;~ STEPHEN EDWARD ALWAY, BoSco, MoSco
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1 THE EFFECTS OF TRAINING ON MUSCLE STRUCTURE AND FUNCTION IN ~HE ~ TRICEPS SURAE by ~ ;~ STEPHEN EDWARD ALWAY, BoSco, MoSco A Thesis Submitted to the School of Graduate Studies in Partial Fulfillment of the Requirements for the Degree Doctor of P~ilosophy McMaster University (October, 1985)
2 / KUaCLE STRUCTURE AND FUNCTION..
3 DOCTOR OF PHILOSOPHY' (1985) (Medical Sciences) McMASTER UNIVERSITY Hamilton, ontario TITLE: The Effects of Training on Muscle structure and Function in the Human Triceps Surae AUTHOR: Stephen Edward Alway, BoSe. (University of Waterloo) 'MoSc. (McMaster University) SUPERVISOR: Professor J. Duncan MacDougall NUMBER OF PAGES: xii, ,, ii,.
4 ABSTRACT The relationship between fibre structural adaptation to strength and endurance training and the fibre physiological " adaptations,to these training procedures has been unexp~~ in humans. Methodological difficulties in fibre identification have,~prevented t~ese investiga~i~ since traditional fibre classification techniques ~tilize various e~zymes wh'ich are inactlvated during f~xation~r electron mlcroscopy. However, myoglobin ls unaf~cted by \) glutaraldehyde fixation. In this study, structural and functional properties of the triceps surae were studied to determine the effects of endurance arid strength training on: 1. the relationship between the fibre volume of sarcoplasmic reticulum and transverse tubules (SR) to the time to peak torque (TPT) of the isometric twitch; and 2. the relationship between fibre volume of mitochondria to muscle fatiguability. Needle biopsies were obtained from the gastrocnemii and soleus muscles and fibre types were classified' for electron microscopy analysis on the basis of their myoglobin content. ~lectron micrographs were taken from the interior - I of 35 type I and 35 type II fibres of each muscle and were analyzed blindly by a stereological short-line test. Contractile properties were obtained from the isometric twitch in the triceps surae complex and separately from the gastrocnemii and soleus... / iii
5 Structural and contractile properties were examined in S'o;. two subject groups: 1. a cross-sectional group made up of 6 subjects each of active controls, strength athletes and endurance athletes (N=18); and ;;., a longitudinal training group (N=7) whom, in a unilateral training model, exercised one leg with a strength protocol and the other leg with an endurance protocol for 16 weeks. The results indicated that TPT was greater (p<.05) following chronic strength vs. endurance training (119.0 vs ms respectively) but TPT was decreased (p<.ol) by 24% and 16% following short-term stren~th and endurance -J training respectively. The fibre volume of SR was not altered by strength or endurance training in either cross-sectional or longitudinal training groups. Resistance to fatigue ~at an absolute load was increased by 1.7 fold after short-term strength training and by 3.5 fold after, short-term endurance training. Mitochondria volume was unaffected by either training protocol in the gastrocnemii but lower (p<. 05) in short-te~ strength type I fibres of../' tra~n~ng (5.76%) the soleus after vs. short-term endurance training (7.26%). It was concluded that fuftcti~nal adaptation to strength J or endurance training may occur independent of fibre organelle volume adaptation to.these training programs. I t iv '. \
6 ACKNOWLEDGEMENTS This thesis was completed at McMaster University through the co-operation of the cardio-respiratory and electron-microscopic departments at the McMaster University Medical Centre and the physical education department. The financial support for this study was provided by The Muscular Dystrophy Association of Canada. I am thankful to the members of my supervisory committee of Drs E. Cosmos, A.J. McComas and J. R. Sutton, for the{r help throughout my work.. I am grateful for the technical expertise, advice and discussions of Dr. Digby G. Sale. A special thanks to Dr. J. Duncan MacDougall, the chairman of my committee for his optimism, advice, direction and encouragement throughout my graduate career. I would like to express my appreciation to Dr. John Sutton for obtaining the biopsies in this study, and to George Turcon for technical assistance in processing samples for electron microscopy.. I would like to thank my wife Susan, for her patience, f encouragement and sacrifice throughout this project. Finally, I am grateful to the Lord for His direction throughout my career, for the success of this project and for the opportunity to obtain a small insight into the workings of His creation. v
