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NEUROMUSCULAR FUNCTION FOLLOWING LENGTHENING CONTRACTIONS
(Spine title: Power-loss following muscle damage)
(Thesis format: Integrated Article)
by
Geoffrey Alonzo Power
Graduate Program in Kinesiology
A thesis submitted in partial fulfillment
of the requirements for the degree of
Doctor of Philosophy
The School of Graduate and Postdoctoral Studies
The University of Western Ontario
London, Ontario, Canada
© Geoffrey Alonzo Power 2012
ii
THE UNIVERSITY OF WESTERN ONTARIO
School of Graduate and Postdoctoral Studies
CERTIFICATE OF EXAMINATION
Supervisor
______________________________
Dr. Anthony A. Vandervoort
Supervisory Committee
______________________________
Dr. Charles L. Rice
______________________________
Dr. Timothy J. Doherty
Examiners
______________________________
Dr. Jonathan P. Farthing
______________________________
Dr. Jeffrey D. Holmes
______________________________
Dr. Donald H. Paterson
______________________________
Dr. Gregory D. Marsh
The thesis by
Geoffrey Alonzo Power
entitled:
Neuromuscular Function Following Lengthening Contractions
is accepted in partial fulfillment of the
requirements for the degree of
Doctor of Philosophy
______________________ _______________________________
Date Chair of the Thesis Examination Board
iii
ABSTRACT
Unaccustomed lengthening contractions have been shown to impair muscle
function - however little is known regarding this impairment on muscle power -
specifically, the velocity component of power during voluntary contractions in
humans. The four studies presented in my thesis investigated power-loss following
lengthening contractions in healthy young and old women and young men.
The purpose of Study 1 was to determine reliability of velocity-dependent
power of the dorsiflexors using the isotonic mode of the Biodex Dynamometer. I
determined the isotonic mode is reliable and can be used to track changes in
velocity and power following fatigue and lengthening contractions.
The purpose of Study 2 was to investigate changes in neuromuscular
properties of the ankle dorsiflexors during and following repetitive lengthening
contractions and throughout recovery in 21 (10 men, and, 11 women) recreationally
active young adults (25.8 ± 2.3 y). The protocol for the following 3 studies involves
subjects performing 5 sets of 30 lengthening contractions, with neuromuscular
measures (i.e., electrically evoked twitch, tetanus, voluntary activation, voluntary
contractions) recorded at baseline, during the task, and throughout recovery.
Exercise induced muscle damage ultimately led to velocity-dependent (i.e., isotonic)
power loss at a moderate load (i.e., 20% maximum voluntary strength).
Compared with isometric and isokinetic tasks, less is known regarding
velocity-dependent muscle power and recovery in older adults following repeated
lengthening contractions. In Study 3 we tested 9 old (68.3 ± 6.1 y) and 9 young
women (25.1 ± 1.3 y). Old were more impaired following the task than young as
shown by greater low-frequency torque depression at task termination leading to a
more pronounced initial loss of power than young. However, power remained
reduced in both groups during the 30 min recovery period. Older women were
more susceptible to power loss than young following lengthening contractions likely
owing to a greater fatigue response.
iv
In Study 4, power curves were constructed [8 men (27 ± 3 y), 8 women (26 ±
4 y)] using various isotonic loads before and following task termination. There was
a preferential loss of power at higher loads, with a relative maintenance of maximal
shortening velocity shifting the power curve down and leftward. When stressed
with heavier loads during dynamic contractions, force modulators arranged in
parallel seem to be affected more by damage than those organized in series
(velocity), which was highlighted by the attenuation of power at higher versus lower
resistances.
The main findings of my thesis are that repetitive lengthening contractions
fatigued and temporarily weakened the dorsiflexors, thus impairing their power
producing ability immediately (i.e., fatigue + weakness) and longer term (i.e.,
weakness) owing to an inability to generate torque rapidly.
KEYWORDS
Muscle Damage, Shortening Velocity, Rate of Torque Development, Power, Sex,
Aging, Eccentric, Isometric, Isotonic, Isokinetic
v
CO-AUTHORSHIP STATEMENT
This thesis contains material from published manuscripts (Chapters 2-4). On all
manuscripts, Geoffrey A. Power was the first author and Brian H. Dalton, Charles L.
Rice and Anthony A. Vandervoort were co-authors. William J. Booth was a co-author
of Chapter 5. All experimental data presented in this thesis were collected,
analyzed, and interpreted by Geoffrey A. Power.
vi
ACKNOWLEDGMENTS
First and foremost I would like to thank my family for their unconditional
love and support for all of my endeavors. Dad, your support whether it was driving
to the races or asking how my school work is going keeps pushing me to reach the
goals I set for myself and make you proud. Mom, I should probably blame you for
my stubbornness or what has actually been key personality trait to my success in
academia “tenaciousness”! Both of you have instilled in me many life lessons and
taught me the meaning of hard work and I am grateful for that. Julie, you support
me in: life, work and leisure all of which seem to overlap and mash into a whirlwind,
sometimes I do not always see when extra attention is needed on the most
important -life. Thanks for your understanding, love and support.
A special thanks to my Lab mates for helping with my experiments and
providing critical feedback on my work. Specifically, Arthur, Brad, and Brian, you
guys truly made this an enjoyable and memorable 4 years. Brian, I attribute much of
my academic success to your guidance and help. Not only did you push me in the
lab but were a fantastic training partner for cycling.
Charles, thanks for allowing me to work in your lab alongside your students.
Your support through discussions and edits to my manuscripts contributed greatly
to my productivity. I really like how you run your lab and this is something I will try
to emulate one day. Your wit and humor made everyday a pleasure. With
everything I have learned from you I will ‘go boldly’ into a future of research.
Tony, your supervision and mentorship has had a profound impact on my
research and professional philosophies. I enjoyed our lengthy discussions which
tended to meander from time to time but perhaps, this was a learning experience in
itself to take a global perspective and not just get caught up in the minute details. I
honestly do not think there is a better training environment than the one you
provided me with, thank you.
