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FOREWORD
How profoundly human it is, how deeply characteristic of a foreword writer, I would like to underline some
of our species—ethologically speaking—to wonder of the features of special importance in Günther
at, study, and investigate behavior of our own and Zupanc’s treatment, without implying that they are
other species toward understanding, in the sense neglected in previous books.
of accounting for, the actions, the appetites, the First and foremost, it is a feature of the subject
drives, alternative modes, and sensory guidance that that it deals with biodiversity in the extreme. The
we observe. How rewarding we find it to think of consequence of evolution is an accumulation
hypotheses, to test and discard them, and to achieve of diversity, particularly in behavior—more
a degree of understanding—at one or more levels— conspicuously and significantly, and more inviting to
and report it to our colleagues. analysis and explanation, than form, color, or pattern.
In all its angles and aspects, this human urge to The usual distillate of biology—that ‘life is genes
embrace, comprehend, and explain what we and propagating genes’—is a serious misrepresentation
other species do—our behavior—is now recognized because evolution has created diversity in what
as a field of endeavor called neuroethology, rivaling animals do between generations; life consists of
those other distinctively human traits such as diverse states and actions—of course including
cooking, dancing in innovative ways, recounting the keeping alive and reproducing. But the big picture is
past and imagining the future, making each other missed if we do not hold up for scrutiny the different
laugh, and making music. ways of doing these things in beetles that burrow,
It strikes me as some kind of a pinnacle to bring butterflies that migrate, corals that luminesce, and
together between book covers what has been learnt lions that sleep away most of the day.
and how it was done so that we can exercise another Zupanc has recognized the importance of
very human trait—wonder at it! organizing the wealth of detail in a reader-friendly
One reason for this somewhat obtuse opening way—with Leitmotifs in special categories and
is that it underlines a strongly felt view of Günther sidebars. He has also recognized the importance of
Zupanc that the raison d’etre of such a book need not descriptive natural history preceding and leading
depend on its potential relevance to practical human into reductionist analysis—neuroethology begins
concerns, such as medicine or the psychology of with adequate ethology.
human aggression, but, in today’s world, upon simple Particularly important in neuroethology, and
curiosity and knowing for its own sake. This latest well represented in this treatment, is comparison—
summing up follows worthily the path pioneered by comparison of sensory stimuli that trigger, of
Jörg-Peter Ewert (Neuro-Ethologie: Einführung in pathways and central structures involved, of
die neurophysiologischen Grundlagen des Verhaltens, background state dependence, and alternative tricks
Springer-Verlag, Berlin, 1976), Jeff Camhi for canceling self-generated signals. Comparison is
(Neuroethology: Nerve Cells and the Natural Behavior the essence and applies to different taxa, ontogenetic
of Animals, Sinauer, Sunderland/Massachusetts, stages, and readiness states. Nature appears rarely to
1984), and most recently Tom Carew (Behavioral use a single mechanism for all animals that exhibit a
Neurobiology: The Cellular Organization of Natural similar behavior—nor does she use a large number
Behavior, Sinauer, Sunderland/Massachusetts, of alternate mechanisms; several is the norm. The
2000), each in its own style. Exploiting the freedom limitation in our knowledge is a limitation of research
viii Foreword
endeavor, perhaps because there is less glamour in with the history of each strand of the fabric of
looking at the same behavior in other taxa than in neuroethology, the drama and dependence on
looking at hitherto unstudied behavior. serendipity and mindset. The results of this historical
Another feature that stands out in the present research are distributed throughout the text, often
treatment, although frequently underplayed in the in sidebars or boxes. May this book illumine the
primary literature, is that every case is identified science, influence the way investigators proceed, and
with a broad or basic issue. This is complemented by draw new ones into the field.
