Development of tonotopy in the auditory periphery

doi:10.1016/j.heares.2011.01.011

Hearing Research

Volume 276, Issues 1–2, June 2011, Pages 2-15

https://doi.org/10.1016/j.heares.2011.01.011 Get rights and content

Abstract

Acoustic frequency analysis plays an essential role in sound perception, communication and behavior. The auditory systems of most vertebrates that perceive sounds in air are organized based on the separation of complex sounds into component frequencies. This process begins at the level of the auditory sensory epithelium where specific frequencies are distributed along the tonotopic axis of the mammalian cochlea or the avian/reptilian basilar papilla (BP). Mechanical and electrical mechanisms mediate this process, but the relative contribution of each mechanism differs between species. Developmentally, structural and physiological specializations related to the formation of a tonotopic axis form gradually over an extended period of time. While some aspects of tonotopy are evident at early stages of auditory development, mature frequency discrimination is typically not achieved until after the onset of hearing. Despite the importance of tonotopic organization, the factors that specify unique positional identities along the cochlea or basilar papilla are unknown. However, recent studies of developing systems, including the inner ear provide some clues regarding the signalling pathways that may be instructive for the formation of a tonotopic axis.

Highlights

► The review discusses recent work on tonotopy in the mammalian, avian, and reptilian hearing organs. ► The functional specializations that mediate tonotopy in both mammals and birds/reptiles are discussed. ► The review links what is currently known about tonotopy in mammals, birds and amphibia with existing studies describing how these systems develop. ► The review also highlights important experiments that could be done to provide greater insight into how tonotopy is established during development.

Introduction

An overarching principle in many sensory systems is the existence of spatial maps that correlate with a fundamental component of each modality. Spatial segregation is maintained throughout multiple aspects of a particular sensory system, often spanning from the primary sensory cells to the cortex. The topographic map of the visual field that exists at multiple levels within the visual system is probably the best known example of a spatial sensory map. However, the presence of a tonotopic map along the length of the avian or mammalian auditory organ, as well as, throughout much of the auditory CNS, is no less impressive. The perceptible auditory environment includes a spectrum of sounds with component frequencies that varies from 20 Hz to greater than 100 kHz. In land bound vertebrates, the auditory organs have evolved as elongated structures with specific anatomic and physiologic specializations that act to spatially segregate these frequencies along their length. However, the specific morphological and physiological modifications that are employed to mediate tonotopy vary between different vertebrate orders, indicating the existence of multiple strategies to address the same challenge.

The development and appropriate patterning of tonotopic specializations is crucial for the perception and appreciation of sound. However, despite an extensive body of knowledge related to the role of tonotopy in auditory function, our understanding of how these graded patterns are initially generated within the auditory epithelia is virtually non-existent. In this review, we will provide an overview of the different mechanisms that are utilized to mediate tonotopic analysis in birds and mammals, as well as discuss the limited data that is available regarding its development. Finally, we will discuss developmental mechanisms that could potentially be involved in the formation of tonotopic gradients within terrestrial auditory systems.

Section snippets

Structure of the peripheral auditory system

The cochlea, refers to the auditory organ in mammals, birds and reptiles (Manley, 2000). Despite differences in structure, the auditory organs of amniotes develop from similar embryonic structures, adopt the same final position in the organism and share a common ancestory (Manley, 2000). In mammals, the cochlea is a coiled structure with between 1.5 and 4 complete turns depending on species, while in birds, reptiles and amphibians it exists as a flat and straight or sickle-shaped epithelium (

Frequency tuning in mammals

The mechanisms that mediate tonotopic analysis along the coiled cochlear duct were initially examined by von Bekesy in the 1950s and 1960s (Bekesy, 1960). Using cadaverous samples he described the generation by incoming sounds of a traveling wave that moves apically along the cochlear duct. Since his pioneering work, the results of multiple studies have provided a comprehensive understanding of the biological mechanism that mediate the tonotopic organization of the cochlea. The passive

Frequency tuning in birds and reptiles

In birds and some reptiles, the auditory epithelium is located in an elongated basilar papilla. In these cases, a tonotopic map similar to that described for the mammalian cochlea, where high frequency sounds stimulate hair cells in the proximal region (equivalent to the base) of the duct and low frequency sounds stimulate those at more distal locations (equivalent to the apex), is also present. Despite these similarities, the mechanisms that mediate frequency tuning along the length of the BP