"Only those who will risk going too far can possibly find out how far one can go."-T. S. Eliot-
vii
TABLE OF CONTENTS
CERTIFICATE OF EXAMINATION .............................................................................................................. ii
ABSTRACT ................................................................................................................................................................ iii
CO-AUTHORSHIP STATEMENT ...................................................................................................................v
ACKNOWLEDGMENTS ..................................................................................................................................... vi
TABLE OF CONTENTS......................................................................................................................................vii
LIST OF TABLES...................................................................................................................................................xii
LIST OF FIGURES .............................................................................................................................................. xiii
LIST OF APPENDICES ...................................................................................................................................... xv
LIST OF ABBREVIATIONS............................................................................................................................xvi
GLOSSARY OF TERMS................................................................................................................................... xvii
Chapter 1 – General Introduction ............................................................................................................... 1
1.0 Mechanics of Lengthening Contractions .................................................................................. 1
1.1 Structural Changes Associated With Muscle Damage...................................................... 4
1.2 Mechanisms of Damage Induced Force Loss ......................................................................... 5
1.3 Common Markers of Muscle Damage......................................................................................... 7
1.4 Neuromuscular Function Following Muscle Damage ...................................................... 9
1.5 Sex Differences in Response to Muscle Damage............................................................... 10
1.6 Effects of Age on Muscle Damage .............................................................................................. 11
1.7 Limb-Muscle Model............................................................................................................................ 12
1.8 Purpose...................................................................................................................................................... 14
1.9 References................................................................................................................................................ 17
viii
Chapter 2 – Reproducibility of velocity-dependent power: before and after
lengthening contractions.......................................................................................................................... 23
2.0 Introduction ............................................................................................................................................ 23
2.1 Methods ..................................................................................................................................................... 26
2.1.1 Experimental approach to the problem....................................................................... 26
2.1.2 Subjects........................................................................................................................................... 26
2.1.3 Experimental set-up ................................................................................................................ 27
2.1.4 Procedures .................................................................................................................................... 27
2.1.5 Lengthening contraction intervention ......................................................................... 30
2.1.6 Data reduction and analysis............................................................................................... 31
2.1.7 Statistical analysis ................................................................................................................... 31
2.2 Results ........................................................................................................................................................ 32
2.3 Discussion ................................................................................................................................................ 37
2.4 References ............................................................................................................................................... 42
Chapter 3 – Delayed recovery of velocity-dependent power loss following
eccentric actions of the ankle dorsiflexors.................................................................................... 45
3.0 Introduction ............................................................................................................................................ 45
3.1 Methods ..................................................................................................................................................... 48
3.1.1 Participants.................................................................................................................................. 48
3.1.2 Experimental set-up ................................................................................................................ 49
3.1.3 Experimental procedures ..................................................................................................... 50
3.1.4 Fatigue and recovery protocol .......................................................................................... 52
3.1.5 Data reduction and analysis............................................................................................... 54
3.1.6 Statistical analysis ................................................................................................................... 55
3.2 Results ........................................................................................................................................................ 55
ix
3.2.1 Baseline measures .................................................................................................................... 55
3.2.2 Fatigue and recovery measures........................................................................................ 58
3.3 Discussion ................................................................................................................................................ 64
3.4 References ............................................................................................................................................... 70
Chapter 4 – Power loss is greater following lengthening contractions in old
versus young women .................................................................................................................................. 75
4.0 Introduction ............................................................................................................................................ 75
4.1 Methods ..................................................................................................................................................... 79
4.1.1 Participants.................................................................................................................................. 79
4.1.2 Experimental arrangement............................................................................................... 79
4.1.3 Experimental procedures ..................................................................................................... 81
4.1.4 Fatigue and recovery protocol .......................................................................................... 83
4.1.5 Data reduction and analysis............................................................................................... 83
4.1.6 Statistical analysis ................................................................................................................... 84
4.2 Results ........................................................................................................................................................ 85
4.2.1 Baseline measures .................................................................................................................... 85
4.2.2 Fatigue and recovery measures........................................................................................ 88
4.3 Discussion ................................................................................................................................................ 96
4.3.1 Baseline .......................................................................................................................................... 97
4.3.2 Lengthening contraction intervention ......................................................................... 97
4.3.3 Fatigue and muscle damage............................................................................................... 99
4.3.4 Young vs. old metabolic (dis)advantage................................................................... 101
4.4 References ............................................................................................................................................ 105
x
Chapter 5 – A leftward shift in the torque-velocity relationship following muscle
damage results in a preferential loss of power at higher loads..................................... 111
5.0 Introduction ......................................................................................................................................... 111
5.1 Methods .................................................................................................................................................. 114
5.1.1 Participants............................................................................................................................... 114
5.1.2 Experimental arrangement ............................................................................................. 114
5.1.3 Electromyography (EMG) ................................................................................................. 115
5.1.4 Electrical stimulation .......................................................................................................... 116
5.1.5 Maximal voluntary isometric contraction (MVC)................................................ 116
5.1.6 Power curve determination ............................................................................................. 117
5.1.7 Damage and recovery protocol...................................................................................... 119
5.1.8 Data reduction and analysis............................................................................................ 121
5.1.9 Statistical analysis ................................................................................................................ 122
5.2 Results ..................................................................................................................................................... 122
5.2.1 Baseline measures ................................................................................................................. 122
5.2.2 Markers of muscle damage .............................................................................................. 128
5.2.3 Lengthening contraction task and recovery measures .................................... 130
5.3 Discussion ............................................................................................................................................. 137
5.3.1 Strength loss ............................................................................................................................. 138
5.3.2 Velocity and power ............................................................................................................... 139
5.3.3 Velocity specific alterations in power ........................................................................ 141
5.4 References ............................................................................................................................................ 144
Chapter 6 – General discussion and summary ............................................................................. 147
6.1 Limitations............................................................................................................................................ 152
xi
6.2 Future Directions.............................................................................................................................. 154
6.3 Summary................................................................................................................................................ 155
6.4 References ............................................................................................................................................ 157
Appendix A ........................................................................................................................................................... 159
Appendix B ........................................................................................................................................................... 160
Curriculum Vitae............................................................................................................................................... 162
xii
LIST OF TABLES
Table 1. Absolute baseline measures and reliability statistics for maximal
shortening velocity and peak power. ...............................................................................................................35
Table 2. Baseline contractile data. ....................................................................................................................57
Table 3. Voluntary and evoked participant baseline characteristics..........................................87
Table 4. Voluntary and electrically evoked neuromuscular properties of the
dorsiflexors. ..................................................................................................................................................................124
Table 5. Dynamic rate of torque development RTD (N·m·s-1) values preceding and
succeeding muscle damage. ................................................................................................................................126
Table 6. Rates of neuromuscular activation (mV/s) preceding and succeeding
muscle damage. ..........................................................................................................................................................127
xiii
LIST OF FIGURES
Figure 1. Force-velocity (FV) relationship. ....................................................................................................3
Figure 2. A schematic depicting the structure of an individual sarcomere. ..............................5
Figure 3. A schematic depicting the sarcomere length-tension (FL) relationship. ...............7
Figure 4. Participant positioned in the Biodex Multi-joint Dynamometer for testing
of the ankle dorsiflexors. .........................................................................................................................................13
Figure 5. Schematic diagram of experimental protocol. .....................................................................28
Figure 6. Bland-Altman plots...............................................................................................................................36
Figure 7. Schematic diagram of experimental protocol. .....................................................................53
Figure 8. Torque-frequency relationship.....................................................................................................57
Figure 9. Maximum isometric voluntary contraction (MVC)...........................................................59
Figure 10. Torque output and activation for a representative subject at 30min of
recovery. ............................................................................................................................................................................60
Figure 11. Low-frequency torque depression (10:50 Hz).................................................................62
Figure 12. Velocity-dependent power. ..........................................................................................................63
Figure 13. Representative unprocessed data. ...........................................................................................87
Figure 14. Velocity-dependent power. ..........................................................................................................89
Figure 15. Maximum voluntary isometric contraction (MVC)........................................................91
Figure 16. Low frequency torque depression (10:50 Hz). ................................................................93
Figure 17. Peak twitch torque (Pt). ..................................................................................................................95
Figure 18. Schematic diagram of experimental protocol. ...............................................................119
Figure 19. Unprocessed data. ...........................................................................................................................122
Figure 20. (A.) Maximal rate of torque development and (B.) maximal voluntary
isometric contraction before and following muscle damage. ........................................................128
xiv
Figure 21. (A.) Maximal shortening velocity and (B.) peak power. ..........................................130
Figure 22. Power loss across multiple loads following muscle damage................................131
Figure 23. Power curves......................................................................................................................................132
Figure 24. (A.) Low frequency torque depression as a combined consequence of
impaired (B.) 10 Hz and (C.) 50 Hz torque. ...............................................................................................134
Figure 25. Peak twitch torque..........................................................................................................................135
Figure 26. Factors related to repetitive lengthening contractions contributing to
reduced shortening velocity and power loss. ..........................................................................................149
Figure 27. Force-velocity and rate of torque development. ..........................................................151
xv
LIST OF APPENDICES
Appendix A. Ethical approval from The University of Western Ontario’s Health
Science Research Ethics Board for research involving human subjects
Appendix B. Permission to reprint previously published manuscripts
xv i
LIST OF ABBREVIATIONS
ANOVA – Analysis of variance
ATP – Adenosine triphosphate
Ca2+ – Calcium
CD – Contraction duration (TPT + HRT)
E-C coupling – Excitation contraction coupling
ES – Effect size
EMG - Electromyography
F-L – Force-length relationship
HRT – Half relaxation time of peak twitch torque
HSD – Honest significant difference
ICC – Interclass correlation coefficients
LFTD – Low frequency torque depression
LOA – Limits of agreement
MVC - Maximal voluntary isometric contraction
M-Wave – Compound muscle action potential
ROM – Range of motion
Pt – Peak twitch amplitude
Pd – Peak doublet amplitude
SD – Standard deviation
SE – Standard error
RMS – Root mean square
RTD – Rate of torque development
TA – Tibialis anterior muscle
TEM – Typical error
TEMCV – Typical error expressed as a coefficient of variation
T-V relationship – Torque-velocity relationship
TPT – Time to peak twitch torque
VA – Voluntary activation
xv ii
GLOSSARY OF TERMS
Angular Velocity – Change in angular position over time.
