Handbook of Sensory Physiology – serie

This volume was designed to focus on the problems of perception and originally was to have been solely edited by Professor Hans-Lukas Teuber who was a member of the editorial board which initiated production of the Handbook. Accordingly, he issued invitations to a number of researchers III perception asking them to contribute chapters written in a style described III his words: " . . . Ire hope that no author lI'ill feel COl/strained to undertake a major search of the literature: he could In'ite, instead. on an area in which he has been quite actire himse?t~ and II'here most of the issues are immediately obt"ious to him. In this Iray, the IITiting of the chapter should be cnjoyable rather than a chore . . it should result in a personal account of the state of a given area rather than in an encyclopedic treatise . . . the field deserves this sort of summary ret'iell", particularly (f it is pointed toward the future and speeds the convergence of det'elopments in sensory physiology and psychological studies of perception, " With the growing burden of national and international commitments includ­ ing departmental headship, Professor Teuber felt that it would be wise to share the editorial responsibilities for this volume and accordingly, asked Professors Richard Held and Herschel Leibowitz to co-edit the volume with him in the same spirit as outlined in his invitation to authors. They agreed to help in this task.

Why should there be a handbook of sensory physiology, and if so, why now' The editors have asked this question, marshalled all of the arguments that seemed to speak against their project, and then discovered that most of these arguments really spoke in favor of it: there seemed to be no doubt that the attempt should be made and that it should be made now. No complete overview of sensory physiology has been attempted since Bethe's "Handbuch der normalen und pathologischen Physiologie", nearly forty years ago. Since then, the field has evolved with unforeseen rapidity. Although electric probing of single peripheral nerve fibers was begun by ADRIAN and ZOTTERMAN as early as 1926, in the somatosensory system, and extended to single optic nerve fibers by HARTLINE in 1932, the real upsurge of such single-unit studies has only come during the last two decades. Single-cell electrophysiology has now been applied to all sensory modalities and on almost every conceivable phylogenetic level. It has begun to clarify peripheral receptor action and is adding to our. understanding of the central processing of sensory information. In parallel with these developments, there have been fundamental studies of the physics and chemistry of the receptors themselves: these studies are leading to insights into the mechanisms of energy transduction and nerve impulse initiation.

Radiation can only affect matter if absorbed by it. Within the broad range of 300-1000 nm, which we call "the visible", light quanta are energetic enough to produce excited electronic states in the atoms and molecules that absorb them. In these states the molecules may have quite different properties from those in their dormant condition, and reactions that would not otherwise occur become possible. About 80 % of the radiant energy emitted by our sun lies in this fertile band, and so long as the sun's surface temperature is maintained at about 6000° C this state of affairs will continue. This and the transparency of our atmosphere and waters have allowed the generation and evolution of life. Before life began the atmosphere probably also transmitted much of the solar short-wave radiation, but with the rise of vegetation a new product - oxygen - appeared and this, by a photochemical reaction in the upper atmosphere, led to the ozone layer that now protects us from the energetic "short-wave" quanta that once, perhaps, took part in the generation of life-molecules. Light is an ideal sensory stimulus. It travels in straight lines at great speed and, consequently, can be made to form an image from which an animal can make "true", continuous and immediate assessments of present and impending events.

Olfaction is involved intimately in two of the most basic functions of animals: food intake and reproduction. There are also many other involvements of olfaction in animal behavior, not the least being communication. The authors of this volume have collected and evaluated the comparative anatomy, electron microscopy, electrophysiology, genetics, psychology, chemistry, and biophysics of the olfactory system and then indicated their roles in animal behavior. The importance of olfaction in the everyday life of an animal is just being realized fully and recent years have brought forth a great surge of research in this area. The diverse dis­ ciplines that contribute to our understanding of olfaction make the development of this volume rewarding for those working in this field. The olfactory system's very high sensitivity and its great power of molecular discrimination interests many chemists and physicists. Data from the study of both vertebrates and insects show that only one molecule of certain odors is necessary to stimulate a single olfactory receptor! The underlying physicochemical events are not yet understood. Also, many mammals can discriminate quickly the difference between two odors of similar structure. Thus the olfactory epithelium and the more centrally located neural components present the ultimate in chemical detection and analysis by a biological system. The principles involved are probably common to those of many other organs.

