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Springer Handbook of Auditory Research Series Editors: Richard R. Fay and Arthur N. Popper Theodore H. Bullock Carl D. Hopkins Arthur N. Popper Richard R. Fay Editors Electroreception With 118 illustrations and two color illustrations Theodore H. Bullock Carl D. Hopkins Department of Neurosciences Department of Neurobiology & Behavior School of Medicine Cornell University University of California, San Diego Ithaca, NY 14583, USA La Jolla, CA 92093-0240, USA [email protected] [email protected] Arthur N. Popper Richard R. Fay Department of Biology Parmly Hearing Institute and Department University of Maryland of Psychology College Park, MD 20742, USA Loyola University of Chicago [email protected] Chicago, IL 60626, USA [email protected] Cover illustration: Gymnotiform fishes from South America utilize electroreception for passive sensing of prey, for active sensing objects detected as distortions in their own electric fields, and for sensing electric communication signals generated from their electric organs. A few of the 27 known genera of gymnotiforms are illustrated: Electrophorus, Gymnotus, Microsternarchus, Brachyhypopomus, Hypopomus, Racenisia, Hypopygus, Steatogenys, Rhamphichthys, and Gym- norhamphichthys (see J.S. Albert and W.G.R. Crampton, p. 364, for key). Library of Congress Cataloging-in-Publication Data Electroreception / Theodore H. Bullock (editor)...[etal.] p. cm. Includes bibliographical references and index. ISBN 0-387-23192-7 1. Electroreceptors. I. Bullock, Theodore Holmes. QP447.5.E44 2005 573.8'7—dc22 2004057843 ISBN 10: 0-387-23192-7 Printed on acid-free paper ISBN 13: 978-0387-23192-1 ᭧ 2005 Springer ScienceϩBusiness Media, Inc. All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer ScienceϩBusiness Media, Inc., 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed in the United States of America. (EB) 987654321 SPIN 10941447 springeronline.com Volume Dedication This volume is dedicated to the memories of two true pioneers in the study of electroreception, Walter Heiligenberg and Thomas Szabo. The contributions that Walter and Tom made to our understanding of electroreception are truly mon- umental, and their discoveries, and those of the students and others they influ- enced, permeate this volume. Thomas Szabo (d. 1994) was the director of the Laboratory of Sensory Physiology at the CNRS in Paris. Along with many co-workers, Thomas was a pioneer in electroreception, espe- cially in its peripheral and central histological ba- sis. Thomas not only did wonderful work in the laboratory, but he also did extensive field work both in Africa and South America. Most impor- tantly, perhaps, he trained a long list of younger workers. Walter Heiligenberg (d. 1994) was a student of Konrad Lorenz and Hans-Jochem Autrum. Wal- ter began a career in behavioral physiology with insects and teleosts, switched to electroreception, and led a large group at the Scripps Institution of Oceanography who worked out the cells, path- ways, and physiology of the jamming avoidance response—probably the best-understood piece of vertebrate elective behavior. Chapters Dedication Each author in this volume dedicates his or her chapter to Theodore Holmes Bullock, a pioneer in the discovery of electroreception and a true champion for understanding the diversity of organisms that possess this wonderful sense. Many of us have worked in Ted Bullock’s laboratory in La Jolla or have col- laborated with him from afar. All of us are inspired by conversations with Ted and by his writing, his lectures, his letters, and his e-mails. He continues to excite, to instruct, and to urge us to rethink old ideas and replace them with new. Many of the topics and discoveries reported in our chapters were in some measure inspired or influenced by Ted’s papers, lectures, remarks, or comments. James S. Albert Joseph Bastian Curtis C. Bell David Bodznick Angel Ariel Caputi Bruce A. Carlson Sheryl Coombs William G.R. Crampton Richard R. Fay Michael H. Hofmann Carl D. Hopkins Jørgen Mørup Jørgensen Masashi Kawasaki Omar Macadar Leonard Maler John C. Montgomery Mark E. Nelson R. Glenn Northcutt Arthur N. Popper Lon A. Wilkens Harold H. Zakon Gu¨nther K.H. Zupanc vii Series Preface The Springer Handbook of Auditory Research presents a series of comprehen- sive and synthetic reviews of the fundamental topics in modern 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 ix Volume Preface This volume represents a slightly different approach for books in the Springer Handbook of Auditory Research—it is not about hearing. At the same time, this volume is about a major sensory system that has evolved multiple times in the history of the vertebrates and shares many similarities in detection and proc- essing with the auditory system. Thus, the series editors concluded that inves- tigators in the hearing sciences would value learning about the electrosensory system, and so they invited two of the world’s leaders in that field, Professor Theodore H. Bullock and Professor Carl D. Hopkins, to collaborate on this volume. Indeed, it is anticipated that future volumes in the SHAR series might cover other topics that, although not directly on the topic of hearing, could provide unique insights into sensory systems that could benefit those of us in the hearing sciences. This volume, like our recent volume on The Vestibular System (SHAR Vol. 19, 2004), is also unlike most other SHAR volumes. Rather than considering a small area within the hearing sciences, it takes a broader view and provides an overview that encompasses a field. Thus, this volume not only includes chapters on physiology, signal processing, receptors, and related topics but also gives the reader a broader historic, behavioral, and taxonomic overview of the field. In effect, someone reading this whole volume will understand not only how electroception works but also its evolution and how animals use electro- reception in their daily lives. The volume starts with a brief historic overview by Bullock and Hopkins (Chapter 1) that gives a personal understanding as to the earliest discoveries in this field. Chapter 2 by Zupanc and Bullock continues this historic perspective but also introduces the reader to the diverse species that produce and detect electric currents. Jørgensen (Chapter 3) provides an exciting overview of the receptors involved in electroreception, while Bell and Maler (Chapter 4) extend the system into the brain and explain the central anatomy and physiology of electroreception as well as potential parallels to the auditory system. In Chapter 5, Northcutt considers the ontogeny of the electric sense and provides a context within which one can view the evolution of electroreception in the vertebrates. Electrosensory systems can be “divided” into low-frequency and high- xi xii Volume Preface frequency types, and these different systems are considered in the next several chapters. In Chapter 6, Bodznick and Montgomery describe the physiology of low-frequency systems, while Kawasaki discusses the physiology of high- frequency systems in Chapter 7. After a discussion of plasticity in the electro- sensory system by Bastian and Zakon (Chapter 8), several subsequent chapters consider the behaviors of fishes with different types of electrosensory systems. In Chapter 9, Wilkens and Hofmann discuss the behavior of fishes with low- frequency systems, while in Chapter 10, Hopkins takes a parallel course with the behavior of fishes
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