Table Of ContentStudies of Brain Function, Vol. 12
Coordinating Editor
V. Braitenberg, Tiibingen
Editors
H. B. Barlow, Cambridge
T. H. Bullock, La Jolla
E. Florey, Konstanz
O.-J. Grosser, Berlin-West
A. Peters, Boston
Studies of Brain Function
Volumes already published in the series:
1 W. H eiligenberg
Principles of Electrolocation and Jamming A voidance
in Electric Fish
2 W. Precht
Neuronal Operations in the Vestibular System
3 J. T. Enright
The Timing of Sleep and Wakefulness
4 H.Braak
Architectonics of the Human Telencephalic Cortex
5 H. Collewijn
The Oculomotor System of the Rabbit and Its
Plasticity
6 M. Abeles
Local Cortical Circuits
7 G. Palm
Neural Assemblies
8 J. Hyviirinen
The Parietal Cortex of Monkey and Man
9 E. Zrenner
Neurophysiological Aspects of Color Vision
in Primates
10 U. Biissler
Neural Basis of Elementary Behavior
in Stick Insects
11 G. A. Orban
Neuronal Operations in the Visual Cortex
12 M. Heisenberg, R. Wolf
Vision in Drosophila
M. Heisenberg R.Wolf
Vision in Drosophila
Genetics of Microbehavior
With 112 Figures
Springer-Verlag
Berlin Heidelberg New York Tokyo 1984
Prof. Dr. MARTIN HEISENBERG
REINHARD WOLF
Institut fUr Genetik und Mikrobiologie
Rontgenring 11
8700 Wiirzburg
ISBN-13: 978-3-642-69937-5 e-ISBN-13: 978-3-642-69936-8
DOl: 10.107/978-3-642-69936-8
Library of Congress Cataloging in Publication Data. Heisenberg, Martin,
1940- . Vision in Drosophila. (Studies of brain function; vol. 12). Bib
liography: p. . Includes index. 1. Drosophila - Behavior. 2. Drosophila -
Genetics. 3. Drosophila - Physiology. 4. Behavior genetics. 5. Insects -
Behavior. 6. Insects - Genetics. 7. Insects - Physiology. I. Wolf, Reinhard,
1947- . II. Title. III. Series: Studies of brain function; vol. 12)
QL537.D76H45 1984 595.77'1 84-14088
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© by Springer-Verlag Berlin Heidelberg 1984.
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Preface
This book is written for our friends in Germany and
abroad to give an account of our main interests during the last
years. We gratefully take the opportunity provided by Springer
Verlag with the Series Studies of Brain Function to present
some of our recent work on vision in Drosophila in a coherent
form and in a broader context than publications in periodicals
would permit. We want to picture the visual system of the fly
fitting it into the natural history from which our own vision
emerged. In this perspective genetics seems to be a useful ap
proach.
Our study is a rather personal exercise. We have neither the
expertise nor the ambition to cover the whole literature or to
compile· all the knowledge about vision in flies. We are not even
in a position to present, with the appropriate weight and
breadth, the pioneering contributions of those who established
this field of research. Our account mirrors our own intersects.
We are selecting and interpreting other peoples' work from this
subjective point of view, although we try to present it in its own
right. For several years we have been fascinated by the first
glimpses of the "inner life" of an insect and we hope to convey
this fascination to those who are not discouraged by the scien
tific procedure.
To a large extent the book reviews published work, but it
also describes many new experiments which have not been
published before. From the published work we largely omit
details and present conclusions without the evidence support
ing them. Our new experiments we elaborate more throughly
and in some cases we even include experimental procedures in
the figures or figure captions. We try to show how these exper
iments should be understood in a broader context. Views,
reviews, and new results are only partially separated into dif
ferent chapters. The reader will find "views" mainly in Intro
duction, Synopsis and the introductory paragraphs to some
other chapters. Chapter 1 to 4,10, and 13 are to a large extent
summaries of other peoples' work; new data from our own
VI Preface
laboratory are to be found mainly in Chapters 5 to 9, 11,
and 12.
