Table Of ContentSPRINGER HANDBOOK OF
AUDITORY RESEARCH
Series Editors: Richard R. Fay and Arthur N. Popper
Springer Science+ Business Media, LLC
SPRINGER HANDBOOK OF AUDITORY RESEARCH
Volume I: The Mammalian Auditory Pathway: Neuroanatomy
Edited by Douglas B. Webster, Arthur N. Popper, and Richard R. Fay
Volume 2: The Mammalian Auditory Pathway: Neurophysiology
Edited by Arthur N. Popper and Richard R. Fay
Volume 3: Human Psychophysics
Edited by William Yost, Arthur N. Popper, and Richard R. Fay
Volume 4: Comparative Hearing: Mammals
Edited by Richard R. Fay and Arthur N. Popper
Volume 5: Hearing by Bats
Edited by Arthur N. Popper and Richard R. Fay
Volume 6: Auditory Computation
Edited by Harold L. Hawkins, Teresa A. McMullen, Arthur N. Popper, and
Richard R. Fay
Volume 7: Clinical Aspects of Hearing
Edited by Thomas R. Van De Water, Arthur N. Popper, and Richard R. Fay
Volume 8: The Cochlea
Edited by Peter Dallos, Arthur N. Popper, and Richard R. Fay
Volume 9: Development of the Auditory System
Edited by Edwin WRubel, Arthur N. Popper, and Richard R. Fay
Volume 10: Comparative Hearing: Insects
Edited by Ronald Hoy, Arthur N. Popper, and Richard R. Fay
Volume II: Comparative Hearing: Fish and Amphibians
Edited by Richard R. Fay and Arthur N. Popper
Volume 12: Hearing by Whales and Dolphins
Edited by Whitlow W.L. Au, Arthur N. Popper, and Richard R. Fay
Volume 13: Comparative Hearing: Birds and Reptiles
Edited by Robert Dooling, Arthur N. Popper, and Richard R. Fay
Volume 14: Genetics and Auditory Disorders
Edited by Bronya J.B. Keats, Arthur N. Popper, and Richard R. Fay
Volume 15: Integrative Functions in the Mammalian Auditory Pathway
Edited by Donata Oertel, Richard R. Fay, and Arthur N. Popper
Volume 16: Acoustic Communication
Edited by Andrea Simmons, Arthur N. Popper, and Richard R. Fay
Volume 17: Compression: From Cochlea to Cochlear Implants
Edited by Sid P. Bacon, Richard R. Fay, and Arthur N. Popper
Volume 18: Speech Processing in the Auditory System
Edited by Steven Greenberg, William Ainsworth, Arthur N. Popper, and Richard R. Fay
Volume 19: The Vestibular System
Edited by Stephen M. Highstein, Richard R. Fay, and Arthur N. Popper
Volume 20: Cochlear Implants: Auditory Prostheses and Electric Hearing
Edited by Fan-Gang Zeng, Arthur N. Popper, and Richard R. Fay
Volume 21 : Plasticity of the Auditory System
Edited by Thomas N. Parks, Edwin W Rubel, and Richard N. Popper
Continued after index
Geoffrey A. Manley
Arthur N. Popper
Richard R. Fay
Editors
Evolution of the
Vertebrate Auditory System
With 101 illustrations
, Springer
Geoffrey A. Manley Arthur N. Popper
Lehrstuhl flir Zoologie Department of Biology
Technische Universitaet Muenchen University of Maryland
85747 Garching, Gennany College Park, MD 20742-4415, USA
This book is dedicated to our families.
GM: Many thanks to Christine for putting up with all the work involved in
preparing this book for publication.
ANP: This volume is dedicated to the ladies in my life-my wife Helen, my
daughters Michelle and Melissa, and my late mother Evelyn. Helen and our
girls have provided infinite love, support, guidance, tolerance, and understanding
during my career. My mother, a consummate teacher, was the ultimate role
model for an aspiring professor.
RRF: I dedicate this volume to my wife Catherine who has imagined and made
possible our life, and the lives of our two children, Christian and Amanda, in
spite of my academic career.
