Table Of ContentFATIGUE
Neural and Muscular Mechanisms
ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY
Editorial Board:
NATHAN BACK, State University of New York at Buffalo
IRUN R. COHEN, The Weizmann Institute of Science
DA VID KRITCHEVSKY, Wistar Institute
ABEL LAlTHA, N. S. Kline Institute for Psychiatric Research
RODOLFO PAOLETTI, University of Milan
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FATIGUE: Neural and Muscular Mechanisms
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FATIGUE
Neural and Muscular Mechanisms
Edited by
Simon C. Gandevia
Prince of Wales Medical Research Institute
Sydney, New South Wales, Australia
Roger M. Enoka
The Cleveland Clinic Foundation
Cleveland, Ohio
Alan J. McComas
McMaster University
Hamilton, Ontario, Canada
Douglas G. Stuart
The University of Arizona
Tucson, Arizona
and
Christine K. Thomas
University of Miami
Miami, Florida
Technical Editor
Patricia A. Pierce
The University of Arizona
Tucson, Arizona
SPRINGER SCIENCE+BUSINESS MEDIA, LLC
Library of Congress Cataloging-in-Publication Data
On file
Proceedings based in part on the symposium on Neural and Neuromuscular Aspects of Muscular Fatigue,
held November 10-13, 1994, in Miami, Florida
ISBN 978-1-4899-1018-9 ISBN 978-1-4899-1016-5 (eBook)
DOI 10.1007/978-1-4899-1016-5
© Springer Science+Business Media New York 1995
Originally published by Plenum Press, New York in 1995
Softcover reprint of the hardcover 1st edition 1995
1098 76 54 3 2 1
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
The challenge is to understand fatigue from the level of the single muscle fiber to the
whole organism. [Photograph from Abbott, Bigland, and Ritchie, Journal of Physiology
(London) 117:382,1952. Reprinted with permission.]
PREFACE
This volume describes the current state of our knowledge on the neurobiology of
muscle fatigue, with consideration also given to selected integrative cardiorespiratory
mechanisms. Our charge to the authors of the various chapters was twofold: to provide a
systematic review of the topic that could serve as a balanced reference text for practicing
health-care professionals, teaching faculty, and pre-and postdoctoral trainees in the biomedi
cal sciences; and to stimulate further experimental and theoretical work on neurobiology.
Key issues are addressed in nine interrelated areas: fatigue of single muscle fibers,
fatigue at the neuromuscular junction, fatigue of single motor units, metabolic fatigue studied
with nuclear magnetic resonance, fatigue of the segmental motor system, fatigue involving
suprasegmental mechanisms, the task dependency of fatigue mechanisms, integrative
(largely cardiorespiratory) systems issues, and fatigue of adapted systems (due to aging,
under- and overuse, and pathophysiology). The product is a volume that provides compre
hensive coverage of processes that operate from the forebrain to the contractile proteins.
The neurobiology of muscle fatigue received minimal attention throughout the first
six decades of the 20th century. Then, in the mid-to late 1970s, a series of reports appeared
on neuromuscular aspects of fatigue that were featured in influential international symposia
held in 1980 (London, UK), 1990 (Paris, France), 1992 (Amsterdam, The Netherlands), and
1994 (Miami, Florida). This sudden acceleration of interest in the study of neural and
muscular aspects of fatigue is attributable to at least three factors: the practical importance
and relevance of the topic; its long-neglected fundamental and clinical significance; and the
type of integrated biological thought and experimentation needed to advance the field,
extending from the cellular/molecular level to the behaving organism. This latter integrative
emphasis is a feature of the present volume in all nine subsections. The volume also stresses
the need for neuroscientists to expand our understanding of the role of the eNS in fatigue
processes to the same extent as our current understanding of peripheral neuromuscular
mechanisms. To this end, several chapters in the present volume emphasize how the full
experimental armamentarium of the field of neuroscience can be applied to the neural aspects
of fatigue.
While the volume forms a cohesive whole, we have respected the individuality of
our authors, including innumerable nuances in their definitions of muscle fatigue. Similarly,
in selected areas, there is a degree of overlap between chapters such that the reader can
contemplate how the same issue is approached by different laboratories. These features of
the volume should prove helpful when reviewed in pre-and postdoctoral training programs.
To facilitate this possibility, the nine subsections of the volume are provided with a brief
introduction prepared by the editors.
