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J. Bligh K. Voigt (Eds.) Thermoreception and Temperature Regulation H.A. Braun K. Bruck G. Heldmaier (Co-Eds.) With 137 Figures and 3 Tables Springer-Verlag Berlin Heidelberg New York London Paris Tokyo HongKong Prof. Dr. J. BLIGH Institute of Animal Physiology and Genetics Research Babraham Hall Cambridge CB2 4AT, UK Prof. Dr. K. VOIGT Phillips Universitat FB Humanmedizin Institut fur Normale und Pathologische Physiologie DeutschhausstraBe 2 3550 Marburg, FRG ISBN-13: 978-3-642-75078-6 e-ISBN-13: 978-3-642-75076-2 001: 10.1007/978-3-642-75076-2 Library of Congress Cataloging-in· Publication Data Thermoreception and temperature regulation 1 J. Bligh, K. Voigt (eds.) p. cm. Includes bibliographical references. ISBN-13: 978-3-642-75078-6 1. Body temperature-Regulation. I. Bligh, J. II. Voigt, Karlheinz. QP135.T478 1990 612'.022-dc20 This work is subject to copyright. All rights are reserved. whether the whole or part of the material os concerned, specifically the rights of translation reprinting, re-use of illustra tions, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the pro visions of the German Copyright Law of September 9, 1965, in its version ofJune 24, 1985, and a copyright fee must always be paid. Violations fall under the prosecution act of the German Copyright Law. © Springer-Verlag Berlin Heidelberg 1990 Softcover reprint of the hardcover 1s t edition 1990 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product Liability: The publisher can give no guarantee for information about drug dosage and application thereof contained in this book. In every individual case the respective user must check its accuracy by consulting other pharmaceutical literature. Typesetting: International Typesetters, Inc., Manila, Philippines 2131/3145-543210 - Printed on acid-free paper Contents Introduction . 1 J. BLIGH 1 Transduction of Temperature into Cellular Responses _____ 1.1 Whither Sensory Specificity? 9 A.IGGO 1.2 Theories and Models of Temperature Transduction 19 H.A. BRAUN, K. SCHAFER, and H. WISSING 1.3 Mechanism of Sensory Transduction in Cold Receptors 30 K. SCHAFER, H.A. BRAUN, and L. REMPE 1.4 The Location and Function of Different Skin Thermoreceptors 37 K.P. IVANOV 1.5 Temperature Sensitivity of the Ampullae of Lorenzini of Elasmobranchs . . . . . . . . . . . . . . . . . . . . 44 G.N. AKOEV 1.6 Long-Term Modulation of Hypothalamic Neurons by Neuropeptides . . . . . . . . . . . . . . . . . . . . 53 H. SCHMID and Fr.-K. PIERAU 2 Central Processing of Temperature Information _______ 2.1 Correlations of Temperature Sensation and Neural Activity: A Second Approximation . . . . . . . . 67 R. KENSHALO 2.2 Central Projections of Thermoreceptors 89 E.R. PERL 2.3 Processing of Thermal Information from the Face 107 R.F. HELLON VI Contents 2.4 Temperature-Evoked Sensation in Human Teeth: Two Com- ponents of Pain in Response to Cold Stimulation ...... 116 E. lYvASJARVI, K.-D. KNIFFKI, M.K.C. MENGEL, and A. STIEFENHOFER 2.5 Neural Basis of Cold Sensation 123 T. JARVILEHTO 2.6 Cerebral Evoked Potentials Induced by Cutaneous Thermal Stimulation in Humans . . . . . . . . . . 133 R. DUCLAUX 2.7 A Neuronal Model Mimicking the Sensations Produced by a Cold Stimulus to the Skin . . . . . . . . . . . . . 137 J.W. WOODBURY and P.R. BURGESS 3 Epistemology 3.1 Physiology and Language. Epistemological Questions About Scientific Theories of Perception . . . . . . . . 151 P. JANICH 4 Temperature and Functional Interactions _________ 4.1 Cells, Cell-Talk and Mammalian Homeothermy . 163 J. BLIGH 4.2 Negative Plus Positive Feedback . . . . . . . . . 174 H.T. HAMMEL 4.3 Temperature/Signal Relations of Thermoreceptors and Input/Output Relations of the Thermoregulatory System 183 C. JESSEN and G. KUHNEN 4.4 Temperature Dependence of Thermal and Nonthermal Regulation: Hypothalamic Thermo-and Osmoregulation in the Duck ....................... 191 E. SIMON and P. NOLTE 4.5 Control of Cardiorespiration During Shivering Thermogenesis in Pigeons . . . . . . . . . . . 200 W. RAUTENBERG 5 Adaptive Modification of Temperature Regulation 5.1 Long-Term and Short-Term Adaptive Phenomena in Temperature Regulation. . . . . . . . . . . . . . . 211 K. BROCK Contents VII 5.2 Models of Cold and Warm Adaptation 224 J. WERNER 5.3 Seasonal Adaptation of Thermoregulatory Heat Production in Small Mammals . . . . . . . . . . 235 G. HELDMAIER, S. KLAUS, and H. WIESINGER 5.4 Thermoreception and Temperature Regulation in Hibernators . . . . . . . . . . . . . . . . . . . 244 W. WONNENBERG and G. KUHNEN 6 Fever _____________________________________________ _ 6.1 The Neurobiology of Endogenous Pyrogens 257 C.M. BLATIEIS 6.2 The Role of Septal Peptides in Thermoregulation and Fever ................... . 273 E. ZEISBERGER 6.3 Phylogeny of Fever 284 M. CABANAC Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . .. 297 List of Contributors You will find the addresses at the beginning of respective contribution. Akoev,G.N. Kniffki, K.