303
THE EFFECTS OF TRAINING ON MUSCLE STRUCTURE AND FUNCTION IN 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 McMaster University (October, 1985)

The Effects of Training on Muscle Structure and Function in the … · THE EFFECTS OF TRAINING ON MUSCLE STRUCTURE AND FUNCTION IN ~HE ~ TRICEPS SURAE by ~;~STEPHEN EDWARD ALWAY,

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Page 1: The Effects of Training on Muscle Structure and Function in the … · THE EFFECTS OF TRAINING ON MUSCLE STRUCTURE AND FUNCTION IN ~HE ~ TRICEPS SURAE by ~;~STEPHEN EDWARD ALWAY,

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)

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/

• KUaCLE STRUCTURE AND FUNCTION

..

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DOCTOR OF PHILOSOPHY' (1985)

(Medical Sciences)

McMASTER UNIVERSITY

Hamilton, ontario

TITLE: The Effects of Training on Muscle structureand 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, 290.

• 0

ii

, ,

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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 difficul ties 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

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Structural and contractile properties were examined inS'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. 95.3 ms respectively) but TPT was decreased (p<.Ol) by

24% and 16% following short-term stren~th and endurance

altered by strength or endurance training in either-Jtraining respectively. The fibre volume of SR was not

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

J

endurance training (7.26%).

It was concluded that fUftcti~nal adaptation to strength

or endurance training may occur independent of fibre

organelle volume adaptation to .these training programs.

I

t

iv

'. \

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f

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,

encouragement and sacrifice throughout this project.

Finally, I am grateful to the Lord· for His direction

throughout my career, for the success of this proj ect and

for the opportunity to obtain a small insight into the

workings of His creation.

v

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\1

TABLE OF CONTENTS

"-CHAPTER 3 METHODS

SUbjects.. ,Muscle Group Investigated'Torque Measurements . .Electrical stimulation.Physiological Measures.Morphological MethodsMorpholQgy. . . . , . Q

statistical Methods .Longitudinal Training Group

Differences Between Type I and II Fibres.Morphological Properties". . " . ,Ultrastructural properties. . , . ,

~ Contractile properties of Type I andType II Fibres . . . . . ,

The Isometric Twitch Response in theTriceps Surae . . " , . : . . .

sarcoplasmic' Ret~lum and its Involvement, in Excitation-contraction Coupling..Correlative Approaches to Examine Fibre

Type Differences in the Triceps SuraeMuscular Adaptation to Chronic ExerciseFatigue of Skeletal Muscle . . . . . .

REVIEW OF LITERATURE':

1

11011

17

171920

28

" 30

35c

414469

86

86888992939799

105106

"Purpose of study,Limitations .Definition of Terms

CHAPTER 2

CHAPTER 1 INTRODUCTION,

'" ':

'.

vi

• c

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)/

CHAPTER 4 RESULTS,

Validation of Myoglobin Localizati~n Methodfor Fibre Typing. . .' . . . . . . .

Reproducibility of Electro-mechanicalMeasures , . . . . . . . . . . • .

Contractile Properties of the Triceps SuraeEffects of Training on Contractile Propertiespossible Explanations for Dissociation of

Function and Structure.'Isometric Twitch TorqueMuscle Fatiquability.Voluntary Strength.Summary •...Conclusibns . •Recommendations for Further InvestigationReferences.Appendix

,108

108

109110III11111~

114116116118119

119

121121122 .125125

128130142

143

153

170

175

176

180 '181186

195204205228'233236239241273

, \'

, ,"

,"

DISCUSSION

General Observations.Twitch Characteristics of the Cross-

sectional Group . .Triceps Surae . . . ,Lateral GastrocnemiusMedial Gastrocnemius.Soleus. , . . . ,Maximal V~untary ContractionMaximal Voluntary Torque to Twitch Ratio.Fatigue Responses . . . ., .•,..."Longitudinal Training Group ...,Twitch Characteristics of the Triceps S~rae

Twitch Characteristics of the LateralGastrocnemius . . , . _. .".

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 Cross-

sectional Group • . . . . . .Ultrastructural P.roperties. . .Morphological comparison~ Between MusclesMorphological proper~ies'-of the

Longitudinal Training ~roup , .Ultrastructural and Physiological

Correlations. . •..Correlations of Fatigue and Strength

Properties. .... . . . . .

CHAPTER 5

vii }

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)

LIST OF TABLES

Table 2.0 Summary of previous UltrastructuralResults iri untrained Subjects

•22

Table 2.1 Summary of Twitch Contractile Speedsof the Triceps Surae of Previous Research. 31

(Table 2.2 Summary of previous Research on the

Contrac~ile Times in Muscles whichComprise the Triceps Surae .

