FATIGUE 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

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

On file

Library of Congress Cata loging- in-Publ ica t ion Data

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

1 0 9 8 7 6 5 4 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 biomedi­cal 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 compre­hensive 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 Bigland­Ritchie 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 Universi­ties 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

xii Contents

Section III: Fatigue of Single Motor Units .................................. 121

8. Intrinsic Properties of Motoneurons: Implications for Muscle Fatigue ......... 123 A. Sawczuk, R. K. Powers, and M. D. Binder

9. Neuromuscular Frequency Coding and Fatigue ........................... 135 D. Kernell

10. Human Motor Units Studied by Spike-Triggered Averaging and Intraneural Motor Axon Stimulation ......................................... 147

C. K. Thomas

11. Human Motor Units Studied by Intramuscular Microstimulation ............. 161 J. M. Elek and R. Dengler

Section IV: Fatigue Studied with NMR Techniques .......................... 173

12. Bioenergetics and Muscle Cell Types ................................... 175 M. 1. Kushmerick

13. Metabolic Correlates of Fatigue from Different Types of Exercise in Man ...... 185 N. K. V011estad

14. Mechanisms of Human Muscle Fatigue: Quantitating the Contribution of Metabolic Factors and Activation Impairment ........................ 195

R. G. Miller, 1. A. Kent-Braun, K. R. Sharma, and M. W. Weiner

15. Emerging Opportunities with NMR ..................................... 211 L. A. Bertocci

Section V: The Case for Segmental Motor Mechanisms ....................... 225

16. Variable-Frequency Stimulation Patterns for the Optimization of Force during Muscle Fatigue: Muscle Wisdom and the Catch-like Property ........... 227

S. A. Binder-Macleod

17. Overview: Potential Role of Segmental Motor Circuitry in Muscle Fatigue ..... 241 U. Windhorst and G. Boorman

18. The Fusimotor System: Its Role in Fatigue ............................... 259 K.-E. Hagbarth and V. G. Macefield

19. Role of Muscle Afferents in the Inhibition of Motoneurons during Fatigue ..... 271 S. J. Garland and M. P. Kaufman

Section VI: The Case for Central Fatigue .................................. 279

20. Central Fatigue: Critical Issues, Quantification and Practical Implications ...... 281 S. C. Gandevia, G. M. Allen, and D. K. McKenzie

Contents xiH

21. Single-Trial Readiness Potentials and Fatigue ............................ 295 D. Popivanov, A. Mineva, and J. Dushanova

22. The Senses of Effort and Force during Fatiguing Contractions ............... 305 L. A. Jones

23. Tryptophan, 5-Hydroxytryptamine and a Possible Explanation for Central Fatigue ....................................................... 315

E. A. Newsholme and E. Blomstrand

Section VII: Task Dependency of Fatigue Mechanisms ....................... 321

24. The Significance of Motor Unit Variability in Sustaining Mechanical Output of Muscle ....................................................... 323

A. J. Sargeant and D. A. Jones

25. Intramuscular Pressures for Monitoring Different Tasks and Muscle Conditions 339 O. M. Sejersted and A. R. Hargens

26. Task-Dependent Nature of Fatigue in Single Motor Units ................... 351 B. R. Botterman

27. Task-Dependent Factors in Fatigue of Human Voluntary Contractions ......... 361 B. Bigland-Ritchie, C. L. Rice, S. J. Garland, and M. L. Walsh

Section VIII: Integrative Systems Issues ................................... 381

28. Fatigue and the Design of the Respiratory System ......................... 383 S. L. Lindstedt and H. Hoppeler

29. An Integrative View of Limitations to Muscular Performance ................ 393 J. A. Dempsey and M. A. Babcock

30. Respiratory Muscle Fatigue ........................................... 401 D. K. McKenzie and F. Bellemare

31. Fatigue of Jaw Muscles and Speech Mechanisms .......................... 415 T. S. Miles and M. A. Nordstrom

Section IX: Fatigue of Adapted Systems: Overuse, Underuse, and Pathophysiology ........................................................ 427

32. Fatigue in Adapted Systems: Overuse and Underuse Paradigms .............. 429 T. Gordon

33. Associations between Muscle Soreness, Damage, and Fatigue ............... 457 P. M. Clarkson and D. J. Newham

34. Muscle Fatigue in Old Animals: Unique Aspects of Fatigue in Elderly Humans 471 J. A. Faulkner and S. V. Brooks

xiv Contents

35. Historical Perspective: A Framework for Interpreting Pathobiological Ideas on Human Muscle Fatigue .......................................... 481

R. H. T. Edwards, V. Toescu, and H. Gibson

36. Fatigue Brought on by Malfunction of the Central and Peripheral Nervous Systems ...................................................... 495

A. J. McComas, R. G. Miller, and S. C. Gandevia

Epilogue

37. Neurobiology of Muscle Fatigue: Advances and Issues ..................... 515 S. C. Gandevia, R. M. Enoka, A. J. McComas, D. G. Stuart, and

C. K. Thomas

Contributors ............................................................ 527

Index ................................................................. 533