7 \1 TABLE OF CONTENTS CHAPTER 1 INTRODUCTION, 1 Purpose of study, Limitations. Definition of Terms " CHAPTER 2 REVIEW OF LITERATURE': 17 Differences Between Type I Morphological Properties".. "., Ultrastructural properties..,., ~ Contractile properties of Type I and Type II Fibres....., The Isometric Twitch Response in the Triceps Surae.. ",. :... CHAPTER "- 3 METHODS and II Fibres. sarcoplasmic' Ret~lum and its Involvement, in Excitation-contraction Coupling.. Correlative Approaches to Examine Fibre Type Differences in the Triceps Surae Muscular Adaptation to Chronic Exercise Fatigue of Skeletal Muscle " c SUbjects.., Muscle Group Investigated 'Torque Measurements.. Electrical stimulation. Physiological Measures. Morphological Methods MorpholQgy....,. Q statistical Methods. Longitudinal Training Group '" ': '. vi c
8 CHAPTER 4 RESULTS, / ),108 General Observations. Twitch Characteristics of the Crosssectional Group.. Triceps Surae..., Lateral Gastrocnemius Medial Gastrocnemius. Soleus.,..., Maximal V~untary Contraction Maximal Voluntary Torque to Twitch Ratio. Fatigue Responses....,.,..." Longitudinal Training Group..., Twitch Characteristics of the Triceps S~rae Twitch Characteristics of the Lateral Gastrocnemius..,. _..". Twitch Characteristics of the Medial, Gastrocnemius,.. ~..,.. Twitch Characteristics of the Soleus. Twitch Tension.,.... '... Maximal Voluntary Torque to Twitch Ratio, Fatigue Responses to Training..... Mo~hological properties of the Crosssectional Group Ultrastructural P.roperties... Morphological comparison~ Between Muscles Morphological proper~ies'-of the Longitudinal Training ~roup,. Ultrastructural and Physiological Correlations.... Correlations of Fatigue and Strength Properties ," ",,, \' III ~ CHAPTER 5 DISCUSSION 175 Validation of Myoglobin Localizati~n Method for Fibre Typing...' Reproducibility of Electro-mechanical Measures, Contractile Properties of the Triceps Surae Effects of Training on Contractile Properties possible Explanations for Dissociation of Function and Structure.' Isometric Twitch Torque Muscle Fatiquability. Voluntary Strength. Summary... Conclusibns. Recommendations for Further Investigation References. Appendix ' ' vii }
9 ) LIST OF TABLES ( Table 2.0 Table 2.1 Table 2.2 Table 3.1 Summary of previous Ultrastructural Results iri untrained Subjects 22 Summary of Twitch Contractile Speeds of the Triceps Surae of Previous Research. 31 Summary of previous Research on the Contrac~ile Times in Muscles which Comprise the Triceps Surae. Summary of SUbject Char~cteristics Table 4.1 Twitch Characteristics of the Triceps Surae. 110 Table 4.2 Twitch Characteristics of the Lateral Gastrocnemius \ Table 4.3 Table 4.4 Twitch Characteristics Gastrocnemius.....,Twit~~haracteristicsOf of the Medial the Soleus Table 4.5 Percentage of LG, MG and SOL muscle contribution to the total twitch torque of the TS complex ' 115 Table 4.6 Table 4.7 Table 4.8 Table 4.9 Maximal Voluntary Contractions Maximal Voluntary Torque to TS Twitch Torque Ratio... : Voluntary Fatigue in the Cross Sectional Group The Effects of Training on the Contractile Properties of the Triceps Surae. 120 Table 4.10 Twitch Tensions. 123 \ Table 4.11 Maximal Voluntary Torque 124 Table 4.12 Voluntary Fatigue Responses of the LongitUdinal Training Group Table 4.13 Fibre Composition of the Triceps Surae: Cross-sectional Group. 129 viii
10 , '. Table 4.14 Fibre Areas of the Triceps Surae in the Cross-Sectional Group 131 Table 4.15 Ultrastnictural Parameters of the Lateral Gastrocnemius.,.,. 135 Table 4,16 Ultrastructural Parameters of the Medial Gastrocnemius... '...., 138. Table 4.17 Ultrastructural Parameters of the Soleus 141 Table 4.18 Type II fibre compos~tion of toe Triceps Surae in the Longitudinal Training Group 144 Table 4.19 The Effect of Training. on Fibre Areas 146 Table 4.20 Morphometric Results for the Lateral Gastrocnemius from the Longitudinal Training ~roup... ".,..,., Table 4.21 Morphometric Results for the Medial Gastrocnemius fro~ the Longitudinal Training Group,..,,..,...,, ~. \ Table 4.22 Morphometric Results for the Soleus from the Longitudinal Training Group 152 \ ix
