The Auditory Periphery Biophysics and Physiology

553 Pages·1973·9.275 MB·English

by  Peter Dallos (Auth.)

The Auditory Periphery
B I O P H Y S I CS A ND P H Y S I O L O GY
PETER D A L L OS
Auditory Research Laboratory (Audiology)
and Department of Electrical Engineering
Northwestern University
Evans ton, Illinois
ACADEMIC PRESS New York and London 1973
A Subsidiary of Harcourt Brace Jovanovich, Publishers
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To the memory of E. Ascher
Preface
My major motivation for writing this book was that a comprehensive
description of the functioning of the peripheral auditory system was not
available. To teach the subject one was forced tö rely on journal articles, some
reviews, and on some excellent but older books such as those of Stevens and
Davis or Wever and Lawrence. The content of "Physiological Acoustics"
(Wever and Lawrence) was closest to what I envisioned as desirable, but it
was fifteen years old and, moreover, I thought it relied too much on viewing
the system through the microphonic potential. Von Bιkιsy's "Experiments in
Hearing" had a much wider scope than just the treatment of the auditory
periphery, and it was a collection of research papers, not a monograph with
continuity. Thus I set out to fill what I perceived as a void. Now, some years
later, the same void still exists even though there is more tutorial material
available as chapters in various compendia.
This book attempts to provide a detailed and relatively complete account of
the biophysics and physiology of the peripheral auditory system. It is aimed at
a relatively heterogeneous audience, since workers in many fields have an
interest in various aspects of the functioning of the hearing organ. I am
hopeful that the work will be useful to biophysicists and bioengineers as well
as to physiologists, otolaryngologists, and speech and hearing scientists.
Because of the desire to provide a comprehensive account of the operation
of the auditory system, the inclusion of considerable mathematical detail was
deemed necessary. The heterogeneity of the envisioned readership, however,
dictated that certain mathematical steps and procedures be explained. My
rationale for choosing what knowledge to assume and what to explain is as
follows. More and more young practitioners of the life sciences are acquainted
xi
xii PREFACE
with differential calculus and have some knowledge of differential equations.
However, probably relatively few would be familiar with, for example, the
use of Laplace transforms in systems analysis. Thus the latter technique is
used more sparingly and on an elementary level. A considerable amount of
mathematics is included in Chapters III and IV, but I believe that even these
segments of the book will prove to be readable by the nonmathematically
oriented reader.
To make the book self-contained, the first chapter provides some back-
ground in the anatomy of the peripheral auditory system and the second
describes the most common experimental techniques. I conceive of the " audi-
tory periphery " as extending to, but not including, the cochlear nerve. Con-
sequently, neural phenomena are treated in the book only to the extent that
they highlight cochlear events. This is arbitrary and clearly reflects my
orientation and approach. The referenced material is necessarily selective, and
I apologize to all colleagues whose pertinent work was overlooked, particu-
larly to those—most likely to be in this category—whose work is not in
English.
There are many individuals who directly or indirectly contributed to the
realization of this book. Dr. Raymond Carhart, Director of the Auditory
Research Laboratory at Northwestern University, provided the appropriate
milieu and freedom during the past ten years to make my laboratory flourish
and allow me to grow professionally. He has also given his friendship and
much valuable advice. George W. Allen, M. D., first introduced me to the
use of animal preparations and physiological techniques. Much credit is
due to my students and collaborators: P. Allaire, M. Billone, B. Chesnutt,
J. R. Boston, J. Durrani, I. Hung, C. O. Linneil, L. Pinto, R. G. Robbins,
Z. G. Schoeny, R. H. Sweetman, C-y. Wang, and D. W. Worthington. W. Ballad
provided valuable help in preparing photographic material for the book.
Dr. C. Laszlo gave me wise suggestions for Chapters II and III. Very special
thanks are due to my associate, Mary Ann Cheatham, for her good work and
invaluable help in the preparation of this book. Mrs. Laura Reiter and her
typists, Mrs. B. Duffin and Mrs. N. Seitz, did an outstanding job in preparing
the manuscript. I thank the various publishers for their permission to repro-
duce copyrighted material and the many authors who helped me by providing
photographs and drawings for illustrations.
The National Institute of Neurological Diseases and Stroke is thanked for
the continuing support of my laboratory and my research efforts. Apprecia-
tion is expressed to the Research Committee of Northwestern University for
defraying the costs of preparing this manuscript.