Force – A vector which has both magnitude and direction, the product of mass and
acceleration.
Isokinetic – A dynamic muscular contraction in which the angular joint velocity is
constant and the resistance (i.e., torque) is variable.
Isometric – A static muscular contraction.
Isotonic – The dynamic contraction mode in which a load is held constant and the
joint angular velocity is variable as the limb moves through a range of motion.
Muscle Damage – Exercise induced dysfunction to the structure and function of
skeletal muscle.
Neuromuscular Fatigue – Any exercise-induced reduction in the ability to generate
torque or power regardless of whether or not the task can be sustained.
Power – The product of torque (N·m) and joint angular velocity (rad/s) expressed
in watts (W); considered to be a more relevant measure of function because it
incorporates both strength and contractile speed.
Torque – Also termed ‘moment’ is the product of the lever arm length, the
magnitude of force vector, and the sine of the angle between the force vector and the
lever arm vector, and is expressed in newton·meters (N·m).
Velocity-Dependent Contraction – Velocity-dependent contractions are those in
which the imposed load remains relatively constant (i.e., isotonic-like) and the
velocity is allowed to vary throughout the joint range of motion and is dependent
upon the maximal effort of the subject.
Muscle Weakness – An inability to produce expected muscular strength.
1
Chapter 1– General Introduction
Skeletal muscle is a remarkable, highly organized tissue which regulates
metabolic processes, is important in thermoregulation and ultimately serves as a
‘molecular motor’. Muscles produce tension, pull on tendons and move bones to
produce meaningful movement and locomotion. Not only do muscles pull and
shorten, but when an external load overcomes the tension produced by the muscle,
they lengthen actively. Lengthening muscle actions are a normal part of daily
activity whether it be absorbing energy when landing from a jump or walking down
a flight of stairs. For a given resistance, these contractions are less energetically
demanding, cause less metabolic disturbance and generally produce greater forces
than shortening or isometric contractions (2, 7, 35). Because of the greater tension
associated with lengthening versus shortening or isometric contractions (28), and
the high strain placed on the myofilaments, this contraction type is prone to causing
muscle damage (46, 63). However, there is minimal knowledge regarding how
unconstrained isotonic-like power (i.e., velocity-dependent power) production in
humans is impaired following muscle damage, specifically the role of shortening
velocity.
1.0 Mechanics of Lengthening Contractions
The first published investigation of lengthening contractions and muscle damage
in humans was a study by Theodore Hough at the turn of the twentieth century (36).
The simple study design involved participants contracting their finger against a
2
spring, thus shortening the muscle while stretching the spring and experiencing
unaccustomed lengthening during the spring recoil. Following the task, Hough
described a long lasting muscle pain which he distinguished from the short term
transient pain of repetitive shortening or sustained isometric actions. Hough
suggested the short term pain was associated with muscle fatigue and was due to
the accumulation of metabolites while the long lasting soreness was caused
ultimately by ‘some sort of rupture within the muscle’, which we now know as
muscle damage. Indeed, lengthening muscle actions possess several unique features
compared with those of other muscle actions, which lead to a greater susceptibility
to muscle damage (4). First, based on the force-velocity (F-V) relationship (Figure
1) established by Katz (39), the force generated during muscle lengthening is 1.5-1.9
times greater as compared to isometric force (24). The F-V relationship dictates
that, as a muscle shortens and velocity changes from zero, force generating capacity
drops, owing to the decreased probability of interaction between the contractile
proteins actin and myosin, and that muscle force also decreases as a function of
shortening velocity (34). Conversely, during lengthening, when a muscle is
stretched actively, muscle force is elevated above isometric and shortening muscle
force due to a tighter packing of myofilaments increasing the contact area between
actin and myosin effectively increasing bond formation leading to a firmer
attachment of the cross bridge (24). As well, the engagement of passive force
transmitting elements (25, 33) contributes to the elevated tension. Katz (39)
observed a discontinuity in the F-V relationship during lengthening such that
greater force was required for a given rate of stretch than for the same rate of
3
shortening. Additionally, following rapid stretching, the muscle became
permanently weaker, and there was a shift in the optimal length of force production
towards longer muscle lengths (39), suggesting the presence of damaged and
overstretched sarcomeres (11, 32).
Furthermore, muscle activity as indicated via surface electromyography (EMG)
is lower for maximal lengthening actions compared with isometric and shortening
(10, 23, 26) contractions. Therefore, the combination of higher forces during
lengthening and lower levels of muscle activity (i.e., less active muscle mass
involved) places greater tensile strain on the involved remaining structures (26).
Finally, force generation during lengthening differs from shortening whereby cross-
bridges are broken mechanically rather than undergoing detachment by high-
energy phosphates (ATP) (5). The forced detachment places greater strain on the
myofilaments and contributes to muscle damage following lengthening contractions.
4
Figure 1. Force-velocity (FV) relationship
The angular velocity of movement is represented along the X-axis, with Vmax
representing maximum unloaded movement velocity for a representative young and
older adult. Torque and power are represented on the dual Y-axis, Fmax represents
maximum voluntary torque and Pmax represents the finely tuned trade-off of
angular velocity and torque to achieve peak power. Note the hyperbolic FV curve
and power curve for the older adult is shifted left-ward (1) down (2) and relative to
the young adult. Adapted from Raj et al. Exp Gerontol 45: 81-90, 2010.
1.1 Structural Changes Associated With Muscle Damage
Unaccustomed repeated lengthening contractions result in muscle damage (28).
Evidence of structural and morphological changes to the muscle following
lengthening contractions in humans came from Friden (29). Following
unaccustomed lengthening contractions of the lower limbs, muscle biopsies were
obtained from the vastus lateralis of participants. Analysis of the muscle tissue was
performed via electron microscopy which identified disturbances to the
ultrastructural milieu of the sarcomere (29). Damage to the sarcomere was
5
observed along the Z-line (Figure 2) which included: Z-line broadening, spreading of
the Z-line material throughout the sarcomere, and non-uniform disturbed Z-lines
throughout the fiber. These structural changes and disorganization of Z -lines
contribute to impaired force production and transmission. Thus, during
lengthening contractions when the muscle is under active strain over the
descending limb of the length-tension (Figure 3) curve (46, 55), there is mechanical
disruption of the actin-myosin bonds, and cytoskeleton of the muscle fibers.
