The Sensory Physiology of Aquatic Mammals

340 Pages·2001·11.47 MB·English

by  Alexander Ya. Supin

THE SENSORY PHYSIOLOGY OF
AQUATIC MAMMALS
THE SENSORY PHYSIOLOGY OF
AQUATIC MAMMALS
by
Alexander Va. Supin
Vladimir V. Popov
Alia M. Mass
Severtsov Institute ofE cology and Evolution
oft he Russian Academy ofS ciences
SPRINGER SCIENCE+BUSINESS MEDIA, LLC
Library of Congress Cataloging-in-Publication Data
Supin, Alexander Ya.
The sensory physiology of aquatic mammalsl by Alexander Va, Supin, Vladimir V.
Popov, Alia M. Mass
p.cm.
Includes bibliographical references (p. ).
ISBN 978-1-4613-5658-5 ISBN 978-1-4615-1647-7 (eBook)
DOI 10.1007/978-1-4615-1647-7
I. Aquatic mammals-Physiology. 2. Senses and sensation. I. Popov, Vladimir V. II.
Mass, A.M. (Alia Mikhailovna) III. Title.
QL 713 .S86 2001
573.8'7195-dc21
2001022995
Copyright © 2001 Springer Science+Business Media New York
Originally published by Kluwer Academic Publishers in 2001
Softcover reprint of the hardcover 1st edition 2001
All rights reserved. No part of this publication may be reproduced, stored in a
retrieval system or transmitted in any form or by any means, mechanical, photo
copying, recording, or otherwise, without the prior written permission of the
publisher, Springer Science+Business Media, LLC.
Printed on acid-free paper.
CONTENTS
Preface ........................................................................................................... ix
Abbreviations ................................................................................................. xi
Chapter 1. INTRODUCTION ......................................................................... 1
1.1. General .................................................................................................... 1
1.2. Aquatic Mammals as Subjects of Experimental Studies ........................ 2
1.3. The Physical Properties of Water as a Sensory Medium ....................... 4
I .3.1 . Acoustics ..................................................................................... 5
1.3.2. Optics .......................................................................................... 6
1.4. Psychophysical Measurement Procedures .............................................. 8
1.4.1. The Operant Conditioning Method ............................................. 8
1.4.2. Conditioned Reflex ..................................................................... 9
1.4.3. The Statistical Basis for Threshold Evaluation .......................... 9
1.4.4. Data-Collection Procedures ...................................................... 17
Chapter 2. HEARING IN CETACEANS ..................................................... 19
2.1. Ear Morphology ..................................................................................... 20
2.1.1. Outer Ear and Middle Ear ......................................................... 20
2.1.2. Inner Ear and Peripheral Neurons ............................................. 23
2.2. Auditory Evoked Potentials in Cetaceans .............................................. 25
2.2.1. Intracranial Evoked Potentials .................................................. 25
2.2.2. Auditory Brainstem Responses (ABR) ..................................... 27
2.2.3. Noninvasively Recorded Cortical Evoked Responses .............. 34
2.2.4. Rhythmic Evoked Potentials ..................................................... 35
2.2.5. Contribution ofYarious Frequency Bands to ABR .................. 41
2.3. Evoked-Potential Procedures in Hearing Measurements ..................... 47
2.3.1. ABR Threshold Measurements ................................................. 47
2.3.2. EFR and RFR Threshold Measurements .................................. 50
2.4. Hearing Sensitivity and Frequency Range ............................................. 52
2.4.1. Psychophysical Data ................................................................. 52
2.4.2. Evoked-Potential Data .............................................................. 56
2.5. Temporal Resolution .............................................................................. 58
2.5.1. Psychophysical Studies ............................................................. 59
2.5.2. Dependence of ABR on Stimulus Duration .............................. 61
VI
2.5.3. ABR Recovery at Double-Click Stimulation ............................ 63
2.5.4. Gap-in-Noise Detection Measurements .................................... 69
2.5.5. Derivation of the Temporal Transfer Function of the
Auditory System ...................................................................... 73
2.5.6. Rhythmic Amplitude-Modulation Test and Modulation
Transfer Function .................................................................... 86
2.5.7. Rhythmic Click Test ................................................................. 92
2.6. Frequency Tuning .................................................................................. 98
2.6.1. Critical Ratios and Critical Bands ............................................ 98
2.6.2. Tuning Curves ......................................................................... 101
2.6.3. Notch-Noise Masking ............................................................. 121
2.6.4. Frequency-Discrimination Limens .......................................... 130
2.6.5. Frequency Resolving Power ................................................... 138
2.7. Sound-Intensity Discrimination ........................................................... 147
2.8. Directional Sensitivity, Spatial, and Binaural Hearing ...................... 150
2.8.1. Psychophysical Studies ........................................................... 150
2.8.2. Directional Sensitivity: Evoked-Potential Studies .................. 153
2.8.3. Binaural Hearing: Evoked-Potential Studies .......................... 158
2.9. Frequency-Temporal and Frequency-Spatial Interactions .................. 163
