Information Processing in the Visual Systems of Arthropods Symposium Held at the Department of Zoology University of Zurich, March 6-9, 1972 Edited by RUdiger Wehner With 263 Figures Spri nger-Verlag Berlin Heidelberg New York 1972 The cover shows a scanning electron micrograph of the compound eye of a desert ant, Cataglyphis bicolor (University of Zurich). ISBN-13: 978-3-540-06020-8 e-ISBN-13: 978-3-642-65477-0 001: 10.1007/978-3-642-65477-0 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re·use of illustrations, broadcasting, reproduction by photocoping 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. 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 Merchandise Marks Act, may accordingly be used freely by anyone. © by Springer·Verlag Berlin' Heidelberg 1972. Library of Congress Catalog Card Number 72-91887. Preface It is now generally accepted for a variety of reasons - morphological as well as physiological - that the visual systems of arthropods provide a suitable model for the study of information proces sing in neuronal networks. Unlike the neurophysiology of the visual pathway in the frog and the cat which is more than adequately documented, recent work on the compound eye and optical ganglia of spiders, crustaceans, and insects has scarcely been summarized. In order to fill this void so that others, especially vertebrate neurophysiologists may become familiar with the advan tages of these systems, our group at Zurich University organized here in March 1972, a European meeting to discuss the anatomical.! neurophysiological and behavioral knowledge on the compound eye and the visual. pathway of arthropods. Systems analysis was regarded as the main theme of the conference, but systems analysis of a network of neurons cannot be done as a mere "black-box" maneuver. The conference therefore tried to reconcile neurophysiology and behavioral analysis in order to make predictions about a necessary and sufficient neural structure. The "wiring dia grams" of such a structure might then be confirmed histologically. Hence the aim of the conferen ce was not to deal only with the structure and function of the compound eye - i.e. data processing in the dioptric apparatus and in the layer of the retinular cells - but to apply this knowledge to the performance of the visual system in color discrimination, pattern recognition, and other cent ral nervous processes. Although the official language of the symposium was German, the contributors wrote their manus cripts in English, also reflecting the extensive discussions that arose both during and after the for mal sessions. We thus hope to make any insights derived from the discussions available to those unable to attend. Besides the authors, we would like to thank all the 77 participants of the symposium for their li vely contributions both inside the lecture hall and outside. The discussions allowed the contribu tors to cross-check recent knowledge and made it clear that the visual systems of arthropods have much to contribute to neurophysiology. Much enthusiasm was generated for planning the further work along these lines. I wish most of all to express our appreciation to the Swiss National Found ation for Scientific Research, which provided generous financial support for the meeting, and to Springer-Verlag for the very rapid publication of the proceedings. Zurich, June 1972 RUdiger Wehner Contents Preface III List of Participants IX Opening Remarks I. ANATOMY OF THE VISUAL SYSTEM 1. V. BRAITENBERG Periodic Structures and Structural Gradients in the Visual Gangl ia of the Fly 3 2. C.B. BOSCHEK Synaptology of the Lamina ganglionaris in the Fly 17 3. N.J. STRAUSFELD and J.A. CAMPOS-ORTEGA Some Interrelationships between the First and Second Synaptic Regions of the Fly's (Musca domestica) Visual