Ultimately, this damage results in a prolonged reduction in maximal voluntary force
(6, 72).
Figure 2. A schematic depicting the structure of an individual sarcomere.
1.2 Mechanisms of Damage Induced Force Loss
The extent of muscle damage induced force loss following lengthening
contractions is determined by multiple factors, which include: the number of
lengthening contractions, the initial muscle length (i.e., location on the force-length
6
(F-L) relationship; Figure 3), amplitude of stretch, the tension reached during
stretch, and the contractile history (4, 18). Ultimately, force is reduced by a
disturbance to the contractile machinery and failure to activate viable intact
structures. Structurally, weakened and overstretched sarcomeres result in a shift in
the peak of the F-L relationship to longer muscle lengths for optimal torque
production (32). As well, sarcomeres stretched further along the descending limb of
the F-L relationship may fail to re-interdigitate, thus producing lower force due to
less thick and thin filament overlap (54, 55). Therefore, when isometric force is
measured at the same muscle length prior to lengthening contractions and not the
new optimal muscle length, force will appear to be reduced. The examination of
isometric strength as a function of joint angle/muscle length reveals a
disproportionate loss of strength at joint angles corresponding to short versus long
muscle lengths (59). These findings lend support to the idea that longer muscle
lengths are required to achieve the same myofilament overlap after muscle damage
and hence one contributing factor to force loss after damage is an increase in series
compliance as a result of overextended sarcomeres (11, 32).
Not only are muscle contractile structures damaged following lengthening
contractions, but, impaired force production can also be attributed to failure of
excitation-contraction (E-C) coupling. Excitation-contraction coupling is the
cascade of events that begins with the transmission of an action potential along the
sarcolemma and ends with the release of calcium (Ca2+) from the sarcoplasmic
reticulum and subsequent activation of the contractile machinery. Reduced Ca2+
release as a result of damage induced dysfunction to structural components
7
involved in E-C coupling, and reduced myofibular Ca2+ sensitivity (5, 37, 71) result in
impaired force production capability (71). A reduced efficiency of the E-C coupling
process is commonly observed following damage and in some cases (37) the failure
to activate the contractile machinery following lengthening contractions contributes
more (75%) than actual structural damage to the functional impairment/force
generation.
Figure 3. A schematic depicting the sarcomere length-tension (FL) relationship.
At short muscle lengths, along the ascending limb of the curve, force is reduced due
to too much overlap of thick and thin myofilaments. Optimal length is reached over
the plateau region. On the descending limb, force is reduced owing to less
interaction of myofilaments. Adapted and modified from Martini (2001, p. 115.)
8
1.3 Common Markers of Muscle Damage
The invasive nature of muscle biopsies, renders this technique less feasible to
perform in some muscles to determine the incidence of muscle damage following
lengthening contractions in humans. It has been suggested that hypercontracted
fibers as evidence of ultrastructural damage might be caused by the biopsy
procedure itself. Thus, the biopsy procedure can produce come changes mistaken
for damage (18). Therefore, many non-invasive indirect measures of muscle
damage are commonly used. The three most frequently used markers are: 1)
subjective reports of muscle soreness, 2) blood protein assessment and 3) recovery
of maximal voluntary muscle strength (18, 72). Maximal voluntary isometric torque
generating capacity (MVC) is generally regarded as the best indirect measure of
muscle damage and functional impairment following lengthening contractions in
investigations on human subjects (72). Maximal voluntary torque is less impaired
immediately following high-intensity lengthening actions than following shortening
or isometric tasks (8, 43, 57). However, when assessed throughout recovery and
day(s) later, MVC torque loss following shortening contractions recovers fully;
whereas following lengthening contractions torque loss remains (68). Because the
fatigue induced from repetitive contractions is transient and recovers relatively
quickly compared with muscle damage, the incomplete recovery of both voluntary
and electrically evoked torque cannot be attributed to fatigue. Thus, the remaining
impairment in maximal torque capacity (i.e., MVC) represents muscle damage.
Self reported soreness and blood markers do not correlate well with measures of
functional impairment. Muscle soreness and blood markers typically peak 48 hrs
9
following the initial insult to the muscle structures (13, 44, 53), during which time
strength is already starting to recover. The mismatch between these markers and
recovery of functional impairment does not lend support to the utility of soreness
and blood markers as indirect measures of muscle damage. Thus, MVC performance
is a relatively accurate and reliable measure, and provides the means for
determining muscle function (12). The incomplete recovery of MVC torque
following lengthening contractions suggests strongly that the muscle fibers are
damaged (6). Nevertheless, an important issue in all studies of lengthening muscle
actions is to distinguish between the reduction in force caused by fatigue and that
caused by muscle damage (17). To corroborate results from an impaired MVC
another useful measure in quantifying muscle damage is the shift in optimal angle of
torque production to longer muscle lengths (62). The presence of overstretched,
disrupted sarcomeres in series with still functional sarcomeres results in an
immediate shift in optimum length of torque production to longer muscle lengths
and is considered to be a reliable indicator of muscle damage (32, 62). This shift
following lengthening contractions has been observed previously in the ankle
dorsiflexors (45, 61).
1.4 Neuromuscular Function Following Muscle Damage
Optimal power generation is based on the finely tuned relationship between
torque and velocity. As velocity increases, less torque can be generated owing to
fewer cross-bridge attachments, requiring a trade-off of torque in favor of velocity
to achieve peak power (3, 47). Following muscle damage, maximal isometric
10
dorsiflexion torque (8, 50, 57) is reduced although little is known regarding power
loss. Voluntary maximal loaded shortening velocity is known to recover rapidly (< 5
min) in young adults after voluntary isometric and concentric fatigue tasks (15, 16).
However, repeated lengthening contractions result in muscle damage which can
take several days to recover fully (18), and it is unclear how this damage may affect
velocity-dependent power production during short-term recovery. Up to now, the
only available data of velocity-specific alterations in power in humans are based on
studies involving isovelocity (i.e., constant speed/isokinetic) actions (12, 67). To
determine the extent of concentric strength loss following muscle damage an
isovelocity model relies specifically on testing the torque component of power when
angular velocity is fixed and results from this paradigm are equivocal. Some report
greater impairments at slow angular velocities, thus reflecting impaired torque
generation (21, 52); whereas others report greater impairments at fast velocities
suggesting shortening velocity is more impaired than torque generation (27, 29, 31).
However, the isovelocity contraction mode constrains angular velocity artificially
and therefore does not properly represent normal contractile function of the limb
muscle model. Importantly, when torque is held constant and velocity can vary
freely (i.e., velocity-dependent), the muscle functions more closely to in vivo
conditions (60), and alterations in the power curve can be explored to offer insight
on the mechanisms of power loss following muscle damage.
A loss of capacity to produce high torques rapidly (i.e., rate of torque
development; RTD) would contribute much less to power production for lighter
loads whereas at higher loads it would presumably impede power production
11
severely. In other words, because shortening velocity is related to the number of
sarcomeres working in series whilst torque production is related to those
sarcomeres in parallel (56), muscle damage would preferentially affect torque
production, and would therefore result in a greater loss of power at heavier rather
than lighter loads following muscle damage. This is an under studied but important
area of research which needs further elucidation, and investigations of populations
with specific characteristics as described below can help explain the role of
shortening velocity and power loss following muscle damage.
