, bundles may be free-­‐‑standing or they may be coupled to a tectorial membrane, otolithic membrane, cupula, or sallet. Because all hair bundles are comprised of similar molecular components, their distinct mechanosensory functions may instead be regulated by their mechanical loads. Dynamical-­‐‑systems analysis provides mathematical predictions of hair-­‐‑bundle behavior. One such model captures the effects of mechanical loading on bundle function in a state diagram. A mechanical-­‐‑load clamp permits exploration of this state diagram by robustly controlling the loads—constant force, load stiffness, virtual drag, and virtual mass—imposed on a hair bundle. Upon changes in these mechanical parameters, the bundle’s response characteristics alter. Subjected to particular control parameters, a bundle may oscillate spontaneously or remain quiescent. It may respond nonlinearly to periodic stimuli with high sensitivity, sharp frequency tuning, and easy entrainment; or it may respond linearly with low sensitivity, broad tuning, and reluctant entrainment. The bundle’s response to a force pulse may resemble that of an edge-­‐‑detection system or a low-­‐‑pass filter. Finally, a bundle from an amphibian vestibular organ can operate in a manner qualitatively similar to that from a mammalian auditory organ, implying an essential similarity between hair bundles. The bifurcation near which a bundle’s operating point resides controls its function: the state diagram provides a functional map of mechanosensory modalities. Auditory function is best tuned near a supercritical Hopf bifurcation, whereas vestibular function is captured by a subcritical Hopf bifurcation and a cusp bifurcation. Within the proposed region vestibular responsiveness, a hair bundle exhibits mechanical excitability analogous to the electrical excitability of neurons. This behavior implies for the first time a direct relationship between the mechanical behaviors of sensory organelles and the electrical behaviors of afferent neurons. Man-­‐‑made detectors function in limited capacities, each designed for a unique purpose. A single hair bundle, on the other hand, evolved to serve multiple purposes with the requirement of only two functional traits: adaptation and nonlinear channel gating. The remarkable conservation of these capabilities thus provides unique insight into the evolution of sensory systems.

Comments

A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy

Recommended Citation

Salvi, Joshua D., "Mechanical Control of Sensory Hair-Bundle Function" (2015). Student Theses and Dissertations. 286.
https://digitalcommons.rockefeller.edu/student_theses_and_dissertations/286