System 23 4. J.A. CAMPOS-ORTEGA and N.J. STRAUSFELD Col umns and Layers in the Second Synaptic Region of the Fly's Visual System: The Case for Two Superimposed Neuronal Arch i cetures 31 5. R. MENZEL The Fine Structure of the Compound Eye of Formica polyctena - Functional Morphology of a Hymenopterean Eye 37 6. P.L. HERRLlNG Measurements on the Arrangement of Ommatidial Structures in the Retina of Cataglyphis bicolor (Formicidae, Hymenoptera) 49 7. H.F. PAULUS The Ultrastructure of the Photosensible Elements in the Eyes of Collembola and Their Orientation (Insecta) 55 II. OPTICS OF THE COMPOUND EYE 1. K. KIRSCHFELD The Visual System of Musca: Studies on Optics, Structure and Function 61 2. N. FRANCESCHINI Pupil and Pseudopupil in the Compound Eye of Drosophila 75 VI 3. W.P. EHEIM Directional Intensity Distribution in Single Ommatidia of the Honeybee, Apis mell ifera 83 4. P. KUNZE Pigment Migration and the Pupil of the Dioptric Appa- ratud in Superposition Eyes 89 5. R. HENGSTENBERG Eye Movements in the Housefly Musca domestica 93 III. BIOCHEMISTRY OF VISUAL PIGMENTS 1. K. HAMDORF, R. PAULSEN, J. SCHWEMER and U. TAEUBER Photoreconversion of Invertebrate Visual Pigments 97 2. H. LANGER Metarhodopsin in Single Rhabdomeres of the Fly, Call iphora erythrocepha la 109 IV. INTENSITY - DEPENDENT REACTIONS l. T. LABHART The Discrimination of Light Intensities in the Honey Bee 115 2. M. FRISCHKNECHT Photopositive Reactions of Honey Bees to Circular Areas of Varying Sizes and Light Intensities 121 3. P. STRECK Screening Pigment and Visual Field of Single Retinula Cells of Call iphora 127 4. G. FLEISSNER Circadian Sensitivity Changes in the Median Eyes of the North African Scorpion, Androctonus austral is 133 5. E. BUCHNER Dark Activation of the Stationary FI ight of the Fruitfly Drosophila 141 V. WAVELENGTH - DEPENDENT REACTIONS 1. D. BURKHARDT and I:DE LA MOTTE Electrophysiological Studies on the Eyes of Diptera, Mecop- tera and Hymenoptera 147 2. R. SCHUEMPERLI Wavelength-specific Behavioral Reactions in Drosophila melanogaster 155 VII 3. W. KAISER and E. LISKE A Prel iminary Report on the Analysis of the Optomotor System of the Bee - Behavioral Studies with Spectral Lights 163 4. W. KAISER A Prel iminary Report on the Analysis of the Optomotor System of the Honey Bee - Single Unit Recordings du- ring Stimulation with Spectral Lights 167 5. F. TOGGWEILER Spectral Sensitivity and Wavelength Discrimination in Cataglyphis bicolor (Formicidae) 171 6. H. ROTH and R. MENZEL ERG of Formica polyctena and Selective Adaptation 177 VI. PATTERN RECOGNITION 1. R. WEHNER Pattern Modulation and Pattern Detection in the Visual System of Hymenoptera 1-83 2. B. SCHNETTER Experiments on Pattern Discrimination in Honey Bees 195 3. H. CRUSE A Qualitative Model for Pattern Discrimination in the Honey Bee 201 4. A. ANDERSON The Ability of Honey Bees toGeneralise Visual Stimuli 207 5. W. REICHARDT First Steps in a Behavioral Analysis of Pattern Discrimi- nation in Diptera 213 6. F. ZETTLER and M. JAERVILEHTO Intraaxonal Visual Responses from Visual Cells and Second- order Neurons of an Insect Retina 217 7. H.W. MEYER Ethometrical Investigations into the Spatial Interaction within the Visual System of Velia caprai (Hemiptera, Heteroptera) 223 8. M.F. LAND Mechanisms of Orientation and Pattern Recognition 231 9. F. SCHALLER Observations on the Yisual Reactiohs of Collembola 249 VIII VII. VISUAL CONTROL OF ORIENTATION PATTERNS 1. K.G. GOETZ Processing of CI ues from the tvbving Environment in the Drosophila Navigation System 255 2. M. HEISENBERG Behavioral Diagnostics; a Way to Analyse Visual Mutants of Drosophila 265 3. P. GOERNER Resultant Positioning between Optical and Kinesthetic Orientation in the Spider Agelena labyrinthica clerck 269 4. M.L. MITTELSTAEDT -BURGER