Neurobiology of Sensory Systems Neurobiology of Sensory SysteDls Edited by R. Naresh Singh Tata Institute of Fundamental Research Bombay, India and Nicholas J. Strausfeld The University of Arizona Tucson, Arizona Springer Science+ Business Media, LLC Library of Congress Cataloging in Publication Data International Conference on Neurobiology of Sensory Systems (1st: 1988: Velha Goa, India) Neurobiology of sensory systems / edited by R. Naresh Singh and Nicholas J. Strausfeld. p. cm. "Proceedings of the First International Conference on Neurobiology of Sensory Systems, held September 25-30,1988, in Goa, India"—T.p. verso. Includes bibliographical references. ISBN 978-1-4899-2521-3 1. Senses and sensation —Congresses. 2. Comparative neurobiology —Congresses. I. Singh, R. Naresh. II. Strausfeld, Nicholas James, 1942- . III. Title. [DNLM: 1. Neurobiology—congresses. 2. Receptors, Sensory—physiology— congresses. 3. Sense Organs —physiology-congresses. WL 70015908 1988] QP431.157 1988 591.1/82-dc20 DNLM.DLC 89-22960 for Library of Congress CIP ISBN 978-1-4899-2521-3 ISBN 978-1-4899-2519-0 (eBook) DOI 10.1007/978-1-4899-2519-0 The cover design is inspired by the hand gestures used to depict the five senses in the "Kathakali" style of Indian Classical Dance. These are, clockwise from the top: vision, smell, touch, taste, and hearing. Proceedings of the First International Conference on Neurobiology of Sensory Systems, held September 25-30, 1988, in Goa, India © 1989 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1989 Softcover reprint of the hardcover 1st edition 1989 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE The traveller to India is urged to visit that country's western shore with the Arabian Sea where, about 300 miles to the south of Bombay, an exceedingly lovely coast reaches the peak of its harmony at the erstwhile Portuguese enclave of Goa. The ambience of this alluring province is an exquisite balance of palm trees and rice fields, aged colonial homes - many still elegant and brightly painted - slowly being swallowed up by the exuberant tropical vegetation, incredible blossoms, colorful and courteous people and, deeper inland, some splendid examples of 17th and 18th century Portuguese ecclesiastical architecture. A feast for the eyes by day, and in the evening enough fresh fish and other good food to satisfy the most demanding gourmet. This was the paradisiacal setting for the first International Conference on the Neural Organization of Sensory Systems (ICONOSS for short), sponsored jointly by the International Brain Research Organization (IBRO), the Tata Institute for Fundamental Research at Bombay, the Department of Atomic Energy of the Government of India, and the Department of Science and Technology of the Government of India. About 100 participants were pleasantly confined at Fort Aguada, a resort cunningly built amongst the ruins of an old Portuguese fort. The conference program achieved an international flavor, recruiting scientists from many nations: India (naturally), Australia, Britain, Canada, Germany, Finland, France, Hungary, Japan, the Netherlands, Sweden, Switzerland and the United States of America. The subjects discussed were as diverse as the countries represented. And although the location alone imbued everyone with an irresistible feeling of collegiality and well-being, what unified the participants was a shared fascination with how sensory systems are organized and operate. This volume summarizes the diverse topics discussed, ranging from mechanosensory receptors of spiders to the mosaic organization of vertebrate photoreceptors, from how crabs view a flat world with eyes on stalks to how bats perceive a three-dimensional world using their mouths and ears, from the perception of speech to the perception of what bits go where in copulating crickets. A vital function ot any international meeting is to dispose of boundaries that humankind in its stupidity has erected between cultures. One great value of scientific pursuit is to provide a common culture through intellectual hybridization. And so it was at this conference: a meeting that introduced scientists from different lands to each other and their research. We departed enriched by the hospitality of our Indian hosts, the beauty of Goa, and by the open and enthusiastic exchange of ideas. For those that were not there, we hope that this volume conveys the spirit as well as the substance of this meeting and whets the appetite for the promise of more to come. The Editors v FOREWORD AND ACKNOWLEDGEMENTS We perceive the world around us through our sensory systems, which function as the windows of our brain, and on which learning, memory and the whole richness of experience depend. The senses provide us with the pleasures of life: beauty, aroma, taste, music and touch. And, too, the pressures and the pain, the perception of which, in common with other