2.9.1. Temporal Interaction of Frequency-Colored Sound Pulses .. 164
2.9.2. Paradoxical Lateral Suppression ............................................. 169
2.9.3. Interaction of Directional and Frequency Sensitivity ............. 176
2.10. Sound-Conduction Pathways ............................................................. 180
2.11.Central Representation of the Auditory System ................................. 190
2.12. Implements to Echolocation .............................................................. 193
2.12.1. Hearing Frequency Range ..................................................... 193
2.12.2. Frequency Tuning and Temporal Resolution ........................ 194
2.12.3. Recovery Functions as a Basis of Invariant Perception of
Echo Signals .......................................................................... 196
2.12.4. Rippled Spectrum Resolution and Echolocation .................. 197
2.12.5. Frequency-Temporal Interactions ......................................... 198
2.12.6. Spatial Resolution ................................................................. 199
2.13. Summary ............................................................................................ 200
Chapter 3. HEARING IN PINNIPEDS AND SIRENIANS ....................... 205
3.1. Hearing in Pinnipeds ............................................................................ 205
3.1.1. Ear Anatomy ........................................................................... 206
3.1.2. Hearing Sensitivity and Frequency Range .............................. 206
3.1.3. Temporal Processing ............................................................... 210
3.1.4. Frequency Tuning ................................................................... 211
3.1.5. Intensity Discrimination .......................................................... 215
3.1.6. Directional Hearing ................................................................. 215
3.1 .7. Auditory Representation in the Cerebral Cortex .................... 216
3.1.8. Hearing Adaptation to Amphibious Lifestyle ......................... 218
3.2. Hearing in Sirenians ............................................................................. 219
3.2.1. Ear Morphology ...................................................................... 220
3.2.2. Psychophysical Audiogram ..................................................... 221
3.2.3. Evoked-Potential Data ............................................................ 222
3.3. Summary .............................................................................................. 226
vii
Chapter 4. VISION IN AQUATIC MAMMALS ....................................... 229
4.1. Vision in Cetaceans ............................................................................. 229
4.1.1. Eye Morphology ...................................................................... 229
4.1.2. Visual Abilities of Cetaceans: Psychophysical Studies .......... 241
4.1.3. Topographic Distribution of Retinal Gangl ion Cells .............. 245
4.1.4. Visual Projections to the Cerebral Cortex .............................. 260
4.2. Vision in Pinnipeds .............................................................................. 264
4.2.1. Eye Morphology ...................................................................... 264
4.2.2. Visual Abilities ofPinnipeds ................................................. 268
4.2.3. Topographic Distribution of Retinal Ganglion Cells and
Retinal Resolution ................................................................. 272
4.2.4. Visual Projections to the Cerebral Cortex .............................. 278
4.3. Vision in Sirenians ............................................................................... 279
4.3.1. Eye Anatomy and Retinal Structure ........................................ 279
4.3.2. Psychophysical Studies ........................................................... 281
4.3.3. Topographic Distribution of Ganglion Cells and Retinal
Resolution .............................................................................. 281
4.4. Summary .............................................................................................. 282
Chapter 5. SOMATIC SENSE IN AQUATIC MAMMALS ...................... 285
5.1. Somatic Sense in Cetaceans ................................................................. 285
5.2. Somatic Sense in Pinnipeds ................................................................. 287
5.2.1. Morphological and Psychophysical Data ................................ 287
5.2.2. Somatosensory Projections to the Cerebral Cortex ................ 288
5.2.2. Tactile Sensitivity of Vibrissae ............................................... 295
5.3. Summary .................................................................................... 297
References ................................................................................................... 299
Index ........................................................................................................... 325
PREFACE
This book is actually a product of efforts of many people, not only of the
authors.
W ide investigations of marine mammals began in Russia (that time, in the
former Soviet Union) in the 1960s when a few teams of enthusiasts founded
experimental stations intended for keeping dolphins and seals in captivity
and for performing experimental studies of these fascinating animals. It was
a time when attention of many people throughout the world was attracted to
dolphins and other marine mammals due to appearance of oceanariums and
dolphinariums, which demonstrated unique capabilities of these animals. So
scientists in many countries concentrated on studies of them. There was
much to learn about the morphology, physiology, and psychology of marine
mammals, and investigators spending their time and efforts on studies in this
field were rewarded by a number of surprising findings.
