CONTRIBUTORS A. M. BROWN L. H. FINLAYSON JOHN P. HESLOP M. P. OSBORNE J. D. PYE ADVANCES IN Comparative Physiology and Biochemistry Edited by O. LOWENSTEIN Neurocommunications Research Unit University of Birmingham, England VOLUME 6 ® 1975 ACADEMIC PRESS New York San Francisco London A Subsidiary of Harcourt Brace Jovanovich, Publishers COPYRIGHT © 1975, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER. ACADEMIC PRESS, INC. Ill Fifth Avenue, New York, New York 10003 United Kingdom Edition published by ACADEMIC PRESS, INC. (LONDON) LTD. 24/28 Oval Road, London NW1 LIBRARY OF CONGRESS CATALOG CARD NUMBER: 61-10693 ISBN 0-12-011506-9 PRINTED IN THE UNITED STATES OF AMERICA CONTRIBUTORS TO VOLUME 6 Numbers in parentheses indicate the pages on which the authors' contributions begin. A. M. BROWN (1), Department of Zoology, University of London King's College, Strand, London, England L. H. FINLAYSON (165), Department of Zoology and Comparative Physi ology, University of Birmingham, England JOHN P. HESLOP (75), Agricultural Research Council Unit of Invertebrate Chemistry and Physiology, Department of Zoology, University of Cambridge, England M. P. OSBORNE (165), Department of Zoology and Comparative Physi ology, University of Birmingham, England J. D. PYE* (1), Department of Zoology, University of London King's College, Strand, London, England * Present Address: Department of Zoology & Comparative Physiology, Queen Mary College, Mile End Road, London El 4NS, England. vi PREFACE The articles presented in this volume are related by their common relevance to comparative neurophysiology. In the account on high-frequency hearing in mammals, the sensitivity to, production, and behavioral utilization of high-frequency sound are comparatively reviewed for a wide variety of mammals ranging from bats, rodents, whales, dolphins, and seals to the insectivores, primates, edentates, and carnivores. The other two papers deal with closely related neurological topics and are to a certain extent complementary. In the first, the axonal flow and fast transport in nerves is the subject of a thorough scrutiny of synthetic sites in the neuron and the mode and rate of transport. Special attention i& paid to the differences in substrate and mechanism in slow and fast transport. The neuron is presented as a suitable cell type for the investi­ gation of intracellular transport in general. The second paper deals with the secretory activity of neurons and related electrical activity. It presents a comparative assessment of all "neurocrine" activities, be they in the service of neuroendocrine coordina­ tion or of synaptic transmission of information. Special attention is paid to the nature of vesicles containing the neurosecretions and transmitter substances and to the mechanisms of release. The electrical events accom­ panying such neurocrine activities are described and critically discussed. 0. LOWENSTEIN Vll CONTENTS OF PREVIOUS VOLUMES Volume 1 DIGESTIVE ENZYMES E. J. W. Barrington THE AMINE OXIDASES OF MAMMALIAN BLOOD PLASMA H. Blaschko TEMPERATURE RECEPTORS R. W. Murray NEUROMUSCULAR PHYSIOLOGY G. Hoyle ANIMAL LUMINESCENCE J. A. C. Nicol RESPIRATORY MECHANISMS AND THEIR NERVOUS CONTROL IN FISH G. M. Hughes and G. Shelton AUTHOR INDEX—SUBJECT INDEX Volume 2 COMPARATIVE ELECTROBIOLOGY OF EXCITABLE MEMBRANES Harry Grundfest THE COMPARATIVE PHYSIOLOGY OF INVERTEBRATE CENTRAL NEURONS Donald Kennedy PHYSIOLOGY AND BIOCHEMISTRY OF KNALLGASBACTERIA H. G. Schlegel COMPARATIVE PHYSIOLOGY OF MARSUPIALS H. Waring, R. J. Moir, and C. H. Tyndale-Biscoe AUTHOR INDEX—SUBJECT INDEX Volume 3 VARIATION IN ENZYME STRUCTURE AND FUNCTION : THE GUIDELINES OF EVOLUTION D. C. Watts MOLECULAR ASPECTS OF CYTODIFFERENTIATION John Paul IX X CONTENTS OF PREVIOUS VOLUMES THE COMPARATIVE METABOLISM OF XENOBIOTICS J. N. Smith THE BIOCHEMISTRY OF SUPPORTING MATERIALS IN ORGANISMS M. V. Tracey CRUSTACEAN METABOLISM A. K. Huggins and K. A. Munday AUTHOR INDEX—SUBJECT INDEX Volume 4 EFFECTS OF ENVIRONMENTAL CONDITIONS ON THE MOTILE BEHAVIOR OF AMEBAS Theodore L. Jahn and Eugene C. Bovee MECHANISMS AND COORDINATION OF CELLULAR LOCOMOTION Lev N. Seravin HYPOTHALAMIC CONTROL OF PITUITARY FUNCTION IN SUBMAMMALIAN VERTEBRATES J. M. Dodd, B. K. Follet, and P. J. Sharp CENTRAL AND PERIPHERAL CONTROL OF ARTHROPOD MOVEMENTS W. H. Evoy and M. J. Cohen THE COMPARATIVE PHYSIOLOGY OF GAMETE POPULATIONS Jack Cohen AUTHOR INDEX—SUBJECT INDEX Volume 5 FEEDING AND DIGESTION IN THE BIVALVIA Gareth Owen COMPARATIVE PHYSIOLOGY OF REPRODUCTION IN ARTHROPODS K. G. Adiyodi and R. G. Adiyodi ISOENZYMES, MULTIPLE ENZYME FORMS, AND PHYLOGENY C. J. Masters and R. S. Holmes SUBJECT INDEX Auditory Sensitivity at High Frequencies in Mammals A. M. BROWN AND J. D. PYE* Department of Zoology, University of London King's College, Strand, London, England I. Methods 2 A. Behavioral Responses 2 B. Cochlear Microphonic (CM) Responses 3 C. Neural Responses 3 D. Limitations of Different Techniques 4 E. Tissue Conduction 6 II. Bats 7 A. Echolocation Sounds of Bats 7 B. Auditory Investigations of Bats 10 C. Use of Sound by Bats 28 D. Summary 29 III. Rodents 30 A. History of Hearing Studies 30 B. Sounds Produced by Rodents 32 C. Review of the Most Commonly Investigated Forms 33 D. Use of Sound by Rodents 40 E. Summary 41 IV. Cetacea and Pinnipedia 41 A. Cetacea 42 B. Pinnipedia 48 V. Other Species 50 A. Insectivores 50 B. Primates 51 C. Edentates 52 D. Carnivores 52 VI. Anatomical Correlates of High-Frequency Hearing 53 A. External Ear 53 B. Middle Ear 54 C. Cochlea 55 D. Central Nervous System 58 VII. Summary and Conclusions 59 References 60 The terms "ultrasound" and "ultrasonic hearing" are generally used to describe sounds and auditory sensitivity above approximately 17-20 * Present address: Department of Zoology & Comparative Physiology, Queen Mary College, Mile End Road, London El 4NS, England. 