Development of Auditory and Vestibular Systems

574 Pages·1983·13.227 MB·English

by  R. Romand (Eds.)

Contributors
MATTI ANNIKO DAVID R. MOORE
JOHN F. BRUGGE JAROMÍR MYSLIVECEK
L. CAZIN EDWARD M. ORNITZ
IAN S. CURTHOYS L. R. PALMBACH
M. S. DEOL W. PRECHT
GÜNTER EHRET EVAN M. RELKIN
RITA B. EISENBERG R. ROMAND
O. G. GAZENKO JERZY E. ROSE
KENNETH R. HENRY JAMES C. SAUNDERS
JAMES A. KALTENBACH HANNA M. SOBKOWICZ
J. LANNOU YA. A. VINNIKOV
D. V. LYCHAKOV THOMAS R. VAN DE WATER
Development of
Auditory and Vestibular Systems
Edited by
R. ROMAND
Laboratoire de Neurophysiologie
Université de Montpellier II
Place Eugène Bataillon
34060 Montpellier Cedex, France
ACADEMIC PRESS
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COPYRIGHT© 1983 BY ACADEMIC PRESS, INC.
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United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
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LiDrary of Congress Cataloging in Publication Data
Main entry under title:
Development of auditory and vestibular systems.
Includes index.
1. Auditory pathways. 2. Vestibular apparatus.
3. Developmental neurology. I. Romand, R. [DNLM:
1. Auditory pathways—Growth and development.
2. Vestibular apparatus—Growth and development.
3. Hearing. WV 272 D489]
QP461.D485 1982 612'.85 82-16400
ISBN 0-12-594450-0
PRINTED IN THE UNITED STATES OF AMERICA
83 84 85 86 9 8 7 6 5 4 3 2 1
Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
MATTIANNIKO (375), Department of Otorhinolaryngology, Karolińska Hospital,
and King Gustav V Research Institute, Karolińska Institute, S-I04 01
Stockholm, Sweden
JOHN F. BRUGGE (89), Department of Neurophysiology, and Waisman Center on
Mental Retardation and Human Development, University of
Wisconsin-Madison, Madison, Wisconsin 53706
L. CAZIN (463), Laboratoire de Neurophysiologie sensorielle, Université de Rouen,
Rouen, France
IAN. S. CURTHOYS (425), Department of Psychology, University of Sydney,
Sydney, New South Wales 2006, Australia
M. S. DEOL (309), Department of Genetics and Biometry, University College
London, London WC1E 6BT, United Kingdom
GÜNTER, EHRET (211), Fakultät für Biologie, Universität Konstanz, D-7750
Konstanz, Federal Republic of Germany
RITA B. EISENBERG (239), Bioacoustics Section, Bioengineering Laboratories,
Department of Neurological Surgery, Albert Einstein College of Medicine, Bronx,
New York
O. G. GAZENKO (537), Sechenov Institute of Evolutionary Physiology and Bio-
chemistry, USSR Academy of Sciences, Leningrad, USSR
KENNETH R. HENRY (273), Department of Psychology, University of California,
Davis, Davis, California 95616
xi
Xli Contributors
JAMES A. KALTENBACH (3), Department of Biology, University of
Pennsylvania, Philadelphia, Pennsylvania 19104
J. LANNOU (463), Laboratoire de Neurophysiologie sensorielle, Université de
Rouen, Rouen, France
D. V. LYCHAKOV (537), Institute of General Genetics, USSR Academy of Sci-
ences, Moscow, USSR
DAVID R. MOORE (121), University Laboratory of Physiology, Parks Road, Ox-
ford 0X1 3PT, England
JAROMÍR MYSLIVECEK (167), Institute of Hygiene and Epidemiology, Prague,
Czechoslovakia, CS 100 42
EDWARD M. ORNITZ (479), Department of Psychiatry, and Brain Research Insti-
tute, School of Medicine, University of California-Los Angeles, Los Angeles,
California 90024
L. R. PALMBACH (537), Institute of General Genetics, USSR Academy of Sciences,
Moscow, USSR
W. PRECHT (463), Institut für Hirnforschung, Universität Zürich, Zürich,
Switzerland
EVAN M. RELKIN (3), Auditory Research Laboratory, Northwestern University,
Evanston, Illinois 60201
R. ROMAND (47), Laboratoire de Neurophysiologie, Université de Montpellier II,
Place Eugène Bataillon, 34060 Montpellier Cedex, France
JERZY E. ROSE (27), Department of Neurophysiology, University of
Wisconsin—Madison, Madison, Wisconsin 53706
JAMES C, SAUNDERS (3), Department of Otorhinolaryngology and Human Com-
munication, University of Pennsylvania, Philadelphia, Pennsylvania 19104
HANNA M. SOBKOWICZ (27), Department of Neurology, University of
Wisconsin—Madison, Madison, Wisconsin, 53706
YA. A. VINNIKOV (537), Sechenov Institute of Evolutionary Physiology and Bio-
chemistry, USSR Academy of Sciences, Leningrad, USSR
THOMAS R. VAN DE WATER (335), Laboratory of Development Otobiology, Rose
F. Kennedy Center, Albert Einstein College of Medicine, Bronx, New York 10461
Preface
Interest in the development of sensory and neuronal functions in mam-
mals and man has grown rapidly during the past decade. Our knowledge
of auditory and vestibular systems has reached a point at which an up-to-
date review of recent research will be of great service to those interested in
the field. The contributions in this volume show the current state of ad-
vancement and provide perspectives for future research on the develop-
ment of auditory and vestibular function.