Taste receptors monitor the quality of all the food ingested. They are intimately involved in both food acceptance and rejection. The sensation of taste is also important in the regulation of many specific chemicals necessary for maintenance of the body. For example, disturbance of the adrenal glands results in a change in the intake of salt which is necessary for regulation of the sodium balance. Curt Richter's early studies on specific hungers and preference thresholds initiated a large number of studies in this field. The relationship between taste and food intake is now well recognized by physiologists, psychologists and nutritionists. Our current concepts of the neural coding of taste quality and intensity are largely based upon the classical paper by PFAFFMANN in 1941. Many subsequent single nerve fiber studies have added to our understanding. In recent years Zotterman and Diamant have successfully recorded from the human taste nerves as they pass through the middle ear. This allowed them to study the relationships between the response of taste receptors and the resultant taste sensation. No similar feat has yet been accomplished with the visual and auditory systems.

This series of concise essays on Enteroceptors is designed to interest the gradu­ ate student and to stimulate research. Even before the advent of electrophysiological studies, classical physiological techniques had shown the essence of the role of many of the enteroceptors. Thus the monitoring influence of the cardiovascular mechanoreceptors on the heart and on the systemic vascular resistance, the role of the arterial chemoreceptors in hypoxia and the influence of the so-called Hering Breuer stretch receptors on breathing had all been documented. The pioneering work of ADRIAN, BRONK, ZOTTERMAN and others using electroneurographic methods gave a remarkable impetus to the study of the enteroceptors themselves. Nowhere is this better exemplificd than in the case of the afferent end organs of the heart, the respiratory tract and the abdominal and pelvic viscera. The remarkable development of our knowledge of the multiplicity of types of nerve endings from the thoracic and abdominal viscera acquired from electrophysiological studies has refocussed our attention on the histological details of the sites of such receptors. Once more research on the structural side has been accelerated by the question raised by evidence obtained from functional studies. This is well illustrated in the case of the carotid body, where the long cherished belief that the innervated epithelioid cells constitute the chemoreceptor complex is now under attack. The detailed consideration of the functional characteristics of each entero­ ceptor considered has not occupied our whole attention.

This volume is a collection of essays which attempts to summarize the recent progress in the field of photoreceptor and retinal physiology. Reflecting the way in which research is organized, each author reports on the studies performed with the techniques with which he is most familiar: morpholo­ gical, chemical or physiological. The first chapters describe the structure of visual cells and the histological architecture of the retina. Next comes a summary of the laws governing photochemical reactions and a report on the biochemistry of photopigments. Four articles cover the optical properties of invertebrate eyes and the electrophysiology and the interactions of their photoreceptors. These are followed by a discussion of the properties of vertebrate eyes, including chapters on optics, on the electrical responses of rods and cones and on the functional organization of the retina. The final chapter provides an extensive review of retinal biochemistry and metabolism. Even though the experimental approach differs, all studies are directed toward the solution of two basic problems: transduction in the photoreceptors and orga­ nization (often called "information processing") in the retina. The central problem of photoreceptor cells is to determine how light produces a response. We know that illumination evokes electrical changes and we have recently learned a great deal about the features of these changes. The evidence indicates however that elaborate processes must be interposed between the ab­ sorption of photons by the pigment and the production of electric currents through the membrane. These intermediary cvents remain to be unraveled.

