Diverse Mechanisms of Sound Frequency Discrimination in the Vertebrate Cochlea

Abstract

Discrimination of different sound frequencies is pivotal to recognizing and localizing friend and foe. Here, I review the various hair cell-tuning mechanisms used among vertebrates. Electrical resonance, filtering of the receptor potential by voltage-dependent ion channels, is ubiquitous in all non-mammals, but has an upper limit of~1 kHz. The frequency range is extended by mechanical resonance of the hair bundles in frogs and lizards, but may need active hair-bundle motion to achieve sharp tuning up to 5 kHz. Tuning in mammals uses somatic motility of outer hair cells, underpinned by the membrane protein prestin, to expand the frequency range. The bird cochlea may also use prestin at high frequencies, but hair cells b1 kHz show electrical resonance. Hair Cell-Tuning Mechanisms and Cochlear Structure Hair cells, the sensory receptors of the vertebrate inner ear, convert sound stimuli into electrical signals, and also separate the frequency constituents of the sound, enabling different subsets of hair cells to encode different frequencies. To ensure survival, an animal uses its auditory apparatus to both identify the sound source, whether friend, food, or foe, and to spatially localize it. Are the cries within the forest at night those of an offspring or a predator? Crucially, from which direction do they originate? Can you recognize the voice of a friend across a dark room at a crowded party? Accurate classification and localization of sounds depend on their frequency make-up [1,2]. The mechanisms involved in frequency discrimination differ between the vertebrate classes (reptile, bird, or mammal) and importantly depend on the tonal range to be detected. During the evolution of land vertebrates, there was a drive to extend the upper frequency limit of hearing from a few hundred Hz in the simplest amphibians or reptiles up to~100 kHz in small mammals. To this end, changes have occurred in sound transmission through the middle ear, in the structure of the cochlea, and in the roles of the hair cells. The reasons for the frequency extension are not known for certain. They may partly derive from selective pressure for localizing sounds in animals with small heads, such as the first mammals, or in finding tiny offspring from their high-frequency cries. Another factor driving frequency extension is communication between species members, exemplified by the croaks of frogs, the chirps of geckos, and bird songs, which are all comprise kilohertz sound frequencies. In this review, I describe the evidence for the different cochlear mechanisms, all of which depend upon resonant behavior. A simple illustration of resonance is that generated by a mass, M, suspended on the end of a spring of stiffness K: when the mass is displaced, it oscillates with a resonant frequency, F O, equal to 1//2π.(K/M) 1/2 , and F O increases with larger stiffness and smaller mass. Resonance refers to the increase in the amplitude of the oscillation if an external force is applied at the resonant frequency (but not if the external force is applied at ...

Mechanical Frequency Tuning by Sensory Hair Cells, the Receptors and Amplifiers of the Inner Ear

“…The frequencies present in a sound are resolved in the auditory periphery by mechanisms antecedent to neural coding (2). This step occurs in two ways that are not mutually exclusive.…”

The Molecular Basis of Outer Hair Cell Electromotility is Defined by Prestin’s Conformational Cycle

“…In spite of the intense attention to Prestin since its identification as the OHC motor 1 , fundamental questions remain unanswered, including its oligomeric state [13][14][15][16] , underlying voltage sensing mechanisms, the molecular basis of electromotility, and the evolutionary relationship between Prestin and other, non-electromotive yet closely-related SLC26 family members 17 .…”

An In Vitro Study on Prestin Analog Gene in the Bullfrog Hearing Organs

“…However, the frog inner ear lacks such a sensitive substrate for its sensory cells. Without the basilar membrane, the frog inner ear relies on the tectorial membrane and HCs for frequency selectivity [33].…”