Finally, my wife Cirla has provided an atmosphere of love, patience,
and understanding without which this work could not have been undertaken,
much less completed.
PETER DALLOS
CHAPTER 1
Introduction
This introduction provides a framework for the detailed discussions that
follow in subsequent chapters. Here, a presentation of the functional organ-
ization of the auditory system is followed by a rather sketchy description
of the gross and neuroanatomy of the hearing organ.
I. Functional Organization of the Auditory System
In Fig. 1.1 a block diagram of the system is presented. The individual
boxes represent the logical structural divisions within the overall system.
The subdivisions above the actual block diagram indicate the function of
any group of blocks, while those below pertain to the predominant mode of
operation within a given block or group of blocks.
The first block represents the outer ear, whose external visible portion
is the auricle or pinna and whose 44inside the head" portion is the earcanal
or external auditory meatus. The auricle in man has very little acoustic
effect. In some animals, however, it is enlarged and quite movable and thus
serves a useful role in the localization of sound in space. The earcanal, a
long narrow tube, funnels the incoming sound to the eardrum, which is its
inner boundary. The main function of the canal is to protect the delicate
middle ear from noxious outside agents. The canal also introduces its own
acoustic resonance into the transmission process; thus it exerts an effect on
1
1. INTRODUCTION
PROTECTION IMMPAETDCAHN CE DIFSITLRTEIBRUINTGIO N TRANSDUCTION INFORMATION PROCESSING
W
OUTER EAR MIDDLE EAR BASILAR SENSORY NERVE BRAINSTEM AUDITORY
MEMBRANE CELLS FIBERS CENTERS CORTEX
EFFERENT SYSTEM
ACOUSTIC REFLEX
AIR MECHANICAL ELECTROCHEMICAL ELECTROCHEMICAL
VIBRATION VIBRATION HYDRODYNAMICS (ANALOG) (ANALOG +DIGITAL )
Fig. 1.1. Block diagram of the auditory system. In the center the anatomical sub-
divisions are shown, with the arrows indicating the direction of information flow. At the
top the function of the various segments is indicated, while at the bottom the dominant
mode of operation is described.
the actual information flow in the auditory organ. Within the earcanal sound
is conducted by the vibration of air molecules. This fluctuating air pressure
sets the eardrum into vibration and thus activates the mechanical lever,
pressure transformer of the middle ear: the ossicular chain. The airborne
sound is then translated into the vibrations of the bones of the middle
ear.
The function of the middle ear is to translate airborne vibrations into
pressure waves in the fluid that fills the inner ear (cochlea) and to match
impedances between this fluid and air. The middle ear fulfills this role by
boosting sound pressure through a combined force-pressure amplification
process. The middle ear is endowed with muscles that can contract reflexively
and thus subserve one of the feedback mechanisms that operate in the
auditory system: the middle ear muscle reflex. The vibrations of the innermost
bone of the ossicular chain are delivered to the fluid that fills the inner ear
cavity. There the pressure wave sets the membranous portions of the inner
ear into vibration and causes local deformations within the complex cellular
structure that forms an important portion of this membrane complex.
The sensory cells of the hearing organ are situated within the cell matrix
attached to the membranous structure, and these cells are deformed in the
above process. The deformation of these cells is the final mechanical event
in the chain that starts with airborne vibrations and continues with mechani-
//. Anatomy of the Auditory System 3
cal movements within the middle ear, followed by hydrodynamic and fine
mechanical events in the inner ear.
The sensory cells are transducers that convert mechanical deformation
to electrical and chemical processes, the latter of which serves as the com-
municating link to the auditory nerve. The fibers of the nerve carry all informa-
tion pertaining to the auditory environment in the form of nerve spikes whose
temporal pattern (density) codes this information. The function of the inner
ear is to perform appropriate filtering of the incoming acoustic signal coupled
with the distribution of acoustic energy to differing groups of sensory cells,
depending largely on the spectral content of the signal. The sensory cells
are the critical transducers in the auditory chain. Feedback signals are trans-
mitted to the inner ear by the well-developed efferent auditory system.
All variables up to the initiation of spikes in the auditory nerve are in analog
form; in other words, they are smoothly graded functions of the parameters
of the incoming sound.
The information carried in the auditory nerve passes up, through various
brainstem centers, to the auditory cortex. There is a great deal of cross con-
nection between the two sides (left and right) beyond the first way station
in the brainstem, and there is also a great deal of centrifugal information
flow from the cortex down to the various brainstem nuclei via the efferent
auditory system and the reticular formation. We can consider the entire
neural network beyond the cochlea to serve the function of auditory informa-
tion processing. One more feedback system should be mentioned for the
sake of completeness. This is the sympathetic innervation of the auditory
nerve fibers and of the blood vessels that serve the inner ear.