The book includes contributions from a number of noted scientists of
different disciplines, all of whom are working on questions concerning the
structural and functional ontogeny of the stato-acoustic system. Although
dealing with specific topics from the whole range of research, the separate
chapters complement each other and present a complete overview of basic,
applied and clinical research, including the latest developments in the field.
The reader will see from the table of contents that emphasis has been
placed on the study of receptors and brainstem nuclei for both the auditory
and vestibular systems. This, in fact, reflects present research trends. Most
current studies are devoted to these peripheral structures, whereas even 15
years ago investigations concerning the development of the auditory sys-
tem, for example, dealt mainly with the cortical level.
Apart from one chapter (Chapter 16), I have limited this book to studies
devoted to mammals, including man, because a review dealing with other
vertebrates, such as birds, is already available. I sincerely hope that readers
xiii
XIV Preface
initially concerned with a particular topic in this volume will also be stimu-
lated by the other chapters and that they will come to share my enthusiasm
for this fast-expanding field of neuroscience.
This volume provides the reader with the broadest possible understand-
ing of the ontogeny of the stato-acoustic system. Part I is devoted to the
development of the auditory system and represents the major portion of
the book. The first chapter, by Saunders, Kaltenbach, and Relkin discusses
the structural and functional development of the outer and middle ear and
their possible implications for the auditory capability of the immature ani-
mal. Chapter 2 by Sobkowicz and Rose concerns the experimental develop-
ment of the acoustic receptors in vitro. Chapter 3 by Romand provides in-
formation on the development of the cochlear potentials, along with some
recently discovered aspects of in vivo structural maturation of the cochlea.
In Chapters 5 and 6, Brugge and Moore broaden our understanding of the
ontogeny of the auditory system. They discuss their experiments on the
brainstem and inferior colliculus, reviewing them in terms of structure and
function, and they offer data on binaural interaction in normal and de-
prived developing animals. In Chapter 6, Myslivecek, a pioneer in the
study of the development of the auditory system, especially at its higher
levels, reviews the development of cortical potentials in animals with re-
spect to some new biochemical findings. In Chapter 7, Ehret discusses the
important subject of the development of auditory response behavior with
respect to the onset of auditory response behavior in a variety of mammals.
Eisenberg (Chapter 8) analyzes the development of hearing in children and
more specifically the neonatal perception of speech and nonspeech signals.
Chapter 9 by Henry is concerned with specific problems related to
audiogenic seizure, drugs, and noise effect during cochlear development
and their implications during development. Deol's chapter on the malfor-
mation of stato-acoustic receptors in mice (Chapter 10) serves as a link be-
tween the two parts of the book.
If the development of the auditory system has been the subject of many
investigations, both at an anatomical and a physiological level, the develop-
ment of the vestibular system has been less studied, especially at a func-
tional level. The first studies were mainly restricted to the differentiation of
receptors, which were often studied in close relation with the auditory re-
ceptors. Van De Water's chapter (Chapter 11) makes it obvious that it is
difficult to separate the two sensory modalities of the stato-acoustic system,
especially at the periphery during early development.
In Chapter 12, Anniko summarizes information on the in vivo structural
development of vestibular receptors in many species. The functional aspect
is analyzed at the first-order vestibular neuron level by Curthoys (Chapter
13) and at the second-order neuron level by Lannou, Precht, and Cazin in
Preface XV
Chapter 14. These two studies represent the first successful quantitative
approaches. Chapter 15 by Ornitz deals with optometric responses in nor-
mal and pathologic children. The last contribution, by Vinnikov, Gazenko,
Lychakov, and Palmbach (Chapter 16), concerns the development of the
vestibular receptors in weightlessness and provides a basis for exciting fu-
ture research on the vestibular system.