Series Preface
The Springer Handbook of Auditory Research presents a series of comprehen-
sive and synthetic reviews of the fundamental topics in modem auditory re-
search. The volumes are aimed at all individuals with interests in hearing
research including advanced graduate students, postdoctoral researchers, and
clinical investigators. The volumes are intended to introduce new investigators
to important aspects of hearing science and to help established investigators to
better understand the fundamental theories and data in fields of hearing that they
may not normally follow closely.
Each volume presents a particular topic comprehensively, and each serves as
a synthetic overview and guide to the literature. As such, the chapters present
neither exhaustive data reviews nor original research that has not yet appeared
in peer-reviewed journals. The volumes focus on topics that have developed a
solid data and conceptual foundation rather than on those for which a literature
is only beginning to develop. New research areas will be covered on a timely
basis in the series as they begin to mature.
Each volume in the series consists of a few substantial chapters on a particular
topic. In some cases, the topics will be ones of traditional interest for which
there is a substantial body of data and theory, such as auditory neuroanatomy
(Vol. 1) and neurophysiology (Vol. 2). Other volumes in the series deal with
topics that have begun to mature more recently, such as development, plasticity,
and computational models of neural processing. In many cases, the series ed-
itors are joined by a co-editor having special expertise in the topic of the volume.
RICHARD R. FAY, Chicago, Illinois
ARTHUR N. POPPER, College Park, Maryland
Vll
Volume Preface
One of the defining characteristics of vertebrate organisms is that they carry
three paired, major sense organs in the head, the nasal epithelia, the eyes, and
the ears. These sense organs of the head region are protected by being partially
or almost completely enclosed within elements of the skull. This enclosure
means that even in fossil vertebrates, some information concerning the size and
structure of the major sense organs can be obtained, even though soft tissues
are very rarely preserved during fossilization. During the evolution of verte-
brates, these sense organs underwent changes associated with changes in lifestyle
(for example, the transition from water to land living) but also with develop-
ments that led to improvements in the performance of the organs as interfaces
to the outside world. This book is concerned with the evolution of one of these
organs, the ear, and, to a lesser extent, the brain pathways associated with the
processing of the auditory information supplied by the ears.
In Chapter I, Manley and Clack provide a framework for understanding the
evolutionary relationships between the various lineages of vertebrates, without
which it is impossible to understand the changes that have occurred over evo-
lutionary time. In spite of current disagreements regarding the exact status and
relationships and even the nomenclature of some vertebrate groups, this system-
atic framework is adhered to throughout the book, to avoid confusion. Manley
and Clack also provide an overview of the subsequent chapters, to help the
reader better integrate the information provided for each of the major groups of
vertebrates. Here, the emphasis is on the amniotes, the reptiles, birds, and mam-
mals, since these lineages show not only the greatest variety of structural ar-
rangements but also the largest and most complex inner ears.
When biologists speak of the "design" of a structure in an organism, they are
referring to the result of selection pressures, sometimes over very long periods
of time, that have shaped the morphology and the function of that structure.
These selection pressures are, in the special case of sense organs, hugely influ-
enced by the physical and chemical nature of the stimuli to be perceived. In
the present case, the stimuli are sound-pressure waves in the media water and!
or air. As is generally the case for sensory organs, selection pressures existed
for attaining very high sensitivities, in other words for the detection of extremely
IX
x 'Volume Preface
small signal strengths even in the presence of noise and competing signals from
various sources.
In Chapter 2, Lewis and Fay discuss some of the important ecological and
physical factors that would have been omnipresent throughout the history of
vertebrate evolution and must have had an impact on the evolution of vertebrate
hearing. They conclude that in addition to having acoustic transducers, the sine
qua non for any auditory system to function in such a world is the ability to
isolate signals from their individual sources. Furthermore, this quintessential
task must be achieved largely by neural computation, and this requirement es-
tablishes essential constraints on the acoustic transducers, on the signal-
processing structures associated with them, and on the brain itself. In the
appendix at the end of the book, Lewis provides a physical-mathematical frame-
work for understanding the nature of the stimulus and the resulting constraints
that operated during ear evolution. These constraints were responsible for mold-
ing the form and function of vertebrate inner ears to those we see today.