organisms, is crucial to our survival. The idea of organizing an International Conference on the neurobiology of sensory systems came to mind about three years ago. Initially, I explored the possibility of holding the conference at the Tata Institute of Fundamental Research (TIFR), Bombay. However, after some exploratory efforts, I realized that the Institute has grown too large and its facilities, like the guest house and the canteen, would not be able to take on the additional load of such an international conference. We then explored places where we could have the conference. The criteria for selection were (1) living conditions should be good and hygienic and (2) all the participants should be accommodated on the same campus so that there would be ample time and opportunity for fruitful and effective interaction at scientific and personal levels. The younger scientists were more likely to benefit from the more established ones in such an atmosphere. The choice of the Fort Aguada Beach Resort and the Taj Holiday Village as the venue of the Conference was made not only on these criteria but also on the basis of the happy experience of some of the other members of the TIFR, who had organized international conferences there earlier. A potential disadvantage of holding the Conference away from the home institution and, at a rather luxurious place as well, would have been that not many participants from within the country would be able to bear the cost of attending. Happily we were able to support several of them through local hospitality or reimbursement of travel expenses or both. And I may say that all who had shown a real interest in the conference were accommodated. This was made possible through the kind support of the following: Tata Institute for Fundamental Research, Bombay International Brain Research Organization Department of Atomic Energy, Government of India Department of Science and Technology, Government of India Honorable Chief Minister and Government of Goa Toshniwal Brothers (Bombay) Limited Company vii Scientific and Engineering Supply Company, Bombay The Taj Group of Hotels, India. I thank all the Members of the International Scientific Advisory Council and the National Organizing Committee for their keen interest and valuable suggestions on many occasions. My appreciation goes to the Members of the Local Organizing Committee for their whole-hearted cooperation. My special thanks are due to M. A. Parelker, the Administrative Secretary of the Conference, for our many discussions about the various organizational aspects, and who provided moral support when it was needed in quite a few anxious moments. Very notable help was rendered by my colleagues Shubha Shanbag, the Scientific Secretary; Seema Deshpande, the Treasurer; Veronica Rodrigues; Chetan Premany; and Kusum Singh who besides being my partner in life has also been an excellent scientific colleague. For the successful conclusion of any project such as this, one seeks the help of many people at various times and stages. Usually one encounters three kinds of individuals: the first are helpful, the second unhelpful. The former give us happiness and strength to go ahead with the project, while the latter make us more resolute and determined for its success. However, the overwhelming joy of life comes from meeting people of another type -- the third kind -- who came to us on their own accord and offered whatever help they could give. Such were Anindya Sinha, Archana Gayatri, Shashi Acharya, Vishwas Saranghdar, Rasmi Sood, Rohini Balakrishnan, Cheryl Lobo, Joyce Fernandes, Raghu Ram, M. M. Kakeri and H. G. Chauhan. My special thanks are due to the former Editor Lisa Honski and the present Editor Melanie Yelity, and their colleagues at Plenum Press with whose excellent cooperation and help the publication of the Proceedings of the Conference has been expedited in the shortest possible time. I also thank all the authors for their contributions. For retyping of certain manuscripts I thank Ms Jennifer Lawrence at the Division of Neurobiology, Arizona Research Laboratories, University of Arizona, and for expert language-editing, Dr. Camilla Strausfeld, at the University of Arizona. The papers presented in this volume have been broadly arranged according to the subject area: vision -- behavior, systems analysis, development and functional organization; olfaction, taste and receptor channels; auditory, tactile and nociception. I hope this volume "Neurobiology of Sensory Systems" will serve as a ready reference to young and future research workers. The Convener R. Naresh Singh INTERNATIONAL CONFERENCE ON NEUROBIOLOGY OF SENSORY SYSTEMS GOA 19B8 viii CONTENTS VISION: Physiology, Functional Organization, Behavior and Developmental Models Primitive Vision Based on Sensing Change . . . . . . . . . . . . . . . . . . . . . . . . .. 1 G.A. Horridge Pupil Control in Compound Eyes: More than One Mechanism in Moths ..... 