Idiothetic Course Control and Visual Orientation 275 5. P. DUELLI The Relation of Astromenotactic and Anemomenotactic Orientation Mechanisms in Desert Ants, Cataglyphis bicolor (Formicidae, Hymenoptera) 281 6. R. WEILER and M. HUBER The Significance of Different Eye Regions for Astromeno tactic Orientation in Cataglyphis bicolor (Formicidae, Hymenoptera) 287 7. R. WEHNER and I. FLATT The Visual Orientation of Desert Ants, Cataglyphis bico lor, by Means of Terrestrial Clues 295 8. A. BURKHALTER Distance Measuring as Influenced by Terrestrial Clues in Cataglyphis bicolor (Formicidae, Hymenoptera) 303 VII I. STORAGE OF VISUAL INFORMATION 1. J. ERBER The Time-Dependent Storing of Optical Information in the Honey Bee 309 2. T. MASUHR and R. MENZEL Learning Experiments on the Use of Side - Specific Infor mation in the Olfactory and Visual System in the Honey Bee (Apis mell ifica) 315 IX. METHODS OF QUANTIFYING BEHAVIORAL DATA 1. O. v. HELVERSEN The Relationship between Difference in Stimuli and Choice Frequency in Training Experiments with the Honey Bee 323 List of Partici pants ANDERSON, A.M., University of Edinburgh, Dept. of Zoology, West Mains Rd., GB-Edinburgh, EH93JT BAESSLER, U., Universitat Trier -Kaiserslautern, Naturwiss. -Techn. Fakul tat, D-675 Kaisers- lautern, Postfach 1019 BAUMANN, F., Universite de Gen~ve, Dept. de Physiologie, CH-1211 Gen~ve 4 BOSCHEK, C.B., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr.38 BRAITENBERG, V., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemann- strasse 38 BRUNNERT, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 BURKHALTER, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstler gasse 16 BURKHARDT, D., Universitat Regensburg, Fachbereich Biologie, D-8400 Regensburg, Universitats strasse 31 BUTENANDT, E., Max-Planck-Institut fUr Verhaltensphysiologie, D-8131 Seewiesen/Obb. CAMPOS-ORTEGA, J.A., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 CRUSE, H., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 DORNFELD, K., II. Zoologisches Institut der Freien Universitat, D-1 Berlin-41, Grunewaldstr.34 DUELLI, P., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 EHEIM, W.P., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 ERBER, J., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnittspahnstr.3 FLATT, E., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 FLEISSNER, G., Zoologisches Institur der Universitat, D-6 Frankfurt a.M., Siesmayerstr. 70 FRANCESCHINI, N., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemann- strasse 38 FRISCHKNECHT, M., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstler- gasse 16 GEIGER, G., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 GOERNER, P., II. Zoologisches Institut der Freien Universitat, D-1 Berlin 41, Grunewaldstr. 34 GOETZ, K.G., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 HAMDORF, K., Ruhr-Universitat Bochum, Lehrstuhl fUr Tierphysiologie, Gebaude ND, 5.0.G., D-463 Bochum HAUSEN, H., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 HEISENBERG, M., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemann strasse 38 HELVERSEN, O.v., Biologisches Institut I (Zoologie) der Albert-Ludwigs-Universitat, D-78 Frei burg i.Br., Katharinenstr. 20 HENGSTENBERG, R., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemann- strasse 38 HERRLlNG, P.L., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 HUBER, M., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 JAERVILEHTO, M., Zoologisches Institut der Universitat MUnchen, D-8 MUnchen 2, Luisenstr. 