1.5 Sex Differences in Response to Muscle Damage
In contrast to the literature on sex-differences following muscle damage in
animals, reports on sex-related differences in response to damaging lengthening
contractions in humans are equivocal, or show a greater impairment in women than
men [for review see (18) and references therein]. Following lengthening
contractions in a large sample of men (n=98) and women (n=94), Sayers & Clarkson
(68) reported that a disproportionately higher number of women than men
demonstrated greater initial force loss. In addition, despite similar indices of muscle
damage in the elbow flexors of both sexes, Sewright et al., (69) showed that
immediate strength loss was more prominent in women than men. Women and
men had similar markers of muscle damage, but women had a greater impairment
in strength. This finding can be interpreted as E-C uncoupling playing a key role in
the observed sex-difference. Additionally, muscle damage results in impaired RTD
(9, 53), potentially diminishing power production. Thus, in women, muscle damage
12
induced dysfunction may be exacerbated due to a greater susceptibility to E-C
coupling failure and lower RTD compared with men, owing to a lower Type II/Type
I fiber area ratio (42).
1.6 Effects of Age on Muscle Damage
Impaired force generating capacity is a consequence of natural adult aging
resulting from many factors (66) including: the loss of contractile muscle mass and
motor units (22, 56, 70), decreased neural activation (1, 65), changes in muscle
architecture (56) and excitation-contraction uncoupling (58). Because E-C coupling
is compromised in older adults (58) and maximal unconstrained shortening velocity
is indeed slower (19, 20, 51, 64) compared with younger adults, the old may be
energetically disadvantaged during repetitive lengthening contractions. Therefore,
older adults may experience a greater perturbation in ATP homeostasis,
consequently exacerbating their fatigue response and resulting in a greater
reduction in shortening velocity and subsequent velocity-dependent power
following repetitive lengthening contractions than young adults. Moreover
functional impairments following muscle damage have been previously attributed
to impaired E-C coupling (71). A mechanical disruption of the link between the t-
tubule and the sarcoplasmic reticulum impairing Ca2+ release (37) could further
impair an already compromised system. Furthermore, dynamic concentric muscle
performance following multi-joint lengthening contractions is known to be impaired
(12, 67) although the underlying mechanisms are not understood entirely. Thereby,
stressing a system which is already compromised in terms of E-C coupling and
13
shortening velocity will aid in understanding these physiological mechanisms of
muscle damage on subsequent power loss.
1.7 Limb-Muscle Model
The ankle dorsiflexors were chosen as the model for my studies due to the many
advantages of this particular muscle group. The fibular nerve is easily accessible at
the head of the fibula for percutaneous electrical stimulation. The dorsiflexor
muscle group’s consistently high voluntary activation level, with minimal
familiarization trials required, aids in comparing muscle damage studies between
young and older adults (40, 41). The main dorsiflexor, the tibialis anterior (TA),
contributes approximately 40-60% to dorsiflexion torque. The 40% value was
estimated via focal tetanus to the TA, relative to fibular nerve stimulation (14, 49).
However, based on the physiological cross-sectional area of the TA relative to the
other dorsiflexors, Fukunaga et al. (30) suggest the TA contributes ~60% to
dorsiflexion torque. The TA is a primarily slow twitch muscle, composed of ~76%
(38) Type I muscle fibers. The dorsiflexors have a flat force-length relationship
(14), reaching peak torque values over both the ascending and plateau regions (48).
Therefore, age-related changes in fiber type and alterations in the F-L relationship
should be of minor influence in interpreting the results.
14
Figure 4. Participant positioned in the Biodex Multi-joint Dynamometer for testing
of the ankle dorsiflexors. Graphic art provided by Mr. Andrew Davidson.
15
Testing was performed on a Biodex dynamometer (Figure 4), using the ankle
attachment for dorsiflexion. All subjects were recreationally active and not
systematically trained. The isotonic mode was used to perform ‘velocity-dependent’
contractions. A velocity-dependent movement is characterized by a participant
producing a dynamic contraction as fast as possible with only minimal constraint in
the angular velocity while the load or resistance is maintained at a pre-determined
value (i.e., %MVC). Before the footplate is displaced during the velocity-dependent
shortening contraction, the pre-programmed resistance has to be overcome by the
participant. The dynamometer absorbs this increase in applied torque resulting in a
directly proportional increase in angular velocity. This is in contra st to isovelocity
actions (i.e., isokinetic) where the velocity is constrained and torque is recorded.
However, the isovelocity contraction mode constrains angular velocity artificially
and therefore does not properly represent normal contractile function of the limb
muscle model. Importantly, when torque is held fairly constant and velocity can
vary freely (i.e., velocity-dependent), the muscle functions more closely to in vivo
conditions (60), and alterations in the power curve can be explored to offer insight
on the mechanisms of power loss following muscle damage.
1.8 Purpose
Understanding the concomitant reductions in torque generating capacity and
shortening velocity are important in elucidating the mechanism by which power
production is reduced and neuromuscular function impaired following damaging
lengthening contractions. Skeletal muscles are designed to modulate shortening
16
velocity based upon the load imposed (isotonic) and not vice-versa (isokinetic). The
following series of investigations employed a velocity-dependent model which
aimed to offer insight into the mechanisms of power loss following muscle damage.
Reliable measures of strength and power output are critical for the assessment of
neuromuscular function. Therefore, In Chapter 2 the purpose was to provide an
initial assessment of the day-to-day reproducibility of shortening velocity and
power variables, using the isotonic testing mode of the Biodex dynamometer.
Owing to the lower metabolic cost of lengthening contractions, but greater
muscle damage compared with isometric or shortening contractions, it remains
unclear whether velocity-dependent power loss is different between this type of
exercise and repeated isometric or concentric contraction tasks. In Chapter 3, the
purpose was to investigate the effect of high-intensity lengthening contractions on
neuromuscular function and velocity-dependent power in young men and women.
A secondary purpose was to explore further the equivocal observations in the
literature regarding sex-related differences in muscle fatigue and responses to
lengthening contractions. As an extension, the purpose of Chapter 4 was to
investigate neuromuscular function in older and younger women with a particular
emphasis on short-term recovery of velocity-dependent power following muscle
damage. Finally, in Chapter 5, the purpose was to investigate velocity-dependent
power loss following muscle damage, and to determine whether a sex -difference
exists when assessed across multiple loads; stressing torque production and near
maximal shortening velocities.
17
The hypotheses were that: 1) measurement methods for velocity and power
following muscle damage will yield good reliability; 2) there will be a modest
reduction in shortening velocity due to muscle damage, resulting in velocity-
dependent power loss which will remain reduced throughout recovery in both men
and women; 3) as a result of muscle damage levels that are comparable, MVC torque
will be reduced similarly in both old and young women and remain reduced
throughout a 30 min recovery period. However, when tested under dynamic
conditions, older women will have a larger reduction in velocity-dependent power
than the young owing to a greater impairment in E-C coupling and shortening
velocity, which are known to be compromised in older adults and may not be
observable during isometric testing. As a result of muscle damage neither group
will recover by 30 min. 4) Because torque production is impaired considerably
following muscle damage and the velocity at which a muscle shortens depends on
the force it is resisting, it was hypothesized there would be a left and downward
shift in the power curve, owing to a preferential loss of power at higher loads.
