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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:
•
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xii, 290.
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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.
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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.
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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.
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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,
'" ':
'.
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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
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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 .•
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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
•
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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
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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
.'
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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
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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.
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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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