14 KAISER, W., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnittspahn- strasse 3 x KIEPENHEUER, J., Universitat Frankfurt, Zoologisches Institut, D-6 Frankfurt a.M., Siesmayer- strasse 70 KIRSCHFELD, K., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 KLEIN, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 KRETZ, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 KUNZE, P., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 KURTH, B., II. Zoologisches Institut der Freien Universitat, D-1 Berlin-41, Grunewaldstr. 34 lABHART, T., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 lAND, M., University of Sussex, Biology Bldg., Falmer, Brighton, Suss. BN1 9QG, Great Britain lANGER, H., Ruhr-Universitat Bochum, Institut fUr Tierphysiologie, Gebaude JC-4/43, D-463 Bochum, Postfach 2148 LISKE, E., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnittspahnstr. 3 MASUHR, T., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnitt spahnstr. 3 MENZEL, R., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnitt- spahnstr. 3 MEYER, L, Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 MEYER, H., Zoologisches Institut der Universitat, D-6 Frankfurt a.M., Siesmayerstr. 70 MITTELSTAEDT, H., Max-Planck-Institut fUr Verhaltensphysiologie, D-8131 Seewiesen/Obb. MITTELSTAEDT, M., Max-Planck-Institut fUr Verhaltensphysiologie, D-8131 Seewiesen/Obb. c., MONDADORI, Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstler- gasse 16 MOTTE de la, J., Universitat Regensburg, Fachbereich Biologie, D-8400 Regensburg, Univer sitatsstr.31 NOWAK, H., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 PAULUS, H., I. Zoologisches Institut der Universitat Wien, A-10lO Wien-1, Dr. Karl Lueger Ring 1 PERRELET, A., Universite de Gen~ve, Dept. Histologie, CH-1211-Gen~ve 4,20, rue de I' Ecol e de Medeci ne PICK, H., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr. 38 REICHARDT, W., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemannstr.38 REISSLAND, A., II. Zoologisches Institut der Freien Universitat, D-1 Berlin-41, Grunewaldstr.34 RIBI, W., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, Kunstlergasse 16 ROTH, H., Zoologisches Institut der Technischen Hochschule, D-61 Darmstadt, Schnittspahnstr.3 ROTHENBACH, D., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstler- gasse 16 SCHALLER, F., I. Zoologisches Institut der Universitat Wien, A-10lO Wien-1, Dr. Karl Lueger Ring 1 SCHIFF-SERTORIO, H., Laboratoire d'Anatomie physique compare, Universite de Gen~ve, CH-1200 Gen~ve, 4, rue Candolle SCHNEIDER, V., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 SCHNETTER, B., Zoologisches Institut der Universitat, D-87 WUrzburg, Rontgenring 10 SCHOENENBERGER, N., Laboratoire d'Anatomie physique compare, Universite de Gen~ve, CH-1200 Gen~ve, 4, rue Candolle SCHUEMPERLI, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 SEGESSER v. BRUNEGG, S., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstl ergasse 16 SPATZ, Ch., Institut fUr Biologie III (Genetik und Molekularbiologie) Universitat Freiburg, D-78 Freiburg i.Br., Schanzlestr. 9-11 STRAUSFELD, N.J., Max-Planck-Institut fUr biologische Kybernetik, D-74 TUbingen, Spemann strasse 38 STRECK, P., Universitat Regensburg, LS Biologie II, D-8400 Regensburg, Universitatsstr. 31 TOGGWEILER, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 XI VIRSIK-STRAUSFELO, R., Max-Planck-Institut fUr biologische Kybernetik, 0-74 TUbingen, Spemannstr. 38 VOGT, K., Max-Planck-Institut fUr biologische Kybernetik, 0-74 TUbingen, Spemannstr. 38 WEHNER, R., Zo:>logisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 WEHRHAHN, Ch., Max-Planck-Institut fUr biologische Kybernetik, 0-74 TUbingen, Spemannstr.38 WEILER, R., Zoologisches Institut der Universitat ZUrich, CH-8006 ZUrich, KUnstlergasse 16 WIEBKING, H., Springer-Verlag, 0-69 Heidelberg-1, Neuenheimer Landstrasse 28-30 ZETTLER, F., Zoologisches Institut der Universitat MUnchen, 0-8 MUnchen-2, Luisenstr. 14 ZIMMERMANN, G., Max-Planck-Institut fUr biologische Kybernetik, 0-74 TUbingen, Spe- mannstr. 38