Development of tonotopic specialization in the auditory sensory epithelia

As discussed, while the mechanisms utilized to spatially separate frequencies along the mammalian and avian/reptilian auditory epithelia differ, a unifying theme is the graded stimulation of hair cells at different positions along the tonotopic axis in response to different frequencies. This suggests that a map of positional identities must exist along the cochlear duct/basilar papilla. Despite extensive research on the timing of the onset of hearing and the ability to discriminate frequencies,

Regulation of positional identity during development

While the results described above provide a reasonable understanding of the temporal development of positional identity, they provide no insight regarding when positional identities become fixed or how these identities are determined. In vitro experiments using spiral ganglion neurons from P3 to P8 mice have suggested that the positional identity of these neurons is modulated by neurotrophins (Adamson et al., 2002a). As neurotrophins are differentially expressed in both embryonic and adult

Hair cell regeneration and tonotopy

A final paradigm that may provide clues regarding the sources of positional information is the examination of hair cell regeneration in the avian basilar papilla. In contrast with mammals, adult birds can regenerate lost hair cells following acoustic or other forms of trauma (Corwin and Cotanche, 1988, Ryals and Rubel, 1988). In most cases, new hair cells arise from supporting cells through either proliferative or non-proliferative mechanisms (Stone and Cotanche, 2007). Moreover, regardless of

Summary

The spatial separation of sounds based on frequency (tonotopy) is one of the most fundamental principles of auditory function. Tonotopic organization is present in the ears of virtually all vertebrates that perceive airborne sounds, including mammals, birds, reptiles and amphibians and is evident at all levels of the auditory system from the primary sensory epithelia through the brainstem nuclei and into the cortex. At the level of the auditory epithelia, the ability to distribute sound energy

Acknowledgement

The authors would also like to acknowledge Professor Guy P. Richardson and Professor Paul Fuchs for critical discussion and comments and Dr Jonathan E. Bird for artistic assistance.

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Published by Elsevier B.V.

ReviewDevelopment of tonotopy in the auditory periphery

Abstract

Highlights

Introduction

Section snippets

Structure of the peripheral auditory system

Frequency tuning in mammals

Frequency tuning in birds and reptiles

Development of tonotopic specialization in the auditory sensory epithelia

Regulation of positional identity during development

Hair cell regeneration and tonotopy

Summary

Acknowledgement

Mol. Cell Neurosci.

Curr. Opin. Neurobiol.

J. Biol. Chem.

Trends Mol. Med.

Hear Res.

Hear Res.

Hear Res.

Hear Res.

Hear Res.

Cell

Neuroscience

Curr Biol.

Cell

J. Struct. Biol.

Hear Res.

Hear Res.

Hear Res.

Trends Biochem. Sci.

Hear Res.

Neuron

Hear Res.

Hear Res.

Neuron

Opposite actions of brain-derived neurotrophic factor and neurotrophin-3 on firing features and ion channel composition of murine spiral ganglion neurons

J. Neurosci.

Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location

J. Comp. Neurol.

Tectorial and basal membranes in experimental hypothyroidism

Arch. Otolaryngol.

Variation of membrane properties in hair cells isolated from the turtle cochlea

J. Physiol.

The calcium-activated potassium channels of turtle hair cells

J. Gen. Physiol.

Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss

J. Neurosci.

Experiments in Hearing

Myosin XVa localizes to the tips of inner ear sensory cell stereocilia and is essential for staircase formation of the hair bundle

Proc. Natl. Acad. Sci. U S A

Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia

Nat. Cell Biol.

Expression of Prox1 during mouse cochlear development

J. Comp. Neurol.

A large-conductance calcium-selective mechanotransducer channel in mammalian cochlear hair cells

J. Neurosci.

Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear

Development

Sound-induced motility of isolated cochlear outer hair cells is frequency-specific

Nature

Central role of supporting cells in cochlear homeostasis and pathology

Ramírez- Med Hypotheses

p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti

Development

Otogelin: a glycoprotein specific to the acellular membranes of the inner ear

Proc. Natl. Acad. Sci. U S A

Regeneration of sensory hair cells after acoustic trauma

Science

Development of location-specific hair cell stereocilia in denervated embryonic ears

J. Comp. Neurol.

An electrical tuning mechanism in turtle cochlear hair cells

J. Physiol.

The Cochlea, an Overview in Cochlear Neurobiology

Prestin, a new type of motor protein

Nat Rev Mol Cell Biol.

Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network

Development

The attachment of the cupulae, otolith and tectorial membranes to the sensory cell areas

Acta Otolaryngol.

Review
Development of tonotopy in the auditory periphery