However, maximal shortening velocity and shortening velocity at low loads will not
be affected significantly owing likely to fewer cross-bridge interactions involved
that do not stress the damaged force generators. Finally - to further highlight the
role of muscle damage and impaired RTD - which is a putative major contributor to
power production; I tested women, whom are known to have lower RTD than men.
It was expected that following damage women will have a greater loss of power at
heavier loads than men because of a greater strength loss driven by larger
impairments in RTD and more reliance on the velocity component of power.
18
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muscle: a new mechanism. J Exp Biol 205: 1275-1283, 2002.
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during arm flexion and extension. Influence of strength level. Eur J Appl Physiol
Occup Physiol 60: 395-401, 1990.
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failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 85:
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contraction with advancing age: a brief review. Eur J Appl Physiol 100: 543-551,
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21
42. Krivickas LS, Suh D, Wilkins J, Hughes VA, Roubenoff R, Frontera WR. Age-
and gender-related differences in maximum shortening velocity of skeletal muscle
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eccentric and concentric exercise of the elbow flexors. Eur J Appl Physiol 96: 235-
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and young men following eccentric exercise of the elbow flexors. J Sci Med Sport 11:
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joint angle of the ankle dorsiflexors following eccentric exercise. Experimental
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induced by repetitive maximal eccentric contractions is marginally influenced by
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development and peak torque after eccentric exercise. Clin Physiol Funct Imaging
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22
55. Morgan DL, Proske U. Popping sarcomere hypothesis explains stretch-induced
muscle damage. Clin Exp Pharmacol Physiol 31: 541-545, 2004.
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significance. Br Med Bull 95: 139-159, 2010.
57. Pasquet B, Carpentier A, Duchateau J, Hainaut K. Muscle fatigue during
concentric and eccentric contractions. Muscle Nerve 23: 1727-1735, 2000.
58. Payne AM, Delbono O. Neurogenesis of excitation-contraction uncoupling in
aging skeletal muscle. Exerc Sport Sci Rev 32: 36-40, 2004.
59. Philippou A, Koutsilieris M, Maridaki M. Changes in kinematic variables at
various muscle lengths of human elbow flexors following eccentric exercise. J Muscle
Res Cell Motil 33: 167-175, 2012.
60. Power GA, Dalton BH, Rice CL, Vandervoort AA. Reproducibility of velocity-
dependent power: before and after lengthening contractions. Appl Physiol Nutr
Metab 36: 626-633, 2011.
61. Power GA, Rice CL, Vandervoort AA. Residual force enhancement following
eccentric induced muscle damage. J Biomech 45: 1835-1841, 2012.
62. Prasartwuth O, Allen TJ, Butler JE, Gandevia SC, Taylor JL. Length-dependent
changes in voluntary activation, maximum voluntary torque and twitch responses
after eccentric damage in humans. J Physiol 571: 243-252, 2006.
63. Proske U, Allen TJ. Damage to skeletal muscle from eccentric exercise. Exerc
Sport Sci Rev 33: 98-104, 2005.
64. Raj IS, Bird SR, Shield AJ. Aging and the force-velocity relationship of muscles.
Exp Gerontol 45: 81-90, 2010.
65. Roos MR, Rice CL, Vandervoort AA. Age-related changes in motor unit
function. Muscle Nerve 20: 679-690, 1997.
66. Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC. Evolving concepts on the
age-related changes in "muscle quality". J Cachexia Sarcopenia Muscle 3: 95-109,
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exercise. Eur J Appl Physiol Occup Physiol 56: 704-711, 1987.
68. Sayers SP, Clarkson PM. Force recovery after eccentric exercise in males and
females. Eur J Appl Physiol 84: 122-126, 2001.
23
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differences in response to maximal eccentric exercise. Med Sci Sports Exerc 40: 242-
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24
Chapter 2 – Reproducibility of velocity-dependent power: before and
after lengthening contractions1
2.0 Introduction
Reliability of isokinetic testing at various fixed angular velocities has been
well established (6, 8, 25, 32). However, when muscle power is tested isokinetically
shortening velocity is constrained artificially and does not provide a measure of
muscle performance replicating daily activities, in which the load is fixed and
velocity is unconstrained. A less common, but useful method used to determine
power is to perform contractions under velocity-dependent conditions, whereby
velocity is unconstrained and the contraction is performed at a pre-determined
load. The Biodex Dynamometer can be operated in the isotonic mode to allow for a
fixed resistance (i.e., % maximum voluntary isometric contraction (MVC)) and a
variable unconstrained angular velocity (29, 30) dependent upon the effort of the
subject. Because these contractions involve the acceleration of a constant load
rather than measuring torque produced at a constant velocity, this mode may serve
as a better tool than isokinetic measures during clinical, athletic and laboratory
testing. Due to the recent increase in use of the isotonic mode for baseline
normative measures (19, 33), training (30, 34) and fatigue studies (2, 3, 5, 18, 28) it
is essential to establish the day-to-day reliability and utility of this measure.
1 A version of this chapter has been published. Used with permission from the NRC Resea rch Press.
Power GA, Dalton BH, Rice CL, Vandervoort AA. Reproducibility of velocity-dependent power:
before and after lengthening contractions. Appl Physiol Nutr Metab 36: 626-633, 2011.
25
When testing participants using the isotonic mode of the Biodex
Dynamometer, the individual must first overcome the preset resistance throughout
the range of motion, while any additional torque generated is translated into
increases in velocity. Due to inherent mechanical limitations of the dynamometer
(unable to maintain an exact constant external load), these contractions are not
strictly isotonic and neither are they iso-inertial as the load is fixed (mechanically)
and is determined by the constant braking of the dynamometer (14). Therefore, we
have chosen to refer to these contractions as “velocity-dependent”, in that these
velocity-dependent movements involve an unconstrained angular velocity while the
contraction is performed at a pre-determined load (i.e., %MVC).
The determination of strength and power under isokinetic conditions has
been shown to be reliable (ICCs) in muscles about the ankle [0.61-0.96] (10, 11, 25,
26), knee [0.82-0.98] (8, 23, 24, 32), elbow [0.95-0.97] (16) and shoulder [0.60-
0.95] (17, 20) joints, as well as during and following fatigue interventions [0.82-
0.89] (23, 25). However, isotonic and isokinetic testing involve different
mechanical constraints which are likely to necessitate altered neuromuscular
strategies to perform each movement effectively (29, 30). Thus, reliability of the
isotonic mode should be evaluated, and may result in different outcomes than
isokinetic maneuvers.
Fatigue, defined as any exercise-induced reduction in muscle performance is
task-dependent and multi-faceted (7), and thus should be assessed using a
multitude of tasks in addition to the most common, isometric strength (3).
Isometric and isokinetic tasks utilize torque as the index of fatigue whereas for
26
velocity-dependent contractions, velocity is the underlying parameter that largely
reflects changes in power over time. Isokinetic contractions are limited by a
constant fixed velocity and provide limited information regarding fatigue-induced
alterations in shortening velocity, which ultimately is the major determinant of
power-loss during daily activities with unconstrained velocities. It is of particular
interest to explore the reliability of these measures to track group changes following
a bout of unaccustomed lengthening contractions, which in addition to muscle
fatigue are known to induce muscle damage (4, 21) and require a prolonged
recovery (28) for the return of neuromuscular function. Because torque generation
capacity is more impaired following damaging lengthening contractions than loaded
shortening velocity (28), a moderately loaded contraction (i.e., 20% MVC) may
provide a reliable day-to-day measure of muscle function following lengthening
contractions such as those incurred during plyometric training.