The present volume covers the physiology of the visual system beyond the optic nerve. It is a continuation of the two preceding parts on the photochemistry and the physiology of the eye, and forms a bridge from them to the fourth part on visual psychophysics. These fields have all developed as independent speciali­ ties and need integrating with each other. The processing of visual information in the brain cannot be understood without some knowledge of the preceding mechanisms in the photoreceptor organs. There are two fundamental reasons, ontogenetic and functional, why this is so: 1) the retina of the vertebrate eye has developed from a specialized part of the brain; 2) in processing their data the eyes follow physiological principles similar to the visual brain centres. Peripheral and central functions should also be discussed in context with their final synthesis in subjective experience, i. e. visual perception. Microphysiology and ultramicroscopy have brought new insights into the neuronal basis of vision. These investigations began in the periphery: HARTLINE'S pioneering experiments on single visual elements of Limulus in 1932 started a successful period of neuronal recordings which ascended from the retina to the highest centres in the visual brain. In the last two decades modern electron­ microscopic techniques and photochemical investigations of single photoreceptors further contributed to vision research.

The waterproof sensory sheet covering the mammalian body has a rich afferent innervation which provides an abundance of complex information for use by the central nervous system often in conjunction with information from receptors in the joints. This book is an attempt to provide a systematic account of the way in which this somatosensory system works. The properties of the peripheral receptors have been debated in scientific terms for about a century and the resolu­ tion of the conflict in favour of the existence of 'specific' receptors for mechanical, thermal and noxious stimuli is reported and discussed in the opening chapters of the book. An awareness of this specificity has forced a re-consideration of the ways in which the central nervous system de-codes the information which is showered upon it. Advances in knowledge of the fine structure of the central nervous system have raised functional questions about the operation and organisation of the sensory systems in the spinal cord and brain. Fresh insight into the morphological complexity of the dorsal horn and higher levels of the nervous system gives the physiologist a clearer idea of the units with which he works. Progress has been made in understanding the function of sensory relay nuclei in general and indivi­ dual tracts in particular and is fully decomented.

In planning The Handbook volumes on Audition, we, the editors, made the decision that there should be many authors, each writing about the work in the field that he knew best through his own research, rather than a few authors who would review areas of research with which they lacked first hand familiarity. For the purposes of the chapters on Audition, sensory physiology has been defined very broadly to include studies from the many disciplines that contribute to our understanding of the structures concerned with hearing and the processes that take place in these structures in man and in lower animals. A number of chapters on special topics have been included in order to present information that might not be covered by the usual chapters dealing with anatomical, physi­ ological and behavioral aspects of hearing. We wish to thank all authors of the volumes on Audition for the contributions that they have made. We feel confident that their efforts will also be appreciated by the many scientists and clinicians who will make use of the Handbook for many years to come. WOLF D. KEIDEL WILLIAM D. NEFF Erlangen Bloomington August 1974 Contents Introduction. By G. v. BEKESY t. With 3 Figures. . . . . . . . 1 Chapter 1 Consideration of the Acoustic Stimulus. By R. R. PFEIFFER. With Chapter 2 19 Figures. . . . . . . . . . . . . . . . . . . . . . . . . 9 Comparative Anatomy of the Middle Ear. By O. W. HENSON Jr. With Chapter 3 23 Figures. . . . . . . . . . . . . . . . . . . . . . . 39 . . . . .

The function of the vestibular system is not as obvious as those of vision, hearing, touch or smell. Vestibular dysfunction, however, is clearly apparent where lesions are present. It is probably for this reason that the vestibular sense was not discovered until the nineteenth century and that clinicians have continued to playa major role in basic vestibular research right up to the present. The relationship between basic and clinical research is certainly stronger in the vesti­ bular field than in that of tactile sensation, for instance, as testified by the work of clinicians as MENIERE, BREUER, BARANY, DEKLEIJN and FRENZEL. In this respect the situation is similar in vestibular physiology and in endocrinology, and for the same reason. This second part of the vestibular volume of the Handbook of Sensory Physio­ logy will be of interest to neurologists, otologists, neurosurgeons, ophthalmologists and physiotherapists on the one hand, and psychologists, physiologists, engineers and aviation specialists on the other. For a full understanding of Part 2, it is necessary to have assimilated the basic anatomy, physiology, and biochemistry of Part 1.

