Table Of ContentHandbook
of
Sensory Physiology
Volume 11113
Editorial Board
H. Autrum . R. Jung . W. R. Loewenstein
D. M. MacKay· H. L. Teuber
Electroreceptors and
Other Specialized Receptors
in Lower Vertrebrates
By
T.H. Bullock· A. Fessard· P.H. Hartline' Ad. J. Kalmijn
P. Laurent· R. W. Murray' H. Scheich . E. Schwartz' T. Szabo
Edited by
A. Fessard
With 118 Figures
Springer-Verlag Berlin· Heidelberg. New York 1974
ISBN-13: 978-3-642-65928-7 e-ISBN-13: 978-3-642-65926-3
DOl: 10.1007/978-3-642-65926-3
This work is subject to copyright. All rights are reserved, whether the whole or part of the materials is concerned,
specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying
machine or similar means, and storage in data banks.
Under § 54 of the German Copyright Law where copies are made for other than private use, a fee is payable to
the publisher, the amount of the fee to be determined by agreement with the publisher. © by Springer-Verlag
Berlin' Heidelberg 1974.
Softcover reprint of the hardcover 1st edition 1974
Library of Congress Cataloging in Publication Data. Fessard, Alfred. Electroreceptors and Other Specialized
Receptors in Lower Vertebrates. (Handbook of Sensory Physiology, V. III/3) Bibliography: p. Contents:
Bullock, T. H. General Introduction. Szabo, T. Anatomy of the Specialized Lateral Line Organs of Electro-
reception. Fessard, A .. Szabo, T. Physiology of Electroreceptors. Murray, R. W. The Ampullae of Lorenzini.
Kalmijn, Ad. J. The Detection of Electric Fields from Inanimate and Animate Sources Other Than Electric Organs.
Scheich, H., Bullock, T. H. The Detection of Electric Fields from Electric Organs. Schwartz, E. Lateral-Line
Mechano-Receptors in Fishes and Amphibians. Laurent, P. Pseudo branchial Receptors in Teleosts. Hartline, P. H.
Thermoreceptors in Snakes.
1. Electroreceptors. 2. Neural Receptors. I. Fessard, Alfred. II. Title. III. Series. [DNLM: 1. Mechanoreceptors.
2. Receptors, Neural. 3. Thermoreceptors. WL700 H236 v. 3 pt. 3] QP351.H34 Vol. 3, no. 3 [QP369] 591.1'82'08s
[596'.01'88] 74-13982
The use of general descriptive names, trade names, trade marks, etc. in this publication, even if the former are
not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and
Merchaudise Marks Act, may accordingly be nsed freely by anyone.
Preface
The originality of this volume is to reveal to the reader the fascination of some
unfamiliar sensory organs that are sometimes ignored and often misunderstood.
These receptors have only recently been identified and their functional specificity
is in some cases still a matter for discussion. The four classes of sensory organs
considered here differ widely from one another in many respects. One might even
say that the only thing they have in common is that they belong to cold-blooded
vertebrates. These classes are:
1. the directionally sensitive lateral-line mechanoreceptors of fishes and amphi-
bians (Chapter 7);
2. the pseudobranchial organs of some teleosts, equipped with pressoreceptors and
at least three other types of receptors (osmo- and chemoreceptors) (Chapter 8);
3. the infrared-sensitive pit organs of some snake families (Chapter 9) ;
4. the various kinds of electroreceptors found in several marine and freshwater
fish families (Chapters 2 to 6).
The first three classes of receptors mentioned above thus rate only one chapter
each, whereas five chapters are devoted to the electroreceptors. Electroreception
has aroused enormous interest among physiologists in specialties ranging from
molecular biology to animal behavior. The resulting quantity of research and
discussion fully justifies this disproportion. However, it cannot be denied that the
contents of the volume must appear unbalanced and heterogeneous, yet it should
not be perceived as a mere juxtaposition of particular and unrelated cases.
On the contrary, the attentive reader will soon discover that this very hetero-
geneity is a source of. enrichment. The juxtaposition itself reveals the general
principles and properties that are common to all these seemingly unrelated ex-
amples of sensory physiology. This point of view is illustrated in several ways by
BULLOCK in his General Introduction (Chapter 1); for instance, he considers the
general question of a biological definition valid for any sensor as well as how to
decide "its proper designation in a given case". Moreover, such studies require in
general a combination of behavioral, physiological and biophysical methods, as
exemplified in our chapters, but the predominant and unifying concept is cer-
tainly that of information. Information provides a common language in which to
express the general operations of coding the significant characteristics of the
stimulus and of processing the nervous messages within the central nervous
system. Conversely due recognition of general properties cannot but lead to a
more accurate definition of specific features. Comparative sensory physiology can
thus profit from this juxtaposition of quite different sensory organs.