The importance of accurately reproducing strength and power values is
critical for the assessment of fatigue and training induced alterations in muscle
function. Furthermore, the ankle dorsiflexors were chosen as the model of study
due to this muscle group’s consistently high voluntary activation with little need for
subject familiarization (15). Therefore, the purpose of this investigation was to
provide an initial determination of the day-to-day reliability of maximum shortening
velocity and peak power in healthy young adults, using an isotonic testing mode and
further the understanding of fatigue and recovery of shortening velocity following
lengthening contractions.
27
2.1 Methods
2.1.1 Experimental approach to the problem: A group of healthy young men
and women performed dynamic contractions on a Biodex Dynamometer operated
using the ‘isotonic mode’. Day-to-day reliability of velocity-dependent power
(calculated at 20% MVC) was evaluated at baseline and following repeated high-
intensity lengthening contractions. Data were collected approximately the same
time of day on two separate testing sessions seven days apart. Intraclass correlation
coefficients (ICC2,1) with 95% confidence intervals were used to determine relative
reliability, while absolute reliability measures included typical error (TEM) and
typical error expressed as a coefficient of variation (TEMCV). Bland-Altman plots
were constructed to provide a visual representation of systematic bias and
variability.
2.1.2 Subjects: Twenty four young men (n=10; 25.6 ± 2.9 y) and women (25.3
± 1.8 y) from the university population volunteered for this study. The mean height
and body mass of the men and women were: 176.4 ± 6.8 cm, 76.8 ± 7.8 kg and 166.9
± 6.6 cm, 61.5 ± 10.7 kg, respectively. Participants were recreationally active and
free from musculoskeletal disorders and were not involved in systematic resistance
training of the dorsiflexors, or were competitive runners. This study received
approval from the University of Western Ontario Review Board for Health Sciences
Research Involving Human Subjects and conformed to the Declaration of Helsinki.
Informed, oral and written consent were obtained prior to testing. Participants
were asked to refrain from strenuous exercise 24 hr prior to the day of testing and
to not consume caffeine on the day of testing.
28
2.1.3 Experimental set-up: A Biodex multi-joint dynamometer (System 3,
Biodex(TM) Medical Systems, Shirley, New York) was used for testing and calibration
was verified according to Biodex(TM) System 3 guidelines. All dynamic contractions
were performed in the isotonic mode. The right foot was strapped tightly to the
footplate with the ankle in line with the rotational axis of the dynamometer.
Extraneous body movements were minimized using non-elastic shoulder, waist and
thigh straps. Participants were positioned on the chair with hip and knee angles at
~110o and ~140o, respectively, and ankle angle at ~30o plantar flexion. All
isometric contractions were performed at 30o of plantar flexion. Voluntary
shortening contractions began from the plantar flexed position of 30o and ended at
the neutral ankle angle (0o), thus moving through a 30o range of motion. Before the
footplate moved during the velocity-dependent shortening contractions,
participants had to overcome the pre-programmed resistance. The dynamometer
absorbs this increase in applied torque resulting in a directly proportional increase
in angular velocity (29).
2.1.4 Procedures: Velocity-dependent contractions were performed at 20% of
MVC. Pilot testing indicated that a 20% MVC load represents a moderate resistance
in which the participant could perform fast shortening contractions without range
of motion failure following high-intensity lengthening contractions. Three MVCs
were performed for 3-5 s, with three min rest between all contractions (Figure 5).
Participants were provided visual feedback of the torque, and exhorted during all
voluntary contractions. To ensure MVCs were maximal, voluntary activation was
assessed using the modified interpolated twitch technique (9).
29
Figure 5. Schematic diagram of experimental protocol.
Baseline measures, a fatigue intervention and recovery measures were performed in
the same order during two sessions separated by 7 days. Day-to-day reliability
analyses were performed on peak velocity and power for the baseline velocity-
dependent contractions and the recovery response of these measures following the
fatigue intervention. Grey bars are maximum voluntary isometric contractions
(MVC). Open triangles are electrically evoked contractions (twitch and twitch
doublet). Open arrows indicate the stimuli of the electrically evoked twitches; and
filled arrows are electrically evoked doublets. Filled profiles are dynamic
contractions; fast velocity-dependent shortening contractions at 20% MVC
(triangles), and dynamic lengthening contractions at 80% MVC (rectangles).
Recovery time points: 30s, 2, 5, 10, 15, 20, 30 min.
30
Contractions of the tibialis anterior were electrically evoked using a bar
electrode held distal to the fibular head over the deep branch of the common fibular
nerve. A computer-triggered stimulator (model DS7AH, Digitimer. Welwyn Garden
City, Hertfordshire, UK) was used with a setting of 400 V and a pulse width of 100
µs. The amplitude of the interpolated torque evoked during the peak plateau of the
MVC (Ts) was compared with a resting twitch doublet torque evoked when the
muscle was relaxed fully ~1 s following the MVC attempt (Tr). If the superimposed
twitch doublet torque amplitude was visible during the MVC, the participant was
encouraged further to perform an additional attempt until there was indeed
minimal voluntary activation failure. Percent voluntary activation was calculated as
voluntary activation (%) = [1- (Ts/Tr)] x 100. Values from the MVC with the highest
torque amplitude were used for data analysis.
Once MVC torque was determined to be maximal, the dynamometer was
switched from the isometric to isotonic mode and a load equal to 20% MVC was
programmed. The dynamometer was programmed to allow the footplate to return
to 30o of plantar flexion at the end of each shortening voluntary contraction while
the participant relaxed fully. Familiarization with these ‘fast’ shortening
contractions involved participants performing several (typically 5) velocity-
dependent shortening contractions until a stable baseline value was obtained (no
change in maximal shortening velocity). To ensure a maximal effort (peak velocity)
contraction, all participants were instructed to move the load “as hard and as fast as
possible throughout the entire range of motion”. To assist participants in reaching
their maximal shortening velocity, visual feedback of the velocity profile was
31
provided via a computer monitor, and a horizontal cursor was positioned at the
previous personal best attempt. Participants rested for 3 min and then performed 2
consecutive contractions, the fastest was used to establish baseline values for
maximum shortening velocity and peak power.
2.1.5 Lengthening contraction intervention: Because many natural movements
are comprised of isometric, shortening and lengthening phases we challenged the
system with an under-studied, but important dynamic task of lengthening
contractions to explore reliability following fatigue in relation to velocity and power,
and also uniquely during a period of recovery. Participants performed 5 sets of 30
lengthening dorsiflexion contractions with a load of 80% MVC and each set
separated by 30 s. The contractions started at the neutral ankle angle (0o) and
ended at 30o plantar flexion, thus moving through a 30o range of motion.
Participants were provided with visual feedback of velocity and instructed to resist
while lowering the foot plate through the 30o range of motion over a 1 s period
(~30o/s). The foot was then returned to the neutral ankle position by the
investigator over a period of 2 s. Following task completion on both day 1 and day 2
absolute peak velocity of the shortening contractions were determined from two
contractions performed at each of seven time points throughout recovery; at 0.5
min, 2 min, 5 min, 10 min, 15 min, 20 min, and 30 min (Figure 5). The absolute peak
velocity values from each of the seven recovery time points from day 1 and 2 were
used to assess the reliability of the overall recovery response to the lengthening
contraction protocol (see statistical analysis for specific measures) (27). This
32
allowed for a comprehensive analysis of the reliability of recovery following the
intervention of lengthening contractions.