The originality of this volume is to reveal to the reader the fascination of some unfamiliar sensory organs that are sometimes ignored and often misunderstood. These receptors have only recently been identified and their functional specificity is in some cases still a matter for discussion. The four classes of sensory organs considered here differ widely from one another in many respects. One might even say that the only thing they have in common is that they belong to cold-blooded vertebrates. These classes are: 1. the directionally sensitive lateral-line mechanoreceptors of fishes and amphi­ bians (Chapter 7); 2. the pseudobranchial organs of some teleosts, equipped with pressoreceptors and at least three other types of receptors (osmo- and chemoreceptors) (Chapter 8); 3. the infrared-sensitive pit organs of some snake families (Chapter 9) ; 4. the various kinds of electroreceptors found in several marine and freshwater fish families (Chapters 2 to 6). The first three classes of receptors mentioned above thus rate only one chapter each, whereas five chapters are devoted to the electroreceptors. Electroreception has aroused enormous interest among physiologists in specialties ranging from molecular biology to animal behavior. The resulting quantity of research and discussion fully justifies this disproportion. However, it cannot be denied that the contents of the volume must appear unbalanced and heterogeneous, yet it should not be perceived as a mere juxtaposition of particular and unrelated cases.

The details of the receptor mechanism are not yet fully understood for any sensory system. However, sufficient data are available (for the vestibular system and for other systems) to permit meaningful tracking of the sensory messages through the nervous system and via conscious experience. The reception, process­ ing, storage and output of information in man and other animals, as done by means of receptors, neurons, secretory cells and muscle fibers, are collectively referred to as mind. Sensory physiologists tend to disbelieve in extrasensory perception. Sensory physiology in general is an area upon which different sciences and methods converge. Anatomists, physiologists, psychologists, physicists, chemists, and engineers have made important contributions to sensory physiology. What is special about vestibular physiology is the fact that many research workers are clinicians, living under the constant pressure of their patient's demands. This is a disadvantage when it comes to writing handbooks, but an advantage for the pa­ tient, since research is guided by clinical practice and can be quickly applied. Modern methods, such as recording from single nerve units and the correlation of electrophysiological and psychophysical data, have greatly contributed to our knowledge, yet the study of lesions is still important, especially in the vestibular field.

This section will consider the structure and function of muscle receptors, as well as the central nervous system mechanisms with which they are concerned. In volume I of this Handbook, receptor mechanisms are discussed in detail. Also, the crustacean stretch receptor and the frog muscle spindle have been considered. The present section will be concerned with vertebrate muscle receptors with an emphasis on mammals. Muscle receptors provide interesting examples of specialized mechanorecep­ tors. The muscle spindle is a striking case of a receptor which is regulated in its function by the central nervous system in efferent neurons. Muscle receptors have long been known to playa crucial role in the reflex regulation of movement. In recent years it has become apparent that these receptors are also important in sensory phenomena such as the perception of position and movement. St. Louis, July 1974 c.c. HUNT Contents Chapter I The Morphology of Muscle Receptors. By D. BARKER. With 99 Figures . . . . . . . . . . . . . . . .. 1 Chapter II The Physiology of Muscle Receptors. By C.C. HUNT. With 21 Figures . . . . . . . . . . . . . . . . . 191 Chapter III Central Actions of Impulses in Muscle Afferent Fibres. By A. K. McINTYRE. With 8 Figures 235 Author Index 289 Subject Index 299 List of Contributors BARKER, David Department of Zoology, University of Durham, Science Laboratories, South Road, Durham DH1 3LE, Great Britain HUNT, Carlton C. Department of Physiology and Biophysics, Washington University, School of Medicine, 660 South Euclid Avenue, St. Louis, Mo. 63110, USA McINTYRE, A. K.