The domain of electroreception is unique. On the one hand, its specific stimulus
is a universal agent of excitation and its differentiating properties depend primarily
- but not exclusively - on very low thresholds in the lateral-line receptors, as
was established by early investigators. On the other hand, electrosensitivity, which
Preface
was initially studied in a few species of electric teleosts, has been found to extend
to an increasing number of genetically alien fish families, some equipped with an
electric organ and others not. Knowledge of this diversification was accompanied
by the recognition of differentiating features in the anatomical macro- and micro-
structures, as well as in the biophysical mechanisms involved. The study of the
role of electroreceptors in the animal's life caused a distinction to be made between
various types of environmental conditions in relation to different behavioral ends.
This was the revelation of an unexpectedly wide diversity, progressively disclosed,
and most probably still concealing further surprises.
The preceding discussion was necessary to explain why it was impossible to
deal with such rich material without distributing it over several chapters, accord-
ing to our major subdivisions. The various chapters were entrusted to six com-
petent, but differently oriented specialists. The editor has done his best to co-
ordinate their contributions without discarding diverging viewpoints and even
contradictory statements. We hope that such a presentation may spur research
workers on to renewed efforts. Similarly, no attempt has been made to exclude
concordant or identical data or explanations by two (or more) different authors.
Apart from the fact that a certain redundancy cannot be avoided when each
aspect of an organic whole is considered separately, this repetition helps toward
a better understanding of the most difficult themes, for example, themes involving
the concepts of physics used in electricity, which are not familiar to biologists in
general.
We hope this volume will attract the attention not only of specialized physi-
ologists, but also of general neurophysiologists, biophysicists and specialists in
information theory, and, at the highest levels of integration, psychobiologists and
ecologists. We think it should interest advanced graduate students in search of an
original orientation. We would recommend such readers to tackle the last three
chapters first, as they are more limited in scope although there are still plenty of
unsolved problems.
As editor, I would like to express my sincere thanks to all my collaborators.
Each of them, with his special material and his own style, has contributed to the
originality of the work.
I owe a particular debt of gratitude to Dr. Bullock for his invaluable help with
my editorial tasks and his unstinting advice during the long period of painstaking
elaboration of the volume.
In view of the length of this period, I must not forget to mention the patience
and efficiency of our publisher, Springer-Verlag.
Paris, September 1974 A. E. FESSARD
Contents
Chapter 1 General Introduction. By T. H. BULLOCK 1
Electroreceptors in the Teleost
Chapter 2 Anatomy of the Specialized Lateral Line Organs of
Electroreception. By T. SZABO. With 24 Figures 13
Chapter 3 Physiology of Electroreceptors. By A. FESSARD and
T. SZABO. With 47 Figures. . . . . . . . . . . 59
Electroreceptors in the Elasmobranch
Chapter 4 The Ampullae of Lorenzini. By R.W. MURRAY. With
5 Figures . . . . . . . . . . . . . . . . . . . . 125
The Role of Electroreceptors in Animal's Life
Chapter 5 The Detection of Electric Fields from Inanimate and
Animate Sources Other Than Electric Organs. By Ad. J.
KALMIJN. With 5 Figures . . . . . . . . . . . . . 147
Chapter 6 The Detection of Electric Fields from Electric Organs.
By H. SCHEICH and T.H. BULLOCK. With 12 Figures. . 201
Other Specialized Receptors
Chapter 7 Lateral-Line Mechano-Receptors in Fishes and Amphi-
bians. By E. SCHWARTZ. With 6 Figures ....... 257
Chapter 8 Pseudobranchial Receptors in Teleosts. By P. LAURENT.
With 20 Figures . . . . . . . . . . . . . . . . . 279
Chapter 9 Thermoreceptors in Snakes. By P.H. HARTLINE. With
8 Figures 297
Author Index 313
Subject Index 321
List of Contributors
BULLOCK, THEODORE H.
Department of Neurosciences, University of California at San Diego, La Jolla,
California 92037, USA
FESSARD, ALFRED
Laboratoire de Neurophysiologie Generale, Station de I'Institut Marey, 4,
Avenue Gordon-Bennett, Paris 16e, France
HARTLINE, PETER H.
Department of Physiology and Biophysics, University of Illinois at Urbana-
Champaign, 524 Burrill Hall, Urbana, Illinois 61801, USA
KALMIJN, AD. J.
Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543,
USA
LAURENT, P.
Laboratoire des Applications Biologiques, Centre National de la Recherche
Scientifique, B.P. 20 CR, 67037 Strasbourg Cedex, France
MURRAY, R. W.
Department of Zoology and Comparative Physiology, University of Bir-
mingham, P.O. Box 363, Birmingham 15, Great Britain
SCHEICH, HENNING
Max-Planck-Institut fiir biophysikalische Chemie, 34 Gottingen-Nikolausberg,
Am Fassberg, West Germany
SCHWARTZ, E.
II. Zoologisches Institut der Justus Liebig-Universitat, 63 Giessen, Wart-
weg 95, West Germany
SZABO, T.
Department of Neurophysiologie Sensorielle Comparee, Laboratoire de Physio-
logie Nerveuse CNRS, 91190 Gif sur Yvette, France
Chapter I
General Introduction
An Essay on the Discovery of Sensory Receptors and
the Assignment of their Functions Together with an
Introduction to Electroreceptors
By
THEODORE H. BULLOCK, La Jolla, California (USA)
Addition to the known roster of sense receptors, not merely of a new organ or
example but of a new class or major modality, is a rare event. The prediction,
discovery, and establishment of electroreceptors is a case history of extreme
interest not only for the intrinsic insight into the life of some lower vertebrates
that see the world through a new sellse but also for the lessons it teaches about
identifying and classifying receptors by function. This may be the most useful
way to introduce a section on specialized receptors in lower vertebrates.
Our knowledge in this category-by-exclusion (really receptors-not-elsewhere-
treated) is remarkably limited. The fascination of the cases dealt with in the
following chapters, each something of a surprise in the framework of familiar
mammalian physiology, should not obscure that fact. We really do not know the
big picture in lower vertebrates with respect to the elementary generalities about
thermoreception, proprioception, mechanoreception, nociception, or general
chemical or visceral afferent reception to name some of the modalities exclusive
of the "special senses." To be sure there has been an impressive series of discoveries
of new sense organs in lower forms in recent years, far more than the general
reader may have noticed. But the lower vertebrates have received less attentIOn
in this respect than the invertebrates.
The important conclusion of both lines of evidence - the surprising discoveries
reviewed in the following chapters, and the large areas of terra incognita that
remain should be a word to the wise: there's gold to be mined in this vein.
How is such gold discovered? How may we expect new receptors to be found, and
why is it safe to predict surprises, especially in sensory physiology?
New receptors have been found in the past according to several scenarios.
(a) One successful approach has been curiosity about the function of a known
structure, as in the instances of baroceptors and chemoreceptors in the carotid
body, the infrared receptors of the rattlesnake facial pit (HARTLINE, Chapt. 9,
this volume), the lateral line mechanoreceptors (SCHWARTZ, Chapt. 7, this
Vol.) and the pseudobranchial interoceptors (LAURENT, Chapt. 8, this Vol.),
as well as many invertebrate organs.
1 Hb. Sensory Physiology. Vol. III/3
2 T. H. BULLOCK: General Introduction
(b) Another method, which has made conspicuous additions to our knowledge
is serendipitous - the chance encounter while recording electrophysiologically
for other purposes. There may be more instances than we know, but good examples
are the J-receptors for lung congestion in the cat (PAINTAL, 1970), chemoreceptors
in the lateral line of some fish (KATSUKI and HASHIMOTO, 1969), photoreceptors
in the last abdominal ganglion of crayfish (PROSSER, 1934), and in the siphon
nerves of the clam, Spisula (KENNEDY, 1960).
(c) A more difficult and rarer approach is the search for a basis for some
behavioral response not accounted for by familiar receptors. This was the route
by which electroreceptors were identified and it may be in this respect nearly a
unique case history. Besides its own interest, having drama, suspense and a moral
or two, it is worthwhile to review this story since there are other outstanding
puzzles where behavioral accomplishment calls for unknown receptors - or for
non-nervous mediation! Examples, ranging widely in general acceptance, include
the responses to hydrostatic pressure in species without gas volumes (ENRIGHT,
1962), to magnetic fields of the same order of strength as the earth's (WILTSCHKO,
1972; LINDAUER, 1972; BROWN, 1960, 1962, 1966) and to caloric value of food
(JACOBS and SHARMA, 1969).
Actually the identification and establishment of electroreceptors took place in two
parallel streams of investigations only recently converging, but doubtless mutually
reinforcing by intangible influences on the scientists concerned. One stream will
be our entry because it is a classic in relation to the fundamental question: "How,
in general, can the modality and proper designation of a receptor be established 1"
This is a highly appropriate issue to face in the introduction to a series of chapters
on relatively unfamiliar organs.