The aim of the chapters to follow is to provide the details of operation
of the various subcomponents of the system that form the "auditory periph-
ery. " These include the middle ear and the inner ear up to and including
the initiation of impulses in the auditory nerve but excluding the delineation
of the code whereby these impulses carry information. Similarly excluded
are the properties of functioning of the subcortical and cortical auditory
centers. We shall include a treatment of the peripheral portions of the
various feedback mechanisms.
II. Anatomy of the Auditory System
A. GROSS ANATOMY*
The overall anatomical structure of the ear can be followed with great
clarity in Fig. 1.2, which is a reproduction of Brödel's well-known illustration
of the cross section of the human ear.
* Zemlin (1968), Wever and Lawrence (1954), Polyak (1946).
4 1. INTRODUCTION
1. The External Ear
The auricle is the externally visible, flaplike portion of the ear that is
attached to the sides of the head. It is largely cartilaginous and has many
convoluted folds that lead to the opening of the external meatus. This is an
irregularly shaped canal, and in the human being is about 3 cm long with a
diameter of approximately 7 mm. The size and shape vary greatly among
species. In the cat, for example, it consists of a narrow peripheral portion
about 1.5 cm long and a wider central portion approximately 0.5 cm in length.
Fig. 1.2. Reproduction of M. BrödeFs classical drawing of the cross section of the
human ear. (From Brodel, 1946.)
These two segments of the canal are almost perpendicular to one another.
A peripheral segment of the canal has cartilaginou s walls, while the medial
segment has bony walls. The relative lengths of these two portions vary
among species. In human beings the two segments are about equal in length,
while in the cat there is virtually no bony segment. The inner wall of the
meatus is lined with skin bearing numerous hairs and wax-producing glands.
//. Anatomy of the Auditory System 5
These serve a protective function and keep intrusion of foreign matter to a
minimum.
2. The Middle Ear
The middle ear is an air-filled volume situated in a cavity which in higher
mammals is surrounded by the temporal bone of the skull but which in most
laboratory animals is surrounded by a thin bony compartment, the auditory
bulla, attached to the skull. The middle ear cavity extends from the eardrum
on its lateral border to the bony cochlear wall on its medial extreme. It
communicates with the cochlea through two openings in the bony wall,
the oval and round windows, and it also communicates with the nasopharynx
via the eustachian tube. In humans the middle ear volume is customarily
divided into two portions: the superior attic and the inferior tympanic
cavities. The former communicates via the tympanic antrum with the mastoid
air cells ; thus the effective volume of the middle ear is considerably in excess
of the volume of the tympanic cavity proper. The entire cavity, including
the antrum and the mastoid air cells, is covered with a smooth mucous
membrane lining. In animals that possess auditory bullae, the middle ear
space is divided by a partition (bony septum) into two volumes. One of these
is analogous to the tympanic cavity and houses the ossicular chain, while
the other communicates with the round window. The relative size of the
cavities and the size of the opening between these volumes are highly species
variable. In some rodents (e.g., chinchilla, kangaroo rat) the bulla is hyper-
trophied and it contains several communicating air-filled compartments that
greatly increase the effective volume of the middle ear cavity.
The lateral border of the middle ear, the eardrum or tympanic membrane,
is a cone-shaped structure held in place by its own thickened, fibrous border,
the annulus, which is inserted into a groove in the bony wall of the earcanal.
The membrane itself is made up of three layers. The outermost layer is con-
tinuous with the lining of the earcanal, while the innermost layer is continuous
with the lining of the middle ear. The structure that gives the membrane its
characteristic cone shape and its structural stability is the central fibrous
layer. This layer is composed of two groups of fibers, one radially oriented
and one concentrically arranged. A long process (manubrium) of the most
peripheral ossicle, the malleus, is firmly attached to the tympanic membrane,
covering the full radius at 12 o'clock. Thus movements of the tympanic
membrane are transmitted into movements of the malleus. The other two
bones of the ossicular chain, the incus and the stapes, transmit the malleolar
vibrations to the oval window of the cochlea, to which a portion of the stapes
is flexibly affixed. The three bones form a functional unit; the joints between
the adjacent bones are relatively firm. In most rodents the malleus and the
incus are actually fused and thus there is only one joint in these species.