nerve; subsequently, however, they concluded that the recordings had been from aberrant cells of the cochlear nucleus lying central to the glial margin of the VIII nerve (GALAMBOS and DAVIS, 1948). The first successful recordmgs from fibres of the cochlear nerve were made by TASAKI (1954) in the guinea pig. These classical but necessarily limited results were greatly extended by ROSE, GALAMBOS, and HUGHES (1959) in the cat cochlear nucleus and by KATSUKI and co-workers (KATSUKI et at. , 1958, 1961, 1962) in the cat and monkey cochlear nerve. Perhaps the most significant developments have been the introduction of techniques for precise control of the acoustic stimulus and the quantitative analysis of neuronal response patterns, notably by the laboratories of KIANG (e. g. GERSTEIN and KIANG, 1960; KIANG et at. , 1962b, 1965a, 1967) and ROSE (e. g. ROSE et at. , 1967; HIND et at. , 1967). These developments have made possible a large number of quanti­ tative investigations of the behaviour of representative numbers of neurons at these levels of the peripheral auditory system under a wide variety of stimulus conditions. Most of the findings discussed herein have been obtained on anaesthetized cats. Where comparative data are available, substantially similar results have been obtained in other mammalian species (e. g. guinea pig, monkey, rat). Certain significant differences have been noted in lizards, frogs and fish as would be expect­ ed from the different morphologies of their organs of hearing (e. g.

after heated and often bitter debates, SIEBENMANN'S opinion finally prevailed, i. e. , a contribution to cochlear lesions due to vibrations of the floor transmitted via bone conduction could not be demonstrated. For one thing, it was hard to see how appreciable amounts of energy could reach the ears in this manner, considering the attenuation that is bound to occur across each of the many joints along the pathway involved. In some older audiological surveys conducted in industry (e. g. , TEMKIN, 1933), groups of workmen were found who displayed signs of apical-turn lesions, i. e. , low-tone hearing losses for air and for bone. Such lesions could not be expected to results from exposure to air-borne sounds because of the low-frequency attenu­ ation of the middle ear. Although WITTMAACK'S explanation, which was frequently invoked in such reports, does no longer appear tenable, such apical-turn lesions could conceivably be caused by bone conduction components of high-intensity noise in the sense of BEKESY (1948). - As far as I am aware of, no newer studies have been conducted in this problem area, and the older experiments and/or surveys were done at times before signal parameters could be precisely controlled or measured. A detailed, critical review of the older studies on the potential contribution of bone-conducted energy to industrial hearing loss and its underlying pathology may be found in Werner (1940) who, incidently, favored SIEBENMANN'S point of VIew.

The vertebrate eye has been, and continues to be, an object of interest and of inquiry for biologists, physicists, chemists, psychologists, and others. Quite apart from its important role in the development of ophthalmology and related medical disciplines, the vertebrate eye is an exemplar of the ingenuity of living systems in adapting to the diverse and changing environments in which vertebrates have evolved. The wonder is not so much that the visual system, like other body systems, has been able to adapt in this way, but rather that these adaptations have taken such a variety of forms. In a previous volume in this series (VII/I) Eakin expressed admiration for the diversity of invertebrate photoreceptors. A comparable situation exists for the vertebrate eye as a whole and one object of this volume is to present to the reader the nature of this diversity. One result of this diversification of ocular structures and properties is that the experimental biologist has available a number of systems for study that are unique or especially favorable for the investigation of particular questions in visual science or neurobiology. This volume includes some examples of progress made by the use of such specially selected vertebrate systems. It is our hope that this comparative approach will continue to reveal new and useful preparations for the examination of important questions.

This preface is addressed to the reader who wishes to inquire into the prevailing concepts, hypotheses and theories about development of sensory systems and wants to know how they are exemplified in the following chapters. I believe that science is hypothesis and theory and that the growth and evolution of any branch of science can be measured by the degree to which its theories have been reified. By that standard, one must conc1ude that developmental neuro­ biologie is in its infancy. The rapid accumulation of observations which has occurred in this branch of science in the past century leads to progress only to the extent that the facts validate or falsify hypotheses. The following chapters show that we have a plethora of facts but a dearth of hypotheses. Another index of the maturity of any branch of science is its level of historical self-awareness. Because the history of any branch of science is essentially the history of ideas and of the rise and fall of theories, the level of historical awareness is related to the extent to which reification of its hypothetical constructs has advanced. It is largely because few theories of development of sensory systems, or indeed, of developmental neurobiology, have progressed far in the process of reification that the his tory of developmental neurobiology remains unwritten. The subject of this volume is hardly mentioned in the many books devoted to the history of related disciplines.