-D. Blatteis, C.M. Kuhnen, G. Bligh,J. Mengel, M.K.C. Braun,H.A. Nolte, P. Briick,K. Ped,E.R. Burgess, P.R Pierau, F.-K. Cabanac,M. Rautenberg, W. Duc1aux, R Rempe, L. Hammel, H.T. Schafer,K. Heldmaier, G. Schmid, H. Hellon, RF. Simon, E. Iggo,A. Stiefenhofer, A. Ivanov, K.P. Werner, J. Janich,P. Wiesinger, H. larvilehto, T. Wissing, H. Jessen, C. Woodbury, J.W. Jyvasjarvi, E. Wiinnenberg, W. Kenshalo, R. Zeisberger, E. Klaus, S. Introduction As indicated in the Preface, the contributions to this volume are based upon the papers presented at the symposium on Thermoreceptors and Temperature Regula tion held in July 1988 at the Institute of Physiology of the University of Marburg (Federal Republic of Germany) to celebrate and commemorate the life and achievements of HERBERT HENSEL, who directed that Institute from 1955 until his death in 1983, and whose most notable and significant contributions to thermo physiology were in the areas of the properties and characteristics of thermo sensors, mammalian thermoregulation more generally, and the psychophysiology of ther mal sensation. All the papers in this volume deal, to a greater or lesser extent, with these discernibly different but closely allied aspects of mammalian physiology. The editors have sought to achieve cohesion, flow, and balance both in the contributed articles and in their order of presentation, without either large gaps or redundancies in the coverage of the recent advances in the understanding of thermoreceptors and thermoregulation. At the same time we have sought to avoid such a degree of editorial control as to destroy the individuality of the contributions, and the judgements upon which they were based. We have also sought to look both backwards and forwards, and to include some legitimate extension of the con sideration of thermosensitivity and thermoregulation into such areas as climatic adaptation and fever. Hence the "greater or lesser" of the closeness of this series of papers to HERBERT HENSEL'S scientific interests. When the typescripts reached Marburg it was evident that the formats of the papers were very different from each other, some being reviews, some being new attempts to interpret the literature, and some being reports of the findings of recent investigations in the authors' laboratories. The editors decided not to ask con tributors to be more uniform in the scope and style of their presentations; nor to attempt to separate the sometimes quite substantial reviews and interpretations of recent researches from the more limited reports of recent studies, but simply to place the contributions into what has seemed to us to be the best order for their presentation. The first section of the book concerns the specificity of sensors (A. IGGo) and the updated theories, mechanisms, and models of temperature transduction into Institute of Animal Physiology and Genetics Research. Babraham Hall. Cambridge CB2 4AT. UK 1 2 Introduction neuronal discharges or impulses (H.A. BRAUN et al. and K. SCHAFER et al.); a consideration of the temperature sensitivity of the ampullae of Lorenzini in elas mobranchs (O.N. AKOEV), the multimodality of which allows the investigation of the electrically as well as the thermally induced responses; and a reconsideration of the proposition that there are thermoreceptors at different depths through the skin, and that these sensors can thereby provide the eNS with information about the heat flow through the thermal gradient between the body core and the environment (K.P. IVANOV). The last paper in this section concerns evidence of an effect of neu ropeptides on temperature-sensitive neurons within the preoptic hypothalamic region of the brain (H. SCHMID and F.K. PIERAU). Not only modulation of temperature sensitivity of warm- and cold-sensitive neurons was demonstrated in response to bombesin application but even temperature-insensitive units were turned into warm-sensitive ones. Similar changes may be caused by pyrogens, hormones, and drugs. Section 2 is principally concerned with the afferent neural projections from thermoreceptors (E.R. PERL), and the processing in afferent pathways as they pass up the eNS towards the afferent! efferent interface (R.F. HELLON). It also considers the neural basis of sensation generally, and of temperature sensations particularly (E. JYVASJARVI, K.