11 LIST OF FIGURES Figure 1 Figure 2 Leg holder device and foot plate. Analysis of the isometric muscle twitch Figure 4.1 Figure 4.2 Figure 4.3 Figure 4.4 The relationship between the change in time to peak torque and the change in the ratio; the volume density of sarcoplasmic.reticulum and T-tubular network to myofibrillar volume density. 156 The relationship between the change in time to peak torque and the change in the ratio of sarcoplasmic reticulum volume density-t tubular network to myofibrillar volume density after shortterm strength training or short-term endurance training The relationship between tae change in half-relaxation time and the 'change in the ratio of sarcoplasmic reticulum tubule complex to myofibrillar volumedensity in type I and type II fibres 162 The relationship between the change in half-relaxation time and the change in the ratio of sarcoplasmic retic~urn tubul~r network volumedensity(,.. i65. Figure 4.5 The relationship between the change in time to fatigue at an absolute load of 30% maximal voluntary effort and the change in the ratio o f mitochondrial volume.density to myofibrillar volume density in type I and type II fibres of the lateral gastrocnemius Fi;.gure 4.6 The relationship between the change in time to fatigue at an absolute load of 30% of maximal voluntary effort to the change in the ratio of; mitochondrial volume density to myofibrillar volume density corrected for fibre type..., x I
12 Figure 5.1 The relationship of the change in time ( '\to peak torque to the change in the.,ratio of the volume density of sarcoplasmic reticulum T tubular network, to myofibrillar volume density cor7. rected for fibre type.. ~ Figure 5.2 The relationship between function and structure among the muscles of the triceps surae ' xi ~,,
13 LIST OF PLATES Plate 1 Plate 2 Serial Sections of the same fibres for ATPase, NADH-TR and myoglobin... A. Light micrograph of semi-thin mictrome section... B. Electron micrograph of a serial ultra-thin section showing the same fibres as A Plate 3 Electron micrograph of a type II fibre. 133 // xii.< / / ( '-l ~ \ (-- L)
14 " CHAPTER 1 INTRODUCTION Purpose of study Human skeletal muscles are composed o~ different types,. of fib:t::es and each fibre type has a different metabolic, physiolog 1 and structural profile. However., it is not known to what extent the differing I structural characteristic between fibre types might account for the different physiological properties between fibres or muscles. In addition, each fibre type in a given muscle may develop different structural and physiological properties in response to altered functional demands which are placed on that muscle. It is not known whether fibre structural adaptations to altered muscle activity might affect the physiological properties of that muscle. Such knowledge is not available. because of methodological difficulties which exist in identifying the different fibre types for ultrastructural analysis. In the absence of such techniques, it is not possible to correlate physiological and structural- properties by fibre type -for the same muscle. 1
15 2 The primary purpose of this study was to answer the following questions: 1. Does chronic participation in different types of physical activity result in struct:ural and/or physiological adaptations within human skeletal muscle fibres? 2. To what extent are physiological properties of fatigue and twitch contractile times affected by structural components such as mitochondria and sarcoplasmic reticulum respectively? Related to these, the secondary purpose ~as to examine the extent to which human type I and type II fibres might differ ultrastructurally and to determine the effects of altered activity patterns upon each fibre type. Rationale Introduction: Human type I and type II fibres are different histochemically (Brooke and Kaiser, 1970;.Askanas and Engel, 1975; Engel, 1977) and structurally (Payne et al., 1975, Sjostrom et al., 1982; Staron et al., 198,4). These fibres also have different 'physiological properties including twitch times (Si~a and McComas, 1971; Garnett et al., 1979) and fatiguability (Garnett et al., 1979). Human muscle is comprised of a mosaic of fibre types, which results in several difficulties, particularly in determining
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