Review
Primary innervation of the avian and mammalian cochlear nucleus

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Abstract

The auditory nerve of birds and mammals exhibits differences and similarities, but given the millions of years since the two classes diverged from a common ancestor, the similarities are much more impressive than the differences. The avian nerve is simpler than that of mammals, but share many fundamental features including principles of development, structure, and physiological properties. Moreover, the available evidence shows that the human auditory nerve follows this same general organizational plan. Equally impressive are reports that homologous genes in worms, flies, and mice exert the same heredity influences in man. The clear implication is that animal studies will produce knowledge that has a direct bearing on the human condition.

Introduction

Adaptations for specialized hearing are impressive and widespread among vertebrates. As a result, auditory neurobiology has benefited greatly from the application of a variety of research techniques to understand structure-function relationships in a range of species. The unique advantages that particular species offer have allowed the development of useful animal models for study of both normal and pathologic aspects of human hearing. Birds and mammals, both endothermic amniotes, share sophisticated abilities to generate complex sounds for communication and to use their hearing as a means to locate and identify potential mates, predators, and prey. Although mammals and birds last shared a reptilian ancestor more than 200 million years ago 8., 34., it has often been informative to examine how similar auditory problems are solved by representative modern birds and mammals. These research programs often begin by analyzing how a particular feature of an animal’s hearing is integral to its ecology and evolutionary history and then seek to understand how derived features of the auditory system serve specific hearing functions. This approach has identified important features common to brain development and function in the terrestrial vertebrates and it appears that the comparative approach will continue to be productive [33].

This review will compare what is known about the projection of the auditory nerve onto the brainstem auditory nuclei in birds and mammals with the intent of highlighting biologically significant similarities and differences. The auditory nerve conveys environmental acoustic information to the brain by taking the output of the sensory hair cells in the inner ear and distributing it to various target neurons in the cochlear nuclei.

Section snippets

Birds

In birds, the auditory nerve enters the lateral aspect of the brain stem and terminates in the cochlear nuclei angularis and magnocellularis (chicken and penguin, 17., 140., 151.). Individual fibers are myelinated, their diameter increases with increasing CF up to about 7 kHz in the barn owl [91], and they arise from a population of ganglion cells that is homogeneous in comparison with mammalian spiral ganglion neurons (chicken, [52]; barn owl, [92]). In the absence of experimenter-controlled

Mammals

Differences between the organization of the avian basilar papilla and the mammalian cochlea are further emphasized by features of the spiral ganglion neurons, primary neurons in mammals, which convey the output of the receptors as input to the brain. There are normally two separate populations of ganglion cell types in adult mammals on the basis of somatic size and staining characteristics 85., 124., 193., 194.. There are large, bipolar, type I cells and small, pseudomonopolar type II cells (

Physiological response properties

In mammals, individual type I auditory nerve fibers may be defined by three fundamental properties: [1] frequency selectivity, [2] response threshold, and [3] spontaneous discharge rate. Frequency selectivity refers to the fiber’s tendency to be most sensitive to a single frequency as defined by a “threshold–tuning curve” 49., 88.. The fiber will respond to any combination of level and frequency that falls within its curve. The tip of the curve indicates the frequency to which it is most

SR and peripheral correlates

Morphologic specializations have been found in the innervation pattern of inner hair cells with respect to SR fiber groupings. High-SR fibers (>18 spikes/s) have thick peripheral processes that tend to contact the “pillar” side of the inner hair cell, whereas low-SR fibers (<18 spikes/s) have thin peripheral processes that tend to contact the modiolar side of the hair cell 98., 111.. Furthermore, there is SR segregation within the spiral ganglion. Low-SR neurons tend to be distributed on the side

Cochlear nucleus

The cochlear nucleus is the sole target of the axon terminals of the spiral ganglion. It is located along the dorsolateral convexity of the pontine-medullary junction, lying beneath the flocculus and paraflocculus of the cerebellum. The auditory nerve enters the cochlear nucleus from below. On the basis of cytoarchitectonic features, the cochlear nucleus can be divided into two main divisions—dorsal and ventral 20., 103., 133., 151.. The DCN is characterized by a distinct layering pattern,

Summary

Analysis of auditory nerve fibers in birds and mammals reveals striking similarities and differences. In view of the 200 million years since these two classes diverged from their common ancestor, the similarities in auditory nerve characteristics are remarkable. The avian nerve is simpler than that of the mammal, but many fundamental principles of neural development, structure and function are shared. Perhaps because of the greater simplicity of the avian system, their study has brought many

Acknowledgements

The authors wish to thank their colleagues and coworkers who contributed data to this project. We are especially grateful to Christine Köppl for pertinent discussions of issues, M. Christian Brown for helpful comments on the manuscript, and to Liana Rose for helping to organize the bibliography. The authors were supported in part by NIH Grants DC00232, DC04395, and DC00144.

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