The authors of this book represent one of such research teams focused on
the neuro- and sensory physiology of marine mammals. A few decades of
studies naturally resulted in the idea to summarize in a book both the results
of these studies and a large body of data in adjacent fields. Our goal was to
synthesize the many research findings and the present knowledge on sensory
capabilities and mechanisms of sensory systems of aquatic mammals. We
realize, however, that the appearance of this book was made possible due to
the help and assistance of many colleagues.
First of all, it should be stressed that experimentation on marine mam
mals would be impossible without the collective participation of the entire
research team. Therefore, it is our pleasant duty to note the participation of
Vladimir Klishin, Tamara Ladygina, Olga Milekhina, Mikhail Tarakanov,
and Mikhail Pletenko in various parts of the studies described herein.
Keeping large animals in captivity is expensive and effort-consuming. It
would not have been possible for us if it were not for Administration of the
x Preface
Institute of Ecology and Evolution of the Russian Academy of Science,
headed initially by Professor Vladimir Sokolov and later by Professor Dmi
triy Pavlov. They always supported our projects and ideas. In recent years,
the Russian Foundation for Basic Research (RFBR) provided valuable
support for our studies. Most of our studies were carried out in the Utrish
Marine Station (the Black Sea coast) built purposefully for this type of
investigation; the extraordinary efforts of the scientific supervisor of the Sta
tion, our friend Lev Mukhametov, made possible the successful functioning
of this institution. We also received a lot of help from the Utrish Dophinar-
1U1l1.
Our understanding of the subject has been markedly enhanced due to dis
cussions with many colleagues in national and international scientific meet
ings. For these opportunities, we are very thankful to organizers of these
meetings, Whitlow Au, Nicolay Dubrovskiy, Ronald Kastelein, Patrick
Moore, Paul Nachtigall, Eugeniy Romanenko, Jeanette Thomas, and many
others.
We have to note that the idea to write this book was put forward by Mi
chael Myslobodsky, who encouraged us to submit the book project to Klu
wer Academic Publishers. The attitude of the Kluwer's staff, particularly
Molly Taylor and Melinda Paul, who did not hesitate to deal with authors
from a country so far from their home, and Rosemary Winfield, who care
fully edited the manuscript, is greatly appreciated.
So there are many people who we are indebted to. We hope they are not
disappointed by the final product.
Alexander Supin
Vladimir Popov
AUa Mass
ABBREVIATIONS
ABR Auditory brainstem re- lID Interaural inten-
sponse sity difference
ACF Autocorrelation function ILD Iinteraural latency differ-
ACR Auditory cortical response ence
AM Amplitude modulation lSI Interstimulus interval
ANR Auditory nerve response ITD Interaural time delay
AP [Cochlear] Action potential MAA Minimal audible angle
CCF Cross-correlation function MTF Modulation transfer func-
EFR Envelope-following re- tion
sponse PND Pposteronodal distance
EP Evoked potential RFR Rate-following response
ERB Equivalent rectangular RMS Root-mean-square
bandwidth ROC Receiver operation charac
ERD Equivalent rectangular teristic
duration Roex Rounded exponential func
ERG Ee Ie ctroreti no gram tion
FM Frequency modulation SAM Sinusoidal amplitude modu
FFR Frequency following re- lation
sponse TSP Time separation pitch
FRP Frequency resolving power
Chapter 1
INTRODUCTION
1.1. GENERAL
Comparative studies of sensory systems in animals adapted to various living
conditions reveal unknown abilities of sensory systems, aid our understand
ing of the mechanisms of perception and information processing, and extend
our knowledge of animal behavior and orientation. It is no surprise that a
number of researchers who worked for many years on traditional laboratory
animals and made major contribution to basic neuro- and sensory physiology
turn their attention to studies of exotic species that were not usual subject of
study for physiologists. As well as yielding factual data on the functional
basis of sensory systems, this approach provides a better understanding of
several aspects of evolution. In particular, there is a great interest in the sen
sory systems of such a specific group of animals as aquatic mammals.
Aquatic mammals differ from most terrestrial ones not only in their life
style in the aquatic environment. From the point of view of phylogeny, they
are specific groups (orders) of mammals that evolved independently of other
orders during tens millions of years. Some tasks that sensory systems en
counter were evolutionarily solved in these animals in other ways than in
terrestrial mammals. Therefore, they provide opportunities for fuller knowl
edge of mammalian sensory mechanisms.
There are several excellent books addressing the sensory systems of
aquatic mammals (Busnel and Fish, 1980; Nachtigall and Moore, 1988;
Thomas and Kastelein, 1990; Thomas et a!., 1992; Kastelein et a\., 1995).
Unfortunately, all of them are contributed books composed of separated arti
cles, so they do not present systematically the situation in the sensory physi-