We thank all our friends and colleagues who contributed
to this book in one way or another. Without their support
the book would not have been written. V. Braitenberg encou
raged us to start this enterprise. His interest in general
problems of brain function was a constant source of inspira
tion. F. Huber, over the years, shared with us his enthusaism
in the discussion of central brain function of insects.
W Reichardt tought us a basic understanding of his theoretical
approach to fly vision. We regard this approach as a necessary
step in behavioral analysis. K. G. Gotz, E. Buchner and
K. F. Fischbach repeatedly acted as consultants in the evalu
ation and design of experiments. Their expertise has been a
permanent resource in our work and a comfort for our sleep.
I. Meinertzhagen, L. Schneider and N. Strausfeld generously
provided unpublished material. We consider it a special honor
to include their original work in the book. V. Braitenberg,
E. Buchner, D. Byers, P. Coombe, K. F. Fischbach, K. G. Gotz,
F. Huber and W Reichardt kindly went to the trouble of
reading parts or all of the book in a preliminary form. They
corrected errors in details, erradicated all too biased opinions
and helped in smoothing and polishing. D. Byers, in particular,
went through the sections on Initiation and scrutinized
every sentence. E. Buchner, K. F. Fischbach, K. G. Gotz and
W Reichardt generously granted permission to use their fig
ures. K. Leopold, K. Schulze, M. Stengl, S. Wagner, J. Winter
and B. Wolf typed, with great patience, parts of the manu
script. D. Dode1 and A. Ledermann helped in the preparation
of drawings. Their friendly cooperation made work fun.
We dedicate the book to our wives who created the time for
the book in our well-packed schedules.
Wiirzburg, Summer 1984 M. HEISENBERG
R. WOLF
Contents
Introduction
Initiating Activity ..... 1
Input-Output Analysis 3
Orientation and Orientedness 5
Neurogenetics . . . . . . . 6
Part A: Eye, Brain, and Simple Behavior
1 The Compound Eye 10
The Distribution of Optical Axes 10
Neural Superposition . . . . . 13
The Equator. . . . . . . . . 16
Angular Sensitivity of Visual Elements 17
Screening Pigments . . . . . 17
Electrical Responses to Light 18
Spectral Sensitivity . . 20
Polarization Sensitivity 22
Ocelli . . 23
Summary . . . . . . 23
2 Neuronal Architecture of the Visual System 25
Retinotopic Maps 25
Visual Foci 26
Lamina ganglionaris 27
Medulla, Lobula, Lobula Plate 31
3 Motion Sensitivity Under Open Loop Conditions 33
Orientation . . . . . . . . . . . . . . . 33
Optomotor Yaw Torque and Turning Behavior 34
Optomotor Equilibrium . . . . . . 43
Optomotor Roll and Pitch Responses . . . . 44
Translatory Optomotor Responses . . . . . 46
Optomotor Posture Control by Visual Motion 48
Visually Induced Start of Flight and Landing 49
VIII Contents
4 Toward Correlating Structure and Function 52
Retinal Subsystems . . . . . . . 52
Color Vision. . . . . . . . . . . . 53
Polarization Sensitivity in Behavior . . 56
Dark Adaptation on Account of Acuity 58
Elementary Movement Detectors 59
3H-Deoxy-Glucose .... 61
Lobula Plate Giant Neurons 63
Other Visual Pathways . . 74
Part B: The Behavioral Structure of the Visual System
5 Flying Straight. . . . . . . . . 82
Artificial Closed Loop Conditions 82
Optomotor Balance. . . . . . . 83
Closed Loop Gain of Freely Rotating Flies 92
6 Endogenous Behavior in Yaw Torque Fluctuations 95
Saccades and Torque Spikes . . . . . 95
Torque Spikes as Fixed Action Patterns . 98
Reafference Control ......... 100
Spontaneous Occurrence of Torque Spikes 104
Torque Spikes Rules 104
Flight Modes . . . . . . 107
7 Orientation Toward Objects 110
Fixation Behavior in Musca, a Theory 113
The Object Response in Drosophila . . 119
Special Role of Front-to-Back Motion 120
Range of Stimulus Parameters for the Position
Function . . . . . . . . . . . . . . 123