-D. KNIFFKI, M.K.C. MENGEL and A. STIEFENHOFER; T. JARVILEHTO; R. DUCLAUX, and J.W.WOODBURY and P.R. BURGESS). The last of these contributions provides a remarkable glimpse at the possibility that the patterns of conscious perception of cutaneous thermal stimuli can be explained in terms of the organizational sequences and properties of neurons in the afferent pathways. The question of whether the intensities and durations of conscious perception, which mayor may not be essential for the formulation of appropriate behavioral responses, can be measured and considered with the same degree of objectivity as can the relations between thermal disturbances and autonomic thermoregulatory responses, was a matter of some concern to HERBERT HENSEL. To some extent, at least, the neuronal model of thermal disturbance and conscious perception by E.R. PERL gives reason to hope that in time it will be possible to show ultimately, even for conscious sensations, a neurophysiological correlate in the eNS. The consideration of consciousness in terms of physiology generally, and neu rophysiology particularly, compels the trespass upon areas of scholarship generally considered to belong more of philosophy than physiology (Section 3). Mindful of HERBERT HENSEL'S abiding interest in this as yet largely unsurveyed hinterland between the functions ofc ells in the eNS and the generation of conscious perception (and thence onward to thought process), it seems appropriate to place the philo sophical consideration of the language necessary for the formulation of scientific theories of perception (P. JANICH) at this juncture in the ordering of the papers. Section 4 concerns temperature regulation and the increasing evidence of the interaction of this with other homeostatic functions and, indeed, with many other concurrent functions controlled by the eNS. The first paper, by J. BLIGH, is intended to be a synthetic overview of mammalian thermoregulation in which the attempt is made to consider the central interface between the afferent pathways from ther mosensors and the efferent pathways to thermoregulatory effectors in terms of the Introduction 3 successional actions of cells upon cells. Ultimately, it is argued, any component system of multicellular existence must be expressible in terms of sequences of environmental influences upon cells, with all but the initial environmental influence upon specific sensors being created by other cells within the organism. Embodied in this thesis is the accepted principle that the essential central nervous function of integration of the many concurrent sensor-effector activities is achieved by con verging and diverging excitatory and inhibitory influences. Thus viewed, inter action between homeostatic functions generally, and between these and other activities involving the CNS, are not only likely to occur, but are virtually inevitable occurrences. That both engineered and biological regulation depend upon the negative feedback of disturbance correction activities upon the disturbance sensors is now widely acknowledged. In the next paper, H.T. HAMMEL introduces his evidence for positive feedback as well as negative feedback. At each synapse on a feedforward pathway from disturbance sensors to correction effectors, there will almost certainly be the summed effects of converging excitatory inputs as well as those of inhibitory ones. The question raised by HAMMEL is whether the evidence of magnified responses to stimuli and/or ofs ustained effector activity after stimulation has ceased is the consequence of positive feedback from the effector activity, or upon some other facilitation of synaptic gating on sensor-to-effector pathway such as occurs in synaptic facilitation. This, no doubt, will be a matter of continuing investigation and debate. While it may be necessary, as a stepping-stone towards an understanding of the nature of the CNS generally, and of home other my particularly, to consider receptor responses to temperature, and the projection of the response by neuronal impulses in a somewhat simplistic way (see, for example, J. BLIGH), reality is almost certainly based upon much more complex patterns of signals in afferent pathways. Evidence for some of this complexity in the temperature/signal relations of thermor eceptors and the input/output relations of the thermoregulatory system is provided by C. JESSEN and G. KUHNEN, while E. SIMON and P. NOLTE shed light upon the inter dependence of thermal and nonthermal regulatory processes in their considera tion of thermo-and osmo-regulation in the duck; and W. RAUTENBERG details aspects of the control of cardiorespiration during shivering thermogenesis in pigeons. Section 5 covers aspects of adaptive modification of temperature regulation by processes of acclimatization to seasonal changes in the natural climate, and ac climation to changes in the ambient temperature in the laboratory. It should be noted that the terminology employed in this section is that recommended in the Glossary of Terms for Thermal PhYSiology (Pfliigers Archiv, 1987,410:567-587). There is no etymological distinction between acclimatization and acclimation, but it is now conventional in environmental and thermal physiology to use the two forms to distinguish between field studies in a natural environment and laboratory studies in which only one component of the environment is varied. There is no composite term other than adaptation to cover observations made under both field and laboratory conditions. Adaptation is a much more global word which encompasses both genotypic and phenotypic changes induced by climatic variations and many other environmental forces.

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