Accepting the prevailing system which denotes receptors according to the
presumed adequate stimulus, we have broad classes such as photo-, mechano-,
thermo-, and chemoreceptors and, at least in higher animals, nociceptors. Sub-
classes, especially of mechanoreceptors are recognized, such as phono-, vibration-,
static position-, joint position-, acceleration-, stretch-, pressure-, tactile-, and
rheo-receptors. How do we decide the proper designation in a given case? This
apparently simple, even innocent question is not only difficult in principle; it is
rarely considered seriously.
The usual approximation appears to satisfy, namely that the form of stimulus
to which a sense organ is most sensitive must be its normal adequate stimulus. The
obvious impossibility of comparing sensitivities to angular acceleration, molar
concentration, and degrees Celsius does not attract discussion and the implicit
position seems to be that extremely high sensitivity - relative to human sensation,
is easily distinguished from extremely high threshold using the same basis. While
this may suffice for some modalities like photoreceptors, which in addition offer
accessory structures like the cornea, lens and iris as hints of the adequate stimulus,
it hardly suffices for most receptors.
It will be our contention that in general (barring special cases such as well
developed eyes and ears) neither physiological nor anatomical methods can satis-
factorily establish the modality of sense organs but only a combination of physio-
logy and behavior.
General Introduction 3
The proper designation of a receptor, which identifies its adequate stimulus
(or stimuli, in the common event of limited ambiguity), requires evidence, either
(a) that the receptor initiates neural signals only with one form of stimulus among
those normally available (this requires knowledge of habit of life), or (b) that the
receptor may respond to more than one but the animal responds with adaptive
behavior as though a certain stimulus had impinged, or (c) that normal behavioral
responses can occur under conditions restricting the stimulus to one form and
permitting the reception to be attributed to the sense organ in question. In short,
an x-receptor must be shown to be an organ from which the animal under natural
conditions obtains biologically significant information from x-al stimuli.
The ampullae of Lorenzini are abundant, specialized skin sense organs charac-
teristic of sharks and rays (MURRAY, Chapt. 4; KALMIJN, Chapt. 5, this Vol.).
Long known and studied histologically, their function had been moot since
the last century.
With the elegant findings of SAND (1938) that they respond to temperature in
an impressive way - not only to mere tenths of a degree, but with an apparently
specialized negative coefficient (increased firing to cooling) for the initial, phasic
discharge, it was generally accepted that ampullae of Lorenzini are thermo-
receptors. HENSEL (1955) confirmed this, emphasized the similarities to mam-
malian cutaneous thermoreceptors and agreed with SAND that they are not
mechanically sensitive. But doubts crept in, whether they are normally signalling
temperature or are perhaps incidentally temperature sensitive. Other cases are
known with a high temperature coefficient giving some ambiguity to the appar-
ently adequate stimulus of some other modality. For one thing the specialized
anatomy, with long canals, is not explained by a thermoreceptor function. New
findings by MURRAY (1960) and LOEWENSTEIN (1960) that these organs respond
to pressure applied by cannulation at least in dissected preparations, led to the
suggestion that they are after all mechanoreceptors. But this too raised doubt.
They are not as sensitive as the ordinary lateral line receptors. It seems improbable
that there is ever a source of sufficient distortion in the normal life of sharks and
rays, except- or even-by their own body movements. Proprioception seemed
unlikely - as an explanation of the elaborate array of specialized tubes.
Next came the intriguing new results of MURRAY (1962) that dilution of sea
water by as little as 3% will cause a signal in ampullary afferents. A function in
detecting sudden salinity change was contemplated, although without evidence
of behavioral response or of a general importance of the required abrupt stimulus
in the life of elasmobranchs as a group. LOEWENSTEIN and ISHIKo (1962) found
an increase in impulse frequency arising from an ampulla when the sodium
chloride concentration in the sea water outside the pore was increased by as little
as 0.5% (2 mM). This is similar to the sensitivity of some taste and hypothalamic
osmoreceptors and they conclude that a "chemo-receptor process of high sensitiv-
ity mediated through an electrical mechanism" is present without resolving
however the question of the physiological role of the ampullae. MURRAY (1960,
1962) had also shown a responsiveness to electric current but doubted that ampullae
are used either to detect electric organ discharges or to aid in navigation and
instead suggested the salinity detection is electrical. DIJRGRAAF and KALMIJN
(1962, 1963) favored an electroreceptive function of the ampullae of Lorenzini,
1*