showing how some species are particularly favorable Theodore Holmes Bullock
for the given study and for closer analysis. La Jolla
A distinctive feature of this book is its concern June 2003
PREFACE
The foundation to writing this book was laid College, U.S.A.); Mark Konishi (California Institute
during my own graduate education. Four teachers of Technology, Pasadena, California, U.S.A.); Bill
have been particularly influential. The late Walter Kristan (UCSD, San Diego, U.S.A.); Jürg Lamprecht
Heiligenberg, in whose laboratory at the Scripps (Max-Planck-Institut für Verhaltensphysiologie,
Institution of Oceanography of the University of Seewiesen, Germany); Ken Lohmann (University of
California, San Diego (UCSD) I had the privilege to North Carolina, Chapel Hill, U.S.A.); Anne Lyons
work both as a Ph.D. student and as a postdoctoral (Oxford, U.K.); Eve Marder (Brandeis University,
fellow. The late Ted Bullock, also of UCSD, has been Waltham, Massachusetts, U.S.A.); Tom Matheson
a source of inspiration since my graduate student (University of Leicester, U.K.); Roswitha M. Marx
days. He made many suggestions on the manuscript (University of Victoria, Canada); Tom Matheson
of the first edition, and also kindly contributed the (University of Leicester, U.K.); James Mazer (Yale
Foreword. Larry Swanson, then at the Salk Institute University, U.S.A.); Jo Ostwald (Eberhard Karls
for Biological Sciences in La Jolla, California, now at Universität Tübingen, Germany); Sarah A. Parker
the University of Southern California at Los Angeles, (Stratford-upon-Avon, U.K.); Alan Roberts (University
taught me how to use neuroanatomy as a tool to of Bristol, U.K.); David Skingsley (Staffordshire
analyze the structural basis of behavioral control University, Stoke-on-Trent, U.K.); Julian Thomas
mechanisms. Equally importantly, he also showed (Sterna Word Services, Somerset, U.K.); Wim van
me that even the teaching of a difficult subject can be de Grind (Universiteit Utrecht, The Netherlands);
joy for both instructor and student. Len Maler of the Gerhard von der Emde (University of Bonn, Germany);
University of Ottawa, Canada, taught me, through Neil Watson (Simon Fraser University, Burnaby, British
many joint projects, how to integrate behavioral, Columbia, Canada); David Wilcockson (Aberystwyth
anatomical, and physiological data to gain an University, U.K.); Janine Wotton (Gustavus Adolphus
appreciation of how the central nervous system College, U.S.A.); and Jayne E. Yack (Carleton
generates behavior. University, Ottawa, Canada).
In the course of writing the three editions of My friend Cecilia Ubilla (UCSD) spent numerous
this book, I greatly benefited from the advice of hours on the manuscript of the three editions to
the following colleagues: Jon Banks (University of optimize my style of writing. Her comments from the
Manchester, U.K.); Jon Barnes (University of Glasgow, perspective of a naive reader on the one hand, and an
U.K.); Bob Beason (University of Louisiana, Monroe, experienced professional writer and teacher on the
U.S.A.); Rob Bell (Queen’s University Belfast, U.K.); other, were instrumental in polishing up the text.
Gary Boyd (University of the West of Scotland, Another factor that proved to be indispensable
Paisley, U.K.); Kenneth H. Britten (University of in writing this book was the excellent collaboration
California, Davis, U.S.A.); Toby Carter (Anglia with the staff of Oxford University Press. Esther
Ruskin University, U.K.); Bruce Carlson (Washington Browning proposed this project and got me started.
University, St. Louis, U.S.A.); Chris Elliott (University Five publishing editors oversaw the writing and
of York, U.K.); Jack Gray (University of Saskatchewan, production of the three editions—Jon Crowe, Ross
Canada); Natalie Hempel de Ibarra (University of Bowmaker, Dewi Jackson, Jess White, and Lucy
Exeter, U.K.); Jane Hoyle (Sheffield, U.K.); Franz Wells. They have been reliable sources of advice and
Huber (Starnberg, Germany); Jason Jones (Vassar encouragement, and I am grateful to each of them.
Acknowledgements xi
Major parts of the manuscript for the book Finally, I am indebted to my wife Marianne, and
were written while I spent summers at UCSD. our children Frederick, Christina, and Daniel for
I am grateful to the Conrad Naber Foundation their (almost) never-ending forbearance. Without
(Germany) for partially funding these visits. I their support, this book would not have been
would also like to thank the Royal Society in the possible.
U.K. for the award of a History of Science grant that Günther K. H. Zupanc
enabled me to collect the information necessary to Boston, Massachusetts
write Chapter 3. November 2018
TABLE OF CONTENTS
Each of the 13 chapters is organized in a similar way and contains a number of valuable tools which aim to
help you to understand and learn.
Text boxes explore key concepts, such as the Box 4.1 Herbert Spencer Jennings
structure and function of central pattern generators, remained the subject of choice in mo
and key people in the field of neuroethology. Following a year of graduate study at
Harvard, where he received his P
descriptive study of the developmen
went to Europe to work with the the
physiologist Max Verworn (Fig. 4.1)
some time in Italy at the Naples Bio
decade of temporary positions, in 19
For students:
• Multiple choice questions for you to test yourself
• Useful weblinks
• A biography of the author and interview about
key questions in behavioral neurobiology
For lecturers:
• Answers to the questions provided at the end of
each chapter
• Figures from the book in a downloadable format
• Journal Club material for each chapter
www.oup.com/uk/zupanc3e
1 Introduction
Introduction 1
Neuroethology: The synthesis of neurobiology and ethology 2
Choosing the right level of simplicity 2
Quantifying behavior: A prerequisite for neuroethological research 4
Finding the right model system 5
Summary 7
The bigger picture 8
Recommended reading 8
Short-answer questions 8
Essay questions 8
Advanced topic 9
individual components, referred to as the individual Obviously, by dividing the behavior of an animal
behaviors or behavioral patterns. As a first step, further and further down, a hierarchical arrangement
the total behavioral repertoire is often divided into results. Niko Tinbergen, one of the founders of
major groups representing functional categories, for ethology (see Chapter 2), called the different levels
example ‘sleep,’ ‘feeding,’ ‘courtship,’ or ‘aggression.’ within this hierarchical system levels of integration.
