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 ScienceBusiness 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 ScienceBusiness 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, especially in its peripheral and central histological basis. 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 research. 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 editors 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 processing with the auditory system. Thus, the series editors concluded that investigators 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 electroreception 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 electrosensory 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 that use high-frequency systems. Finally, Nelson (Chapter 11) analyzes target detection and provides models to help understand how electroreceptive fishes are able to analyze the information they are sensing. In the remaining chapters, authors consider several additional and important topics that help in understanding electrosensory systems. It has long been held that the electrosensory and lateral line senses are phylogentically related, and this, as well as functional similarities and differences, are considered in Chapter 12 by Coombs and Montgomery. In Chapter 13, Albert and Crampton describe how molecular techniques are used to explore the systematic relationships among and between electrosensory fishes. Finally, in Chapter 14, Caputi, Carl- son, and Macadar explore how the organs that emit electric signals are controlled by the central nervous system.

Theodore H. Bullock, La Jolla, California Carl D. Hopkins, Ithaca, New York Arthur N. Popper, College Park, Maryland Richard R. Fay, Chicago, Illinois Contents

Volume Dedication ...... v Chapters Dedication...... vii Series Preface ...... ix Volume Preface ...... xi Contributors ...... xv

Chapter 1 Explaining Electroreception ...... 1 Theodore H. Bullock and Carl D. Hopkins

Chapter 2 From Electrogenesis to Electroreception: An Overview . . 5 Gu¨ nther K.H. Zupanc and Theodore H. Bullock

Chapter 3 Morphology of Electroreceptive Sensory Organs...... 47 Jørgen Mørup Jørgensen

Chapter 4 Central Neuroanatomy of Electrosensory Systems in Fish ...... 68 Curtis C. Bell and Leonard Maler

Chapter 5 Ontogeny of Electroreceptors and Their Neural Circuitry ...... 112 R. Glenn Northcutt

Chapter 6 The Physiology of Low-Frequency Electrosensory Systems ...... 132 David Bodznick and John C. Montgomery

Chapter 7 Physiology of Tuberous Electrosensory Systems...... 154 Masashi Kawasaki

Chapter 8 Plasticity of Sense Organs and Brain...... 195 Joseph Bastian and Harold H. Zakon

xiii xiv Contents

Chapter 9 Behavior of Animals with Passive, Low-Frequency Electrosensory Systems ...... 229 Lon A. Wilkens and Michael H. Hofmann

Chapter 10 Passive Electrolocation and the Sensory Guidance of Oriented Behavior ...... 264 Carl D. Hopkins

Chapter 11 Target Detection, Image Analysis, and Modeling ...... 290 Mark E. Nelson

Chapter 12 Comparing Octavolateralis Sensory Systems: What Can We Learn? ...... 318 Sheryl Coombs and John C. Montgomery

Chapter 13 Diversity and Phylogeny of Neotropical Electric Fishes (Gymnotiformes) ...... 360 James S. Albert and William G.R. Crampton

Chapter 14 Electric Organs and Their Control ...... 410 Angel Ariel Caputi,Bruce A. Carlson, and Omar Macadar

Index ...... 453 Contributors

james s. albert Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA joseph bastian Department of Zoology, University of Oklahoma, Norman, OK 73019, USA curtis c. bell Neurological Sciences Institute, Oregon Health Sciences University, Beaverton, OR 97006, USA david bodznick Department of Biology, Wesleyan University, Middletown, CT 06459-0170, USA theodore h. bullock Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, CA 92093-0240, USA angel ariel caputi Department of Comparative Neurophysiology, Instituto de Investigaciones Bio- lo´gicas Clemente Estable, CP 11600 Montevideo, Uruguay bruce a. carlson Department of Biology, University of Virginia, Charlottesville, VA 22904, USA sheryl coombs Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43402, USA william g.r. crampton University of Florida, Gainesville, FL 32611-7800, USA