The sensory cells that sub serve the function of hearing are among the oldest
of cell types, with possible forerunners among chordate ancestors and perhaps
even other invertebrate organisms. Thus "hair" cells not only are found in the
inner ear, but also are the typical sensory cell of fish and amphibian lateral-line
organs. In fact, they are the primary sensory cells used by vertebrates for the
detection of mechanical signals from external sources. Since mechanoreceptive
organs can have their stimuli filtered by accessory structures and be required to
provide information on different aspects of the stimuli (acceleration, velocity,
displacement), it is not surprising to find that selection pressures have greatly
influenced the characteristics of such accessory structures. In parallel, however,
we find modifications to hair cell structure and function that are large enough
to justify the recognition of different types of hair cells. In Chapter 3, Coffin
et al. describe the variety of hair cell types in different vertebrates and provide
us with a framework for classifying them and understanding the functional back-
ground for hair cell specialization.
It is clear that the sense of hearing in vertebrates arose well before the origin
of sensory organs especially dedicated to that sense. In fact, the rich acoustic
world of fishes is testimony to the fact that fishes, which form by far the largest
group among vertebrates (more than 50% of species), have created a very useful
hearing system by utilizing preexisting sensory epithelia of the vestibular part
of the inner ear. Since these animals not only live in water but also have a body
largely made up of water, acoustic signals from the environment have no diffi-
culty in penetrating their tissues and are thus not attenuated at the water-to-body
interface. The only requirement for them to be able to detect acoustic stimuli
is that relative motion at the sensory epithelium be produced, and this is only
possible at an impedance transition such as from water to a dense inner-ear
otolith or at the boundary between tissue and the fish's air bladder. It is thus
evident that in fishes, sound detection is based on the use of sensory epithelia
that are also used to detect linear acceleration, and there must be some kind of
compromise in the organs' sensitivities to these different stimuli. In Chapter 4,
Volume Preface xi
Ladich and Popper describe how fishes achieved this compromise, which organs
are involved, and the constraints imposed by the requirement to retain vestibular
responses.
Together with comparative studies of form and function in a variety of modem
vertebrate groups, the study of fossil organisms is the most direct source of
information as to which changes occurred when over evolutionary time. The
transition to land during the development of the first land vertebrates (the la-
byrinthodont amphibians) greatly changed the selection pressures that operated
on the various major sense organs. The nasal epithelium was moistened and
could continue to operate with few changes. The eye required little more than
a change in the optical properties of the lens to accommodate the fact that the
air-corneal interface provided much more refraction of light than a water-cor-
neal interface. Similarly, the largest acoustic problem for the inner ear was to
overcome the huge impedance mismatch between air and body tissues. Or at
least, that was the thinking that influenced the interpretation of the fossil story
for many years.
In Chapter 5, Clack and Allin have gathered together a wealth of data from
vertebrate fossils, providing a detailed interpretation as to what can be read out
concerning the status of the inner ear and especially any special bony connec-
tions between it and the outside world. These authors indicate that tympanic
middle ears as we know them were not characteristic of the earliest land ver-
tebrates, but in fact arose quite late in their evolution, many millions of years
after the origin of the amphibians. This implies not only that important initiating
impulses were missing, but also that the early amphibians and, indeed, early
reptiles were well served by the inner ear without a tympanic middle ear. Cer-
tainly the early land vertebrates had large heads, short necks, and short limbs,
implying that in fact the head was in close or often direct contact with the ground
and that sound and vibrational stimuli from the substrate thus had no problem
influencing the inner ear. Clack and Allin demonstrate that tympanic middle
ears have arisen a number of times independently in different lineages, a crucial
finding that makes it possible to understand the great variety of inner-ear struc-
tures and the parallel developments that they show.
Before tympanic middle ears arose, the land vertebrates had already diversi-
fied into a number of different lineages. Existing alongside the amphibians,
several lineages had arisen from the stem reptiles, the lepidosaurs, the archo-
saurs, and the mammal-like reptiles that later gave rise to the mammals. The
lack of a tympanic middle ear as we now know it probably meant that during
those periods of time, selection pressures for the development of larger and more
complex inner-ear hearing epithelia were missing or weak. It is apparent that,
while the amniote descendants of the stem reptiles all inherited a rather simple
hearing papilla largely supported by the basilar membrane, the ancestors of
modem amphibians developed two separate epithelia. As Smotherman and Na-
rins describe in Chapter 6, it is possible, perhaps even probable, that strictly
speaking, neither of these epithelia is homologous with the basilar papilla of
amniotes (in spite of one of them bearing the same name). Nonetheless, as