Since the mid-1970s, Brenda Bigland-Ritchie has been in the forefront of the study
of the neuromuscular aspects of muscle fatigue. Using human subjects, she has shown to
vii
viii Preface
what extent the fatigue findings from animals or isolated tissues apply to real-life situations.
More than this, she has stimulated inquiry into the search for reflex mechanisms which may
serve to match the activity of the spinal cord with that of the fatiguing muscles. The present
generation of scientists who study muscle fatigue owe much to her contributions and
enthusiasm for the field. The chapters that follow document her impact. They also provide
the rationale for why the editors and contributing authors have enthusiastically dedicated
this volume to Dr. Bigland-Ritchie. Her efforts have been exemplary.
Simon C. Gandevia
Roger M. Enoka
Alan J. McComas
Douglas G. Stuart
Christine K. Thomas
ACKNOWLEDGMENTS
We greatly appreciate the dedication, effort, and talent that our technical editor,
Patricia Pierce, has displayed in bringing this research monograph to successful fruition. We
would also like to thank several University of Arizona colleagues: Dr. Edwin Gilliam, Dr.
Jennifer McDonagh, Robert Gorman, and George Hornby for their help with the review and
executive processing of the chapters in this volume.
Much of the work in this volume was presented by the authors of each chapter at an
International Symposium, Neural and Neuromuscular Aspects of Muscle Fatigue, held in
Miami, FL, November 10-13, 1994. Designated as a Satellite Symposium of the Annual
Meeting of the Society for Neuroscience, the symposium honored Professor Brenda Bigland
Ritchie and was organized by Drs. Roger Enoka, Simon Gandevia, Alan McComas, Douglas
Stuart, and Christine Thomas. The presentations in Miami by 33 invited scientists from
Canada and the United States were supported largely by their own research funds, with some
assistance from the University of Miami (Department of Neurological Surgery, Miami
Project to Cure Paralysis) and the University of Arizona (Research Office of the College of
Medicine, and Regents' Professor funds of Douglas Stuart). Travel awards were provided to
37 scientists from other countries (Australia, Belgium, Denmark, Finland, France, Germany,
Israel, Norway, Slovenia, Switzerland, The Netherlands, UK, Yugoslavia) by the American
Physical Therapy Association (Research and Analysis Division, and Section on Research),
the Muscular Dystrophy Association (Conference grant no. 46168), the National Institutes
of Health (National Center for Medical Rehabilitation Research, NICHD) and the Universi
ties of Miami and Arizona. Ten trainee awards were provided by The Miami Project to Cure
Paralysis. We would also like to thank Bette Mas (Miami Project to Cure Paralysis,
University <;>f Miami) and Lela Aldrich, Lura Hanekamp and Joan Lavoie (Department of
Physiology, University of Arizona) for their considerable efforts to ensure the success of the
symposium. The abstracts and discussion summaries from the symposium will be published
by Muscle & Nerve in the Fall of 1995, as sponsored by the Henry L. and Kathryn Mills
Charity Foundation and the Cleveland Clinic Foundation.
The Editors
ix
CONTENTS
Looking Back ......................................................... .
Brenda R. Bigland-Ritchie
The Scientific Contributions of Brenda Bigland-Ritchie ........................ 11
C. K. Thomas, R. M. Enoka, S. C. Gandevia, A. J. McComas, and
D. G. Stuart
Section I: Fatigue of Single Muscle Fibers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 27
1. Myofibrillar Fatigue versus Failure of Activation. . . . . . . . . . . . . . . . . . . . . . . . .. 29
K. A. P. Edman
2. Mechanisms of Excitation-Contraction Coupling Relevant to Skeletal Muscle
Fatigue ....................................................... 45
D. G. Stephenson, G. D. Lamb, G. M. M. Stephenson, and M. W. Fryer
3. The Role ofIntracellular Acidosis in Muscle Fatigue. . . . . . . . . . . . . . . . . . . . . .. 57
D. G. Allen, H. Westerblad, and J. Liinnergren
4. Role ofInterstitial Potassium. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 69
G. Sj0gaard and A. J. McComas
Section II: Fatigue at the Neuromuscular Junction .......................... 81
5. Fatigue at the Neuromuscular Junction: Branch Point vs. Presynaptic vs.
Postsynaptic Mechanisms .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 83
G. C. Sieck and Y. S. Prakash
6. The Role of the Sarcolemma Action Potential in Fatigue .................... 101
A. J. Fuglevand
7. Single Fiber Electromyography in Studies of Neuromuscular Function ........ 109
J. V. Trontelj and E. StAlberg
xi