xv xvi Contributors michael h. hofmann Institute of Zoology, University of Bonn, 53115 Bonn, Germany carl d. hopkins Department of Neurobiology & Behavior, Cornell University, Ithaca, NY 14853, USA jørgen mørup jørgensen Department of Zoophysiology, University of Aarhus, DK 8000 Aarhus C, Denmark masashi kawasaki Department of Biology, University of Virginia, Charlottesville, VA 22904, USA omar macadar Department of Neurophysiology, Instituto de Investigaciones Biolo´gicas Cle- mente Estable, CP 11600 Montevideo, Uruguay leonard maler Department of Cell and Molecular Medicine, University of Ottawa, Ottawa, ON K1H 8M5, Canada john c. montgomery Leigh Marine Laboratory and School of Biological Sciences, University of Auckland, Auckland 1020, New Zealand mark e. nelson Beckman Institute, University of Illinois, Urbana, IL 61801, USA r. glenn northcutt Neurobiology Unit, Scripps Institution of Oceanography, and Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, CA 92093-0240, USA lon a. wilkens Center for Neurodynamics, Department of Biology, University of Missouri–St. Louis, St. Louis, MO 63121, USA harold h. zakon Section of Neurobiology, University of Texas, Austin, TX 78712, USA gu¨ nther k.h. zupanc School of Engineering and Science, International University Bremen, D-28725 Bremen, Germany 1

Explaining Electroreception

Theodore H. Bullock and Carl D. Hopkins

What is electroreception? It may call to mind stories about ambiguous confer- ence titles that invite speculation by guests in the hotel elevator, or a column in the paper about microchips implanted under the skin, or some new-fangled weapons control. It has a more interesting history than any of these, however. In the early 1950s there was no such term or phenomenon to be named. Then Harry Grundfest in New York, collaborating with an aquarist with unusual tropical fish, became curious about the many species of tropical New World fish related to the familiar electric eel, which can discharge pulses of hundreds of volts. He found that relatively tiny cousins—smaller than a pencil—are dis- charging small fractions of a volt all the time. The old German literature had shown they have electric organs, but very small ones, called pseudoelectric organs. What can they do with such feeble, sustained discharges? Some species are going at several hundred pulses per second, night and day. So far, there was no reason to suspect a new sense modality. No functions had been discovered and the research being done was effector centered. Then Hans Lissmann at Cambridge (on the Cam) thought up a key experiment. By now it was known that another large order of freshwater fishes in Africa (mormyriforms) is all electric, meaning that all species tested have electric organs and they discharge pulses all the time. Hans kept a few of the large, eel-like Gymnarchus long before they became readily available and patiently taught them that certain objects mean food. He found (Lissman and Machin 1958) that the fish can dis- criminate between a porous porcelain container with aquarium water and one in which 20% of the liquid is distilled water—and that discrimination could not have been possible by chemical, mechanical, or visible clues but must have been the result of electrical conductivity of the fish’s maintained 300-Hz sinusoidal discharges! Here then was strong evidence for an object-detection function re- quiring fantastic sensitivity to small differences in the local intensity of the fish’s field in the surrounding water. Hence a sensory system was necessary, specialized for high sensitivity—electroreceptors! Mo¨hres (1957) in Tu¨bingen soon showed evidence of a social communicating function as well, using another mormyriform fish, Gnathonemus, that changes the repetition rate of its brief

