ReviewPrimary innervation of the avian and mammalian cochlear nucleus
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.
References (232)
- et al.
Some quantitative observations on the cochlear division of the eighth nerve in the squirrel monkey (Saimiri sciureus)
Brain Res.
(1971) - et al.
Clearance of glutamate inside the synapse and beyond
Curr. Opin. Neurobiol.
(1999) - et al.
Central trajectories of type-II spiral ganglion cells from various cochlear regions in mice
Hear. Res.
(1994) - et al.
A monoclonal antibody labels type II neurons of the spiral ganglion
Brain Res.
(1986) - et al.
Differential expression of N-methyl-d-aspartate receptor in the cochlear nucleus of the mouse
Neuroscience
(1996) - et al.
Tonotopic organization of the anteroventral cochlear nucleus of the cat
Hear. Res.
(1981) - et al.
Projections of thin (type-II) and thick (type-I) auditory-nerve fibers into the cochlear nucleus of the mouse
Hear. Res.
(1990) - et al.
The nucleus magnocellularis in the red-eared turtle, Chrysemys scripta elegans: eighth nerve endings and neuronal types
Hear. Res.
(1988) - et al.
Projection of primary vestibular afferent fibers to the cochlear nucleus in the guinea pig
Neurosci. Lett.
(1988) - et al.
The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope
Neuroscience
(1979)
Evolution and development of time coding systems
Curr. Opin. Neurobiol.
Cochlear frequency-place map in adult chickens: intracellular biocytin labeling
Hear. Res.
Postnatal maturation of human spiral ganglion cells: light and electron microscopic observations
Hear. Res.
GABAA receptors in auditory brainstem nuclei of the chick during development and after cochlea removal
Hear. Res.
Glycine-immunoreactivity in the auditory brain stem of the chick
Hear. Res.
Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs
Hear. Res.
Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS
Neuron
A study of cochlear innervation in the young cat with the Golgi method
Hear. Res.
Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections
Brain Res.
Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry
Int. J. Dev. Neurosci.
Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat
Brain Res.
Non-N-methyl-d-aspartate receptors mediating synaptic transmission in the avian cochlear nucleus: effects of kynurenic acid, dipicolinic acid and streptomycin
Neuroscience
Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study
Neuroscience
Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: a Golgi study
Neuroscience
Neuronal morphology in the human cochlear nucleus
Arch. Otolaryngol. Head Neck Surg.
Immunocytochemical localization of aspartate aminotransferase immunoreactivity in cochlear nucleus of the guinea pig
Proc. Natl. Acad. Sci. U.S.A.
The cytoarchitecture of the human anteroventral cochlear nucleus
J. Comp. Neurol.
Potassium currents in octopus cells of the mammalian cochlear nucleus
J. Neurophysiol.
The generation and subtraction of sensory expectations within cerebellum-like structures
Brain Behav. Evol.
Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus
J. Comp. Neurol.
Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate
Proc. Natl. Acad. Sci. U.S.A.
Hair cell innervation by spiral ganglion cells in the mouse
J. Comp. Neurol.
Neurofilament antibodies and spiral ganglion neurons of the mammalian cochlea
J. Comp. Neurol.
Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis
J. Neurophysiol.
Projection of the cochlear and lagenar nerves on the cochlear nuclei of the pigeon
J. Comp. Neurol.
The neuronal architecture of the cochlear nucleus of the cat
J. Comp. Neurol.
Morphology of labeled afferent fibers in the guinea pig cochlea
J. Comp. Neurol.
Central trajectories of type II spiral ganglion neurons
J. Comp. Neurol.
Morphological evidence for secondary vestibular afferent connections to the dorsal cochlear nucleus in the rabbit
Cells Tissues Organs
The central projections of auditory nerve fibers in the barn owl
J. Comp. Neurol.
Organization of the nucleus magnocellularis and the nucleus laminaris in the barn owl: encoding and measuring interaural time differences
J. Comp. Neurol.
Development of the time coding pathways in the auditory brainstem of the barn owl
J. Comp. Neurol.
Distribution of GABAergic neuron and terminals in the auditory system of the barn owl
J. Comp. Neurol.
A neuroethological theory of the operation of the inferior colliculus
Brain Behav. Evol.
Late appearance and deprivation-sensitive growth of permanent dendrites in the avian cochlear nucleus (Nuc Magnocellularis)
J. Comp. Neurol.
Pharmacology and functions of metabotropic glutamate receptors
Annu. Rev. Pharmacol. Toxicol.
Cited by (103)
Using high spatial resolution fMRI to understand representation in the auditory network
2021, Progress in Neurobiology6.18 - Development and Segmental Organization of First Order Information Processing Centers in the Hindbrain
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second EditionModulatory influences on time-coding neurons in the ventral cochlear nucleus
2019, Hearing ResearchHidden hearing loss and endbulbs of Held: Evidence for central pathology before detection of ABR threshold increases
2018, Hearing ResearchCitation Excerpt :In particular, attention has focused on endbulbs of Held (EBs; Held, 1893)—large, axosomatic endings of myelinated auditory nerve fibers that target bushy cells (BCs) in the anteroventral CN (AVCN). These synaptic endings are among the largest synapses in the brain (Ryugo and Spirou, 2009) and show evolutionary conservation across all vertebrates examined to date (Lenn and Reese, 1966; Ryugo and Parks, 2003). They are a crucial structure in the timing pathway, delivering auditory spikes at rapid rates and with high fidelity (Manis et al., 2011).