1 2 A. M. BROWN AND J. D. PYE kHz, that is, above the upper frequency limit of human hearing. There is increasing evidence that this upper limit is low among mammals (see Masterton et al., 1969; Manley, 1971), and it is intended here to review the present state of knowledge about high-frequency hearing. This must involve a detailed discussion of those forms in which particular sensitiv­ ity to high frequencies is now well known, namely bats, rodents, and cetacea; but it will also include a brief consideration of other forms in which hearing has been indicated in various ways up to high frequencies. Finally, it is intended to discuss the anatomical peculiarities that have been associated with high-frequency hearing. I. METHODS Before considering in detail the groups of animals known to exhibit high-frequency sensitivity, it is necessary to review briefly the various test techniques used and to discuss their relative advantages and draw­ backs. There are three main methods used for obtaining information about the auditory capabilities of mammals. These are the observation of many possible types of behavioral response, the recording of the cochlear microphonic (CM) responses, and the recording of neural activ­ ity from the eighth nerve or higher centers in the auditory nervous sys­ tem. In addition, the physical vibration of the tympanic membrane, stapes, and basilar membrane have been measured, using the Mössbauer effect (Johnstone and Boyle, 1967; Manley et al, 1972). A. Behavioral Responses 1. Reflexes Many simple reflexes normally produced in response to sounds have been used to give an indication of hearing ability. For instance, Preyer's reflex (pinna twitch), the vibrissa-twitching reflex, and a shrug of the skin of the back have been used, by Schleidt (1952) in rodents. A rapid, retrad jerk of the head in response to sound has been observed in hedge­ hogs by Chang (1936). Middle ear reflexes have been observed in bats, using the cochlear potentials as indicators (Galambos, 1942b; Wever and Vernon, 1961a; Henson and Henson, 1972). Audiogenic seizures in rodents have been used to obtain hearing curves in mice by Dice and Barto (1952) and Darrouzet and Guilhaume (1967). Sound has been shown to inhibit vocalization in the normally very vocal sea lion (Schus- terman et al, 1972). HIGH-FREQUENCY HEARING IN MAMMALS 3 2. Conditioned Responses A simple conditioned reflex (type 1) has been used in the measurement of galvanic skin resistance (GSR) after preconditioning of sound to mild electric shock in mice (Finck and Berlin, 1965). Operant conditioning techniques (conditioned reflex type 2) have been used in a variety of mammals to obtain hearing curves. They involve training an animal to respond to a tone with a particular action, such as pressing a lever, to obtain a reward. Members of all three of the major groups to be discussed here have been studied by this method, including dolphins by Johnson (1966), rats by Gourevitch and Hack (1966), and bats by Dalland (1965a,b). Dalland (1970) has described his methods in some detail. The literature on behavioral audiometry in mammals has recently been reviewed in detail by Francis (1975, in press). B. Cochlear Microphonic (CM) Responses The CM response may be recorded from within the cochlea by using fine intracochlear electrodes for differential recording from the scala media and scala tympani or scala vestibuli along the length of the coch­ lea. The most favored site for recording the gross CM response is the round window. This is frequently done using a silver wire electrode, since silver may be easily melted to form a terminal bulb to place on the round window membrane, but other metals are also employed. The most com­ monly used stimulus is a train of tone pulses containing terminal ramps that are gradual enough to minimize the other frequencies (sidebands or "transients") generated. Recently Brown (1970, 1973a,c) has used broad-band sounds with an approximately flat spectrum caused by a train of sparks in air. The re­ sponse to a train of sparks at a rate of 200 Hz was recorded on tape and later displayed as an integrated spectrum on a sonagraph (sound spectrograph). This technique gave rapid results, showing the frequency response curve of the cochlea to a constant intensity distribution without the necessity of recording at several frequencies in turn. An example is shown in Fig. 1. C. Neural Responses Recording from the auditory nervous system may be accomplished with fine microelectrodes recording from single units at all levels. This tech­ nique has been used extensively in bats (Suga, 1964-1972; Grinnell, 1963-1973) to investigate the behavior of large samples of single units within a particular neural complex. Gross electrodes have been used to