Morphology and physiology are two fields which cannot be separated. This statement needs to be amplified: purely factual results of a morphological or physiological nature only have real value when they are gained in the context of certain guiding, embracing questions. By themselves they are mostly of little value, because only a guiding hypothesis or theory is of any importance. Equally, a physiological question will always raise questions as to the morphological substrate, and vice versa. Thus, Wiedemann's discovery, for instance, that the visual cells in each ommatidium of the dipterans have differing fields of vision has revived the question as to what the optical properties of individual visual cells, and the complete ommatidium, might be and how neighboring ommatidia interact. These questions in turn led to that of the morphological, neuronal wiring diagram of the visual cells in the optical ganglia. Within the realm of invertebrates, the morphological and physiological problems of visual perception have been resolved in very different ways on various levels, from the photo­ receptor to higher centers; despite many investigations, however, there remain unsolved problems. The first chapter of Vol. VII/6B deals with the neuroarchitecture in the visual system of two groups: crustaceans and insects. These systems are best known through recent investigations. The second chapter is devoted to the neural principles in the visual system of insects. It could not have been written without parallel research into morphology.

In the comparative physiology of photoreception by the Protista and the invertebrates two aspects are emphasized: (1) the diversity of visual processes in these groups and (2) their bearing upon general mechanisms of photoreception. Invertebrates have evolved a far greater variety of adaptations than vertebrates­ modifications aiding survival in the remarkably different biotopes they occupy. The number of species in itself suggests this multiformity; each of them has peculiarities of its own, in morphology as well as in physiology and behavior. But these special adaptations are variations on a few great themes. Although the catalogue of invertebrate species is immense, the literature concerning them nearly rivals it in extent-even if one considers only that fraction dealing with visual physiology. Taxonomy proceeds by grouping the species, categorizing them in genera, families, orders, and progressively larger units. Similarly, comparative physiology aims at an analogous, more or less compre­ hensive, classification. This Part A of Volume VII/6, like Part B that follows it, emphasizes the broad questions that concern groups larger than the individual species; in some cases these questions have general applicability. The middle course between approaches that are too specialized and those that are too general is often elusive, but here we attempt to follow it. The vast number of special adaptations-probably, as we have said, as large as the number of species-is beyond the range even of a handbook.

Volume VII, Part 6 brings to a conclusion the Handbook of Sensory Physiology, the publication of which has spanned 9 years. In the General Preface of Volume I it was stated that: "The purpose of this handbook is not encyclopedic completeness, nor the sort of brief summaries provided by periodic annual reviews. " The Editorial Board and the editors hope that this golden mean has been achieved: An absorbing, thorough, but nevertheless exemplary presentation should, with the aid of relevant examples, enable the reader to become accustomed with the numerous facets of the sensory system without sacrificing an overview of the subject. The main issues of sensory physiology were formulated in the nineteenth and early twentieth centuries by JOHANNES MULLER, H. VON HELMHOLTZ, E. HERING, S. EXNER, 1. VON KRIES, W. TRENDELENBURG, and E. D. ADRIAN, to name but a few. Modern development in the field has been characterized by interdisciplinary cooperation, the foundation for which was laid in the second half of the nineteenth century by VON HELMHOLTZ, EXNER, MAXWELL, and others. Progress made in bio­ chemistry, physics, mathematics, and information theory has not only made pos­ sible unanticipated refinement of methods of measurement; it has above all per­ mitted the transformation of mere hypotheses into established, accepted theories as well as revealing new problems. However, at the same time such development has, in recent decades, resulted in the literature becoming dispersed in specialist journals; consequently, it has grown increasingly difficult to survey.