Table 3.1 Summary of SUbject Char~cteristics

32

87

Table 4.1 Twitch Characteristics of the Triceps Surae. 110

Table 4.2 Twitch Characteristics of the LateralGastrocnemius. . . .. .... \.. . · 111

of the MedialTable 4.3

Table 4.4

Twitch CharacteristicsGastrocnemius. . . . .

,Twit~~haracteristicsOf the Soleus

112

113

Table 4.5 Percentage of LG, MG and SOL musclecontribution to the total twitch torqueof the TS complex. . . . • . .

Table 4.6 Maximal Voluntary Contractions

Table 4.7 Maximal Voluntary Torque to TS TwitchTorque Ratio . . . :

.' 115

· 115

· 116

Table 4.8 Voluntary Fatigue in the Cross­Sectional Group..• · 117

Table 4.9 The Effects of Training on theContractile Properties of theTriceps Surae .• 120

129

Table 4.10 Twitch Tensions. 123\

Table 4.11 Maximal Voluntary Torque 124

Table 4.12 Voluntary Fatigue Responses of theLongitUdinal Training Group. ... ..... 127

Table 4.13 Fibre Composition of the TricepsSurae: Cross-sectional Group .•

viii

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'.

Table 4.14 Fibre Areas of the Triceps Surae inthe Cross-Sectional Group 131

Table 4.15 Ultrastnictural Parameters of theLateral Gastrocnemius . , . , . 135

Table 4,16 Ultrastructural Parameters of theMedial Gastrocnemius . . . '. . . . , 138 .

Table 4.17 Ultrastructural Parameters of the Soleus 141

Table 4.18 Type II fibre compos~tion of toe TricepsSurae in the Longitudinal Training Group 144

Table 4.19 The Effect of Training. on Fibre Areas 146

Table 4.20 Morphometric Results for the LateralGastrocnemius from the LongitudinalTraining ~roup ..... " . , .. , . , .. 148

Table 4.21 Morphometric Results for the MedialGastrocnemius fro~ the LongitudinalTraining Group , . . , , . . ,... , , . . . . 149

,

\

. ~ \ .Table 4.22 Morphometric Results for the Soleus

from the Longitudinal Training Group

ix

152

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Figure 1

Figure 2

LIST OF FIGURES

Leg holder device and foot plate.

Analysis of the isometric muscle twitch

91

96

Figure 4.1 The relationship between the change intime to peak torque and the change inthe ratio; the volume density of sarco­plasmic.reticulum and T-tubular networkto myofibrillar volume density . 156

Figure 4.2 The relationship between the change intime to peak torque and the change inthe ratio of sarcoplasmic reticulumvolume density-T tubular network tomyofibrillar volume density after short­term strength· training or short-termendurance training. . . . . . . • . . 159

Figure 4.3 The relationship between tae change inhalf-relaxation time and the 'change inthe ratio of sarcoplasmic reticulumtubule complex to myofibrillar volume-density in type I and type II fibres 162

Figure 4.4 The relationship between the change inhalf-relaxation time and the change inthe ratio of sarcoplasmic retic~urn

tubul~r network volumedensity(, . . i65

. Figure 4.5 The relationship between the change intime to fatigue at an absolute load of30% maximal voluntary effort and thechange in the ratio o·f mitochondrialvolume.density to myofibrillar volumedensity in type I and type II fibres ofthe lateral gastrocnemius . . • • . . . 169

Fi;.gure 4.6 The relationship between the change intime to fatigue at an absolute load of30% of maximal voluntary effort to thechange in the ratio of; mitochondrialvolume density to myofibrillar volumedensity corrected for fibre type. . .

x

,

... 172

I

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Figure 5.1 The relationship of the change in time( '\to peak torque to the change in the. ,ratio of the volume density of sarco­

plasmic reticulum T tubular network,to myofibrillar volume density cor7 .rected for fibre type.•. ~ . . . . 178

Figure 5.2 The relationship between function andstructure among the muscles of thetriceps surae. . . • . . . . . . • . . 184

.'

xi

, ,~

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Plate 1

Plate 2

Plate 3

LIST OF PLATES

Serial Sections of the same fibres forATPase, NADH-TR and myoglobin. . .

A. Light micrograph of semi-thinmictrome section . . .

B. Electron micrograph of a serialultra-thin section showing thesame fibres as A . . . . . . . .

Electron micrograph of a type II fibre.

102

104

104

133

//

xii .<

(

//

'-l ~\ (--

L)

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"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

muscles.

physiological properties between fibres or

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

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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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