The Sodium Theory Revisited: Or 45 Years of a Full Time Cnrs Neurophysiologist
By Yves Pichon
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The sodium theory has been elegantly proposed by Hodkin, Huxley and Katz in the early fifties, after their experiments on Plymouth squids, to account for the role of sodium and potassium ions in nerve activity. Since then, the electrophysiological techniques and the data acquisition techniques have known an amazing development. In this short paper, Yves Pichon wants to give an account of what happened since then in different laboratories (mostly marine) with a variety invertebrate species and mostly insects. One of the most important technical development has been the use of single cockroach axons which have been found to behave very much like squid axons. Another, almost simultaneous development which revealed extremely useful for the understanding of the nerve function was in situ microelectrode recording which enables an indirect analysis of the extraaxonal environement. Experiments on several species indicate that the CNS is protected from the ionic environment by a blood-brain barrier. On the other hand, quite unexpectedly, little ion accumation is detected in the vicinity of the axonal membrane in physiological conditions. Another innovating technique was the 'patch-clamp' technique which enables the recording of the activity of individual ionic channels in cultured neurones. The last chapter of this report is devoted to different mechansims leading to repetitive activity through modificatrion of the sodium and potassium axonal conductances.
Yves Pichon
Yves Pichon was born in Brittany before WW2 and obtained his Degrees (biology) from the University of Rennes. During his first year at University, he has been fascinated by the experiments of Hodgkin and Huxley on squid axons (1956 , Croonian Lecture, ) and their formulation of the ionic theory of nerve function. Since then, first as technician, then as full time resarcher at the CNRS (Paris), Yves has spent 45 years in several Laboratories, (Rennes, Gif sur Yvette, Cambridge, Plymouth, WoodsHole) to elucidate the various functions of ions (mostly Na+ and K+) in the nervous system of invertebrates. He has published numerous paper, edited several books and organized several international meetings, the last one in Rennes (2004), was entitled «Ion channels: from biophysics to disorders» and is published in the European biophysical Journal. In the present short report the author illustrates the main findings of his research in which he has combined many innovating electrophysiological techniques and sophisticated computer programs.
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Book preview
The Sodium Theory Revisited - Yves Pichon
Copyright © 2013 by Yves Pichon.
Library of Congress Control Number: 2013902591
ISBN: Hardcover 978-1-4797-9371-6
Softcover 978-1-4797-9370-9
Ebook 978-1-4797-9372-3
All rights reserved. No part of this book may be reproduced or transmitted
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This book was printed in the United States of America.
Rev. date: 03/22/2013
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Contents
Foreword
Chapter 1 The Original Ionic Theory (Hodgkin And Huxley, 1957)
Chapter 2 Blood Potassium Concentration And Insect Activity
Chapter 3 Ionic Basis Of Nerve Activity In Insects
Chapter 4 The Insect Blood-Brain Barrier
Chapter 5 The Blood-Brain Barrier In Crustaceans
Chapter 6 Ionic Regulation In The Cns: Accumulation Effects
Chapter 7 Osmotic Stress
Chapter 8 Axonal Membrane Channel Noise
Chapter 9 Pharmacological Modifications Of The Ionic Channels Of Squid And Cockroach Axons
Chapter 10 Patch-Clamp Analysis Of The Ion Channels In Cultured Neurons
Chapter 11 Computer Reconstruction Of The Ionic Channel-Induced Axonal Repetitive Activity
Selected Bibliography
Acknowledgement
FOREWORD
A few years after my official retirement from full-time CNRS employment, I have been faced with my personal responsibility in conveying my experiences of a life of experiments on some of the basic functions of the nervous system in invertebrates. It occurred to me that, although I am not a writer, I could illustrate some of the facets of my work which cannot be found in the published mass of scientific papers and could, however, be of some use to my family, friends, and colleagues.
My interest in neurobiology has been fostered by the publication of the Croonian Lecture given by A. L. Hodgkin in 1956 at his official reception of the Nobel Prize (with A. F. Huxley) on the ionic theory of nerve function. At that time, amongst the several questions which remained unanswered was the status of insects—the blood of which was known to often contain large concentrations of potassium ions for very little sodium ions.
This has led us to analyse the blood ionic composition of a common insect species, the American cockroach, Periplaneta americana, its variations in different experimental conditions and its correlations with the activity of the animal. The next step of our study has been to analyse the effects of high potassium concentrations on the spontaneous activity originating from the sixth abdominal ganglion of this same insect.
A definite answer to the question of the role of ions in the action potential production was obtained by an adaptation of the voltage-clamp technique to isolated giant axons of the cockroach. Our favourite insect revealed to be ideal for this kind of study. The giant axons, which convey the escape reflex to a puff of air on the cercae to the insect thoracic ganglia, form a bundle which is separated from the external medium by a complex sheath which can be dissected out. Such dissection, which was a prerequisite to enable the penetration of the tip of the microelectrodes into the giant axons (Boistel and Narahashi), was used to isolate single cockroach axon for the voltage-clamp studies. Interestingly, the giant axons of Periplaneta were found to behave very much like squid axons.
The only other explanation of the preservation of nerve activity in adverse ionic conditions is the existence of a blood-brain barrier, the properties of which remain to be investigated.
Our approach consisted of using fine-tipped microelectrodes impaled through the nerve sheath into the giant axons, usually by creating a small depression on the surface of the connective tissue and inducing a small mechanical vibration of the electrode holder. The penetration of the electrode tip was characterised by a sharp negative deflection (around −60 mV) of the oscilloscope trace. Pulling out the electrode was most usually followed by a transient positivation (about 15 mV)—the sheath potential. Under these conditions, replacement of all the sodium in the external medium by isotonic potassium failed to affect the action potential but was accompanied by a fast depolarisation of the external surface of the nerve sheath. This extraneuronal potential, which could also be recorded using a sucrose gap of the connectives, reflected the properties of the nerve sheath and the degree of mechanical stretch of the nerve cord. This has been checked