This book will certainly be of value to a wide range of scientists, not only
to those already involved in the study of the development of the stato-
acoustic system but also to those interested in developmental neuroscience
in general. It will be of interest to otologists, audiologists, physicians in-
volved in child care, auditory physiologists, and others. Scientists and stu-
dents just starting work in this rapidly growing area of research will find
this volume an important source of comprehensive information.
1
The Structural and Functional Development
1
of the Outer and Middle Ear
JAMES C. SAUNDERS
JAMES A. KALTENBACH
EVAN M. RELKIN
I. Introduction
The auditory system in all vertebrates contains a number of signal-pro-
cessing components. In general, we use the anatomical divisions of the
auditory system to define these components; the outer, middle and inner
ear, and the auditory regions of the central nervous system (CNS). The
development of hearing in any species is best understood in terms of the
maturation of each component. This is particularly important in the audi-
tory periphery, where the components are arranged in a serial sequence.
Each component of the series has a response characteristic that describes
the way energy is transferred from the input to the output. For example,
the range of frequencies over which the pinna responds restricts the fre-
quency input to the ear canal, and the frequency range of the ear canal
response may set further limits on the frequencies affecting the tympanic
membrane (TM), and so on. Thus, the input to the auditory nerve, regard-
less of the mechanisms involved, cannot exceed the limitations imposed by
more distal elements of the peripheral ear.
In this chapter, the development of the most peripheral components,
the outer and middle ears, will be considered. We will proceed by discuss-
ing the outer ear, then the structural organization of the middle ear during
lrrhe authors gratefully acknowledge the support of the Pennsylvania Lions Hearing
Research Foundation and the Deafness Research Foundation in the preparation of this chapter.
Mr. Kaltenbach is a Predoctoral Fellow supported by NIH Grant 5T32-GM-07517-04.
3
DEVELOPMENT OF AUDITORY AND Copyright © 1983 by Academic Press, Inc.
VESTIBULAR SYSTEMS All rights of reproduction in any form reserved.
ISBN: 0-12-594450-0
4 James C. Saunders, James A. Kaltenbach, and Evan M. Relkin
the final stages of maturation, and finally, the functional ontogeny of the
middle ear. Human and animal literature will be presented in order to
demonstrate similar and different patterns of development in these areas.
II. Maturation of the Outer Ear
A. Anatomical Aspects
Few studies have traced the maturation of interaural distance (head
size), pinna size and convolutions, and the length and diameter of the ear
canal (external meatus). The human adult interaural distance, as measured
from tragus to tragus, is 17.5 cm (Woodworth, 1938), whereas that in the
newborn is only 11.2 cm. This represents a 36% expansion from the infant
to the adult. The interaural distance changes by 25% from the young kitten
to the adult (Moore and Irvine, 1979). In the adult mouse, the interaural
distance, as measured between the entrance to the ear canals is 8.6 mm
(Saunders and Garfinkle, 1982). We have measured the interaural distance
in the 11-day-old neonate, and it is about 5.1 mm. This represents a 41%
change between the neonate and adult.
The human pinna achieves an adult shape in the 20-week fetus. Howev-
er, this structure continues to expand in size and does not stop growing
until around the ninth year (Northern and Downs, 1974). At birth, the
pinna in the kitten appears flat and is not much more than a slight protru-
sion about the ear canal (Villablanca and Olmstead, 1979). The convolu-
tions of the pinna are not developed and the tragus is nothing more than a
minor protuberance. The pinna does not exhibit adult characteristics until
around 31 days postnatally (Villablanca and Olmstead, 1979). In the adult
cat, the pinna has increased in size, the tragus becomes pronounced, and
the other folds of the auricle are sufficiently convoluted so that they appear
to obstruct the ear canal. Thus, whether the pinna first appears prenatally
(human) or postnatally (kitten), the growth process continues into
adolesence.
There is also evidence that the ear canal changes with postnatal age. The
adult human has a canal length between 25 and 27 mm (Shaw, 1974;
Wever & Lawrence, 1954). The length of the canal in the newborn is
difficult to measure because the TM is nearly parallel to the walls of the
canal, but it appears to be about 22.5 mm (McLellan and Webb, 1957).
Furthermore, the canal appears to be oval in cross section, but much nar-
rower than the adult in diameter. The ear canal continues to mature in the
child up to 7 years of age (Northern and Downs, 1974). During this time
there are changes in the canal wall, in the canal diameter, and in the
position of the TM. There is some information about ear canal develop-
ment in the kitten and mouse. Between 7 and 12 days of postnatal life, the