Two Responses Contribute to Yaw Torque . 125
Analysis of Individual Torque Traces . . . 129
Mutants with Altered Orientation Behavior 131
Fixation in Flight 134
Fixation in Walking Flies 141
8 Menotaxis. . . . . . . 146
Small Angle Oscillations. 147
Significance of Reafferent Stimuli . 153
The Object Response During Menotaxis 154
Contents IX
9 Foreground-Background Experiments 158
Figure-Ground Discrimination in Musca 158
One Output-Multiple Input Systems . . 160
A Simple Model Generating Figure-Ground
Discrimination . . . . . . . . . . . . . 162
Figure-Ground Discrimination in Drosophila 163
Tracking . . . . . . . . . . . . . . 165
Interplay Between Object Response and
Optomotor Balance . . . . . . . . . 166
Dissociation into Object and Background 174
Interpretation of Object Response . . . 176
Can the Musca Theory on Pattern-Induced Flight
Orientation Be Applied to Drosophila? 178
10 Visual Control in Free Flight 180
11 Selective Attention. . . . 183
Displacement Experiments 184
Open Loop Oscillations 187
12 Plasticity of Visuo-Motor Coordination 194
13 Valuation 205
Hypotheses . . . . . . . . . . . 206
Significance of Simple Visual Stimuli 209
Context Dependence ...... . 210
Visual Components of Courtship Behavior 213
Conditioning . . . . . . . . . . . . . 215
Synopsis
The Three Levels of Orientation 217
Parallel Processing. . 218
Actions and Responses 219
Voluntary Behavior 220
Orientedness Revisited 223
Appendix 1: List of Neurological Mutants 226
Appendix 2: Symbols, Dimensions, Abbreviations 230
References. . 232
Subject Index 243
Introduction
Vision is naively considered by many people as a process originating in
an organism and directed toward the world. In early scifmtific illustrations
rays were drawn from the eye to the object. Only in the last few centuries with
the growing awareness of the nature of light has it become generally accepted
that the relevant light travels from the object to the eye and that information
flows from the world into the body. While this concept today is the un
contested basis of vision research, it tends to overemphasize the role of the
viewing subject as that of a passive receiver. Particularly in comparative
studies of small animals, stimulus-response chains are considered the hard
core of visual behavior. Our experience as humans with vision as a continu
ous series of verifications or rejections of guesses is taken as a specialty of
higher vertebrates.
Initiating Activity
Among the most important brain functions of which we know introspec
tively is the ability to initiate activity. We do not have to wait until a stimulus
gets us going. We can ourselves start a train of events which then leads to a
change in the situation. Initiation is a constituent of nearly all behavior.
Choice, will, self, the pursuit of goals, and probably all mental activity such
as imagination and thinking require this all-pervasive faculty of the brain. We
hope to convince the reader in this book that initiation cannot have been
added late in evolution as a result of growing complexity. Rather, it must be
a basic trait of all brains, even of small ones. The natural history of voluntary
behavior must have started at the very beginning of the evolution of brains.
We emphasize the self-sufficiency of brains in generating activity since we
feel that although this idea was put forward long ago, it has not been fully
appreciated by many people in the field and is still questioned by some of
them. One of the reasons for scepticism has been that the evidence for truly
endogenous activity has never been compelling. Animal observations in the
natural environment cannot exclude the possibility that some uncontrolled
stimulus might have caused a suddenly occuring behavior. In fact, in the
tradition of empiricist philosophy the so-called behaviorists for a long time
maintained that all behavior, including spontaneous behavior, could in prin-