Yet, these categories are still too large to be quantified The lateral display of cichlids, for example, involves
and analyzed in a meaningful way. This makes a alignment of the fish beside its opponent, typically
further subdivision necessary. within a few centimeters, and a rapid, powerful
sideways thrust of the tail. During this display, the
dorsal, anal, and pelvic fins are erect and the opercula
Ethogram The entire behavioral repertoire of an animal extended. The erection of the fins, on the other hand,
species. is defined by the action of the individual fin rays,
whose movement is the result of the contraction
of muscle fibers controlled by neural motor units.
Example: Cichlids are a family of more than Fig. 1.3 illustrates this stepwise subdivision of
2000 teleost fishes. They are well known for their behavior into smaller and smaller elements.
highly developed aggressive, courtship and parental- While it hardly makes sense to undertake a study
care behavior. As illustrated in Fig. 1.2, the behavior aimed at elucidating the neural basis of ‘aggression’
subsumed under the term ‘aggression’ actually consists in a cichlid fish, one would likely succeed, with the
of a number of individual behavioral patterns, techniques available, in identifying the structures
including chasing, butting, frontal display, lateral within the central nervous system that control the
display, and mouth wrestling.
Figure 1.2 Aggressive behavior of the blue acara (Aequidens head of the opponent. (d) Mouth grasping. The fish grasp
pulcher), a teleost fish of the cichlid family. (a) Lateral display. each other at the lower or upper mandible. (e) Mouth pulling.
The fish align beside each other, spread the dorsal, anal, and Each fish tries to pull the opponent, after having grasped each
pelvic fins, and intensify the coloration of their bodies. These other’s mouth. (f) Defeat. The fish at the front gives up. It folds
threats are accompanied by light tail beats. (b) Circling. While its fins, adopts a pale coloration, and swims off. (After: Wicker,
circling each other, the fish have the ventral part of the mouth W. (1968).)
lowered. (c) Tail beating. One fish beats its tail against the
4 Chapter 1 Introduction
Aggressive
behavior
Lateral Mouth
Circling
display fighting
Figure 1.3 Splitting the lateral display, an aggressive behavioral hierarchical arrangement in which various levels of integration
pattern of cichlid fish, into individual elements. This leads to a are distinguished. (Courtesy: G. K. H. Zupanc.)
dorsal fin erected?’), their duration (‘How long is the are a major reason why many fundamental cellular
dorsal fin kept in an erect position?’), and/or their mechanisms underlying learning and memory
intensity (‘Is the dorsal fin erected maximally, with are very similar among animals, including both
the fin rays almost perpendicular to the dorsal edge vertebrates and invertebrates. On the other hand,
of the fish’s body, or do the fin rays adopt positions these universals of life make it possible to establish
intermediate between the maximal and the minimal principles of learning and memory processes by
angle?’). A similar attempt to quantify the lateral studying the rather simple neural network of the sea
display would be very difficult, particularly because slug Aplysia, although ultimately most researchers
of the complexity of the different actions involved in would like to understand more complex systems,
the execution of this behavior. As not all individual including those of humans (see Chapter 13).
actions are necessarily executed simultaneously Despite the existence of similar solutions to
during lateral display, a main problem would be a given behavioral problem in many species,
to identify the end points of this behavior. Lack of not each of them is equally suited for exploring
such information makes it virtually impossible to the neural implementations of these solutions.
determine the parameters’ ‘rate of occurrence’ and Recognizing the dilemma of the right choice of
‘duration.’ Also, measurement of the intensity would experimental animals, the Danish physiologist
be difficult: Is the behavior more intense when a August Krogh published in 1929 an essay in which
larger number of individual actions are displayed, or he wrote: ‘For a large number of problems there
when the degree of execution of individual patterns will be some animal of choice or a few such animals
is maximized? in which it can be most conveniently studied.’