17 D.-E. Nilsson, I. Henrekson, and A.C. Jarema Early Visual Processing in the Compound Eye: Physiology and Pharmacology of the Retina-Lamina Projection in the Fly ............ 23 R.c. Hardie, Simon Laughlin, and Daniel Osorio Analysis of Sensory Spike Trains ................................ 43 Hiroko M. Sakai Signal Coding and Sensory Processing in the Peripheral Retina of the Compound Eye ..................................... 53 Matti Jarvilehto, Matti Weckstrom, and Eero Kouvalainen Dynamics of Second-Order Neurons of Cockroach Ocelli ................ 71 Makoto Mizunami Processing of Movement Information in the Fly's Landing System: A Behavioral Analysis ..................... . . . . . . . . . . . . . . . . 85 Alexander Borst and Susanne Bahde Motion Sensitivity in Insect Vision: Roles and Neural Mechanisms ....................................... 97 M. V. Srinivasan Response Behaviour of Elementary Movement Detectors in the Visual System of the Blowfly . . . . . . . . . . . . . . . . . . . . . . . . . .. 107 R. Bult, F.H. Schuling, and H.A.K. Mastebroek Spatial Vision in a Flat World: Optical and Neural Adaptations in Arthropods ............................ 123 J. Zeil, G. Nalbach, and H.-O. Nalbach ix Search and Choice in Drosophila ............................... 139 K.G. Gatz The Evolution of the Tiered Principal Retinae of Jumping Spiders (Araneae: Salticidae) 155 A David Blest and David O'Carroll Developmental Studies on the Optic Lobe of Drosophila Using Structural Brain Mutants . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 171 K.F. Fischbach, F. Barleben, U. Boschert, AP.M. Dittrich, B. Gschwander, B. Hoube, R. Jager, E. Kaltenbach, RG.P. Ramos, and G. Schlosser Developmental Genetic and Molecular Analyses of Lethal (1) Ogre, a Locus Affecting the Postembryonic Development of the Nervous System in Drosophila melanogaster . . . . . . . . . . . . . . . . . .. 195 Douglas R. Kankel, Toshiki Watanabe, R Naresh Singh, and Kusum Singh Development and Fine Structure of the Nervous System of Lethal (1) Optic Ganglion Reduced Visual Mutants of Drosophila melanogaster .................................. 203 R Naresh Singh, Kusum Singh, and Douglas R Kankel Critical Developmental Phases in the Ontogeny of Human Lateral Geniculate Nucleus During Prenatal Life . . . . . . . . . . . . . . . . . . 219 Shashi Wadhwa and Veena Bijlani In Oculo Differentiation of Embryonic Neocortex into Retina in Adult Rat .................................. 231 Gomathy Gopinath, Ashok Kumar Shetty, Ranjita Banerjee, and P.N. Tandon Axonal Outgrowth and Process Placement of Sensory Lumbar Neurons in the Nematode Caenorhabditis elegans ....................... 241 Shahid S. Siddiqui Recent Progress in the Identification of Neurotransmitters Used by Vertebrate and Invertebrate Photoreceptors ............... 267 P. Vijay Sarthy Colour Vision and Immunologically Identifiable Photoreceptor Subtypes .... 275 A Szel and Pal Rahlich Chemical Neuroanatomy of the Insect Visual System . . . . . . . . . . . . . . . . . . 295 Dick R. Nassel x OLFACTION AND TASTE: Comparisons with Other Senses, Anatomy, Physiology, Genetic Analysis, Ion Channel Models Insect Vision and Olfaction: Common Design Principles of Neuronal Organization .................................... 319 N.J. Strausfeld Identified Glomeruli in the Antennal Lobes of Insects: In variance, Sexual Variation and Postembryonic Development ................. 355 Jean-Pierre Rospars and Irene Chambille Drosophila Chemoreceptors .................................... 377 Renee Venard, Claude Antony, and Jean-Marc lallon The Antennal Glomerulus as a Functional Unit of Odor Coding in Drosophila melanogaster .................................. 387 Veronica Rodrigues and Ludwin Pinto Complex Chemical Messages in Drosophila melanogaster . . . . . . . . . . . . . . . . . 397 Jean-Francois Ferveur, Matthew Cobb, and Jean-Marc lallon The Isolation of Antennal Mutants and Their Use in Drosophila Olfactory Genetics ............................... 411 Richard Ayer, Paula Monte, and John Carlson Isolation of Autosomal Behavioral Mutations in Drosophila ............. 419 Satpal Singh, Maninder J.S. Chopra, Poonam Bhandari, and Devasis Guha Projections and Functional Implications of Labellar Neurons from Individual Sensilla of Drosophila melanogaster ................. 427 Shubha R. Shanbhag and R. Naresh Singh Cationic Acceptor Sites on the Labellar Chemosensory Neurons of Drosophila melanogaster ............................ 439 Swati Joshi, Kavita Arora, and Obaid Siddiqi Drosophila Homologs of Vertebrate Sodium Channel Genes ............. 449 Mani Ramaswami, Ali Lashgari, Mark A. Tanouye ACOUSTIC PERCEPTION, MECANORECEPTION AND NOCICEPTION The Functional Organization of the Auditory Brainstem in the Mustache Bat and Mechanisms for Sound Localization ............. 469 George D. Pollak xi