1 2 T.H. Bullock and C.D. Hopkins pulses drastically to stimuli of ethological interest such as the proximity of a conspecific fish. We now had, not simply a function for the puny electric organs, but two classes of functions: object detection and social communication, but no details about either one. The kinds of questions raised by this level of discovery were: What is the code for one’s own electric organ discharge (EOD) and for the neighbor’s? How does a fish tell one from the other? What is the repertoire of signals that any individual of the species would understand? Where and how, in the brain, are these signals generated after the preceding signal had been read and interpreted? At this point in the narrative we are into the 1960s and well into the phenomenon of electroreception in a few favorable species of the New World, tropical gymnotiforms. Descriptive natural history was still important and determined which species and behaviors to study. We had learned that among the species there were “wave fish” and “pulse fish”—species whose EOD, when converted from electricity into sound, is a quasisinusoidal, steady tone, in the range from about 200 to 2000 Hz, the intervals between single EODs quite uniform and about equal to the duration of the discharge versus those species with much less frequent EODs, long and irregular intervals, making sputtering sounds usually between 1 and 100 Hz, when the electric signal is sent to a loudspeaker. We had learned that each individual of the wave species has its own preferred EOD frequency, maintained over hours and days, but under brain control and labile to special stimuli, whereas pulse species are not obviously individual; are very low in repetition rate at rest; and easily, widely, speeded up by many stimuli, among them EODs of other individuals, manifesting the communicative function. We had learned that sharks, rays, and catfish show electroreception of slowly changing electric currents, less than 20 Hz, even in species that lack EODs and electric organs—opening the general question of which other fishes or taxa might have this sensory modality. This was answered some decades later: quite a number of nonteleost taxa have it, including lampreys, ratfish, lungfish, stur- geons, and paddle fish, even some salamanders. Reciprocally, some teleosts with electric organs and presumably functional EODs, such as the stargazers (Ura- noscopids), seem to lack the sense modality. We are not through with natural history, either in the phylogenetic distribution or in the functional uses of electroreception. For years we were pessimistic about identifying the sense cells or sensory organs. Skin senses, such as touch, tickle, pain, cold, and heat, have been worked out only slowly and haltingly in the most frequently studied forms— laboratory mammals. Electrophysiological recordings showed the afferent nerve fibers must be in certain branches of the lateral line nerve, most numerous on the head. Suspected were the ampullae of Lorenzini, characteristic of elasmo- branchs and a few other taxa and with a checkered history of functional assign- ment (Bullock 1974). Kalmijn (1974) provided the crucial evidence that in fact these ampullae are quite specialized electroreceptors, and although they can re- 1. Explaining Electroreception 3 spond to cold and to some mechanical events, these responses are adventitious and unusual in nature. Somewhat similar organs occur in catfish and other species but on substantial grounds are not considered homologous. I (T.H.B.) well remember the day when, with my co-worker, Shiko Chichibu, we encoun- tered for the first time, in a gymnotiform fish at the Goeldi Museum in Belem, an afferent unit that was sensitive to electrical events but fired at a frequency unrelated to the frequency of the stimulus, which had to be low (below 30 Hz) and could be simply the DC field around a freshly killed fish—similar to the class of non-Lorenzini receptors in siluriforms (catfish). Another whole line of sense organs apparently evolved in the teleosts with electric organs and EODs, called tuberous organs. They typically respond to fast or brief electrical events, up to components of several kiloHerz, whereas the ampullary organs, of both the elasmobranch type and the siluriform type, respond to low-frequency components, best below 5 Hz. The tuberous receptors are specialized into subcategories, usually two in each species, differing in the dynamics of response and hence in their functional roles. This is the “bottom line” of a long series of researches, with surprises and repeated “Ah, so’s.” The variety of sense organs bespeaks a corresponding com- plexity in central connections and maplike representations, funneling toward a midbrain of higher neurons with rather complex input requirements for firing— relatively high-level “recognition units” as well as circuits that reduce the sensitivity to signals coming from the animal’s own movements. Each of these topics and ancillary ones has had a dramatic history of discoveries and is developed in the chapters that follow in this volume. They are all incompletely understood and are ready for another advance in understanding, which usually means a bit more adequate description at the next lower level—cellular, membrane, or molecular and sometimes at a higher level, such as circuit, as- semblage, topographic, or algorithmic, leading to behavioral, ethological, and ecological levels. In addition to these developments in the chain of integrative levels of orga- nization and function, there are striking contributions to the “whence” class of questions—the ontogeny within each taxon and the evolution among taxa. Each has benefited from dramatic steps such as learning how to keep and to breed some species, how to raise young fish of each group, and how to supply modern techniques for DNA analysis. Many of the findings explaining electroreception impinge on broad questions in general biology, for which these fish provide especially favorable exemplars. One chapter deals, not with electroreceptors, but with the electric organs and the EODs as the signals for sensory analysis, their fields, and their control, synchrony, and modulation. Convergent and parallel evolution are illustrated as well as species diversity and adaptive specialization. The field is still young, so that instead of a wide choice of authors, the writers of each chapter tend to be world authorities pioneering on their respective fronts.