Krogh’s Principle, as it was dubbed later, has been
➤ A behavioral pattern can be quantified using its rate of widely used by comparative physiologists and
occurrence, duration, and/or intensity. neuroethologists as a guide in the experimental-
design process. For example, the success in the
identification and characterization of the neural
circuitry that controls rhythmic motor activity was
largely based on the choice of Xenopus tadpoles,
Finding the right model system with their relatively simple organization of the
spinal cord, and the possibility of evoking neural
The above considerations underline the importance of activity associated with the motor behavior from
choosing the right model system. Such systems are not physiological preparations (see Chapter 6). Barn
primarily studied to provide insights into the neural owls as nocturnal hunters rely heavily on acoustic
mechanisms underlying the behavior of the respective cues for localization of prey. They are, therefore,
species. Rather, their characterization enables the particularly well suited to elucidating the neural
neuroethologist to extract principles applicable to mechanisms that underlie processing of auditory
many, if not all, animals. This is possible because information (see Chapter 7).
there are, probably in any case, only a finite number Besides selecting a model system based on a good
of solutions to a given behavioral problem. Keeping match of the research question and the relevant
the body oriented, for example, requires the analysis biological properties of the organism, other
of geophysical invariants, but the number of options important considerations are that the behavior
available is limited to a few, such as the measurement under scrutiny should be simple and robust, readily
of the direction of the incident light or of the animal’s accessible, and ethologically relevant; and the
angle relative to gravity (see Chapter 4). animal displaying this behavioral pattern should
Many solutions to such problems were invented be inexpensive, suitable for examination in the
very early in evolution, so that frequently the neural laboratory, easy to maintain, and possible to breed.
implementations of these solutions are homologous These requirements are far from trivial to meet, and
in different species. Such homologous developments the right choice of a suitable model system always
6 Chapter 1 Introduction
demands profound knowledge in both animal mode of regularity (Fig. 1.4b, c). These modulations
biology and husbandry. are used, for example, to encode information in the
context of intraspecific communication, such as
Example: Two orders of teleost fish produce, by during aggressive encounters (Fig. 1.5). In addition,
means of a specialized organ, electric discharges the fish employ their discharges for object detection.
of low voltage. As will be demonstrated in detail in The electric behavior, therefore, meets the above
Chapter 8, these so-called electric organ discharges requirement of ethological relevance. Moreover,
are quite simple in terms of their biophysical many weakly electric fishes can be kept in aquaria
properties, highly robust, and they can readily under semi-natural conditions; several species have
be monitored by placing recording electrodes even been bred successfully in the laboratory. Taken
near the fish. Their rate of occurrence, duration, together, these properties make them ideal subjects
and intensity can easily be measured, thus allowing for neuroethological research.
the researcher to quantify this behavior. This is
illustrated by Fig. 1.4, which shows the discharge This and other examples of good neuroethological
pattern of the elephant nose (Gnathonemus model systems are discussed in detail in the
petersii). This mormyriform fish produces very following chapters of this book. Their exploration
brief electric pulses, which are, even over hours over the last decades has greatly advanced our
and days, highly stable in terms of their physical understanding of how the brain controls behavior.
appearance (Fig. 1.4a). However, the fish are able Moreover—and equally important—this research
to modulate the discharge pattern, for example by has also deepened our appreciation for the biology
altering the pulse repetition rate or by changing the of the whole animal.
(a)
2msec
(b)
(c)
3sec
Figure 1.4 Electric organ discharge of the elephant between the individual pulses are somewhat irregular.
nose, Gnathonemus petersii. (a) Each discharge results in (c) After stimulating an isolated fish with the discharges of a
a brief electric pulse, which is highly constant in terms of second elephant nose (indicated by the horizontal
duration, amplitude, and waveform. (b) Resting discharge bar below the trace), the discharge pattern changes
pattern over a slower timescale. As the individual pulses significantly. In the example shown, the fish discharges
are highly constant, this behavior can readily be quantified at almost three times the resting rate, and the pattern of
by counting the number of pulses (here represented as pulse production becomes more regular. The result of this
vertical bars) produced per second and by analyzing the experiment underlines the ethological relevance of the
pattern of discharge. In the example shown, approximately electric organ discharge. (Courtesy: G. K. H. Zupanc and
five pulses per second are generated, and the intervals J. R. Banks.)
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Language: English
THE
DIPLOMATIC
CORRESPONDENCE
OF THE
AMERICAN REVOLUTION;
BEING
TOGETHER WITH
ALSO,
BOSTON:
NATHAN HALE AND GRAY & BOWEN;
G. & C. &. H. CARVILL, NEW YORK; P. THOMPSON, WASHINGTON.
1829.
THIRD VOLUME.
Page.
To John Hancock, President of Congress. Nantes,
5
December 8th, 1776,
Recommending M. Gerard.
Devices on coins.
Mr Pultney.—Errors corrected.
Relative to supplies.
To the President of Congress. Passy, March 12th,
192
1781,
Military operations.
Supplies.
Introducing Dr Putnam.
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