2.1.6 Data reduction and analysis: Torque, position and velocity data were
sampled at 100 Hz and converted to digital format using a 12-bit analog-to-digital
converter (model 1401 Power, Cambridge Electronic Design, Cambridge, UK). Spike
2 software was used to determine off line values for MVC torque, and voluntary
maximum shortening velocity. Power was calculated as the product of torque (Nm)
and the peak shortening velocity (rad/s) of the faster of two contraction attempts
(as described above).
2.1.7 Statistical analysis: All statistical analyses were performed using SPSS
software (version 16, SPSS Inc. Chicago, IL) and Microsoft Excel 2007 (Microsoft,
Seattle, WA). Paired t-test analysis between day 1 and day 2 was performed to
establish whether reproducibility bias was present for baseline measures.
Reliability of baseline and recovery measures was assessed using the following
statistical analyses. Bland-Altman plots were constructed to provide a visual
representation of systematic bias and variability (1) by plotting the difference of day
1 and day 2 against the individual mean of day 1 and day 2 using either peak
velocity or power at baseline and following the lengthening contractions. Reliability
of maximum shortening velocity and peak power were assessed using the intraclass
correlation coefficient ICC2,1 which is based upon a repeated-measures ANOVA with
testing session as the independent variable (31). The first subscripted number
denotes the model (i.e., 2), selected because it is based upon repeated measures
analysis of variance during which all participants are assessed by the same rater.
33
The second subscripted number signifies the form using either a single score (1) or
the mean of several scores (2). The scores were peak absolute values (31). This
model takes into account differences among participants, testing sessions, and error
variance. Therefore, ICC2,1 with 95% confidence intervals were used to determine
the relative reliability across the 2 testing sessions of peak shortening velocity and
power at baseline and following lengthening contractions. Measures of absolute
reliability include: typical error (TEM), typical error expressed as a coefficient of
variation (TEMCV), and the limits of agreement (LOA) reflecting 95% probability
limits between which the difference scores of day 1 and 2 should fall. Typical error
(TEM) was calculated as the standard deviation of the difference score between the
two days, divided by the square root of 2. Coefficient of variation of the typical error
was calculated as the TEM divided by the average of all trials, multiplied by 100
(12). The LOA was calculated as the mean difference between the two days ± 1.96 x
SD of the difference between the two days. Alpha was set at 0.05, and Table 1 is
presented as means ± standard deviations (SD).
2.2 Results
Among participants, MVCs ranged from 24 to 66 N·m while individual scores
were highly reproducible day to day, thus resulting in similar 20% loads (8.2 ± 2.2
and 8.3 ± 2.2 N·m) with which the loaded velocity-dependent shortening
contractions were performed. The means and SDs for MVC, maximum shortening
velocity, and peak power on day 1 and day 2 are presented in Table 1. There were
no significant differences between day 1 and day 2 for any of these measures (p >
34
0.05). As well, voluntary activation was near maximal at baseline both days (99% ±
1%) and following (96% ± 5%; 95% ± 6%) the lengthening contractions both days
(p > 0.05).
Intraclass correlation coefficients were calculated separately for men and
women for maximum shortening velocity and power at baseline, however ICCs were
not different between sexes for velocity [0.93 (men), 0.94 (women)] or power [0.97
(men), 0.98 (women)]. Thus, data were pooled to represent the reliability of
velocity and power for both men and women for all subsequent analyses.
The differences between test day 1 and day 2 for maximum shortening
velocity and peak power at baseline and following lengthening contractions are
plotted against the average of the two testing sessions for each individual (Figure 6).
The results from the Bland-Altman plots show the mean bias to be positive and
relatively small for velocity and power measures indicating values were slightly
higher on day 2, with fatigue data showing a greater bias towards a positive
difference between the two testing sessions. For all Bland-Altman plots, the 95%
limits of agreement were symmetric around the zero line, with a greater tendency
towards asymmetry for the fatigue data.
Despite fluctuations in mean bias, the intraclass correlations for maximal
shortening velocity and peak power at baseline (presented in Table 1) were
classified as ‘high’ (27). The pooled recovery data over 30 min for maximum
shortening velocity and peak power following the lengthening contractions also
displayed high intraclass correlations for maximal shortening velocity and peak
power.
35
Table 1 Absolute baseline measures and reliability statistics for maximal shortening
velocity and peak power.
Between measurement p-values are not reported for day-to-day recovery data
because the data were pooled over the testing sessions and analyzed as a time effect
of the fatigue intervention.
36
A.
B.
37
C.
D.
Figure 6. Bland-Altman plots
Maximum shortening velocity (deg/s) (A) and peak power (Watts) (B) at baseline
and following the fatigue intervention (C and D), respectively, for women (open
circles) and men (closed circles). The horizontal lines represent the mean bias
(dotted line) and upper and lower 95% limits of agreement. The x-axis is the mean
value of day 1 and day 2, and the y-axis is the difference score of day 2 – day 1.
38
Measures of absolute reliability for maximum shortening velocity and peak
power are presented in Table 1. The typical error and coefficient of variation
associated with shortening velocity was 4.66o/s and 3.25%, respectively. The
typical error and coefficient of variation associated with peak power was 1.2 Watts
and 5.63 %, respectively. Following the lengthening contractions, the typical error
associated with shortening velocity was 6.8o/s and the coefficient of variation was
5.2%. The typical error associated with peak power following the lengthening
contractions was 1.8 Watts and the coefficient of variation was 8.7%.
2.3 Discussion
This study analyzed the day-to-day reproducibility of maximum shortening
velocity and velocity-dependent power with a load set at 20% MVC in healthy young
adults before and after an intervention of repeated high-intensity lengthening
contractions. Our findings demonstrate relative reliability (ICCs) to be ‘high’ at
baseline and following lengthening contractions. Absolute reliability, as assessed,
via coefficient of variation of the typical error for maximum shortening velocity and
peak power resulted in an error of ~3% and ~9% at baseline and following the
lengthening contractions, respectively. As suggested by Portney and Watkins
(2000) intraclass correlations greater than 0.75 are considered to have good
reliability. In this study, ICC confidence intervals for velocity and power at baseline
ranged from 0.85-0.97 and 0.95-0.99, respectively. As well, following the
lengthening contractions we obtained ICC confidence intervals ranging from 0.82-
0.90 and 0.93-0.96 for velocity and power, respectively indicating high reliability.
39
The high reliability of this measure is encouraging and suggests the isotonic mode
can be used in various settings to track group changes such as before and after
training and following fatigue and lengthening contractions.
This study reported TEM and TEMCV; these statistics provide an absolute and
generalizable measure, respectively for comparisons of reliability between
individuals of different strength and power. Typical error provides a reliability
statistic free from the influence of correlations, as well; TEMCV serves as a
dimensionless measure which allows for the comparison across reliability studies
using different testing protocols, participants and measurement tools (12). Here,
lower values for TEM and TEMcv indicate high reliability. Velocity measures
resulted in a TEM of 4.66o/s, and TEMcv of 3.25%, which suggest one would need a
signal-to-noise ratio greater than ~5o/s and a 3.25% difference to observe a value
that would not be associated with systematic error. Power measures resulted in a
TEM of 1.19 Watts, and TEMcv of 5.63%, which suggest one would need a signal to
noise ratio greater than 1.19 Watts and a difference of 5.63% to observe a value that
would not be associated with systematic error. Visual analysis of the graphs and
interpretation of the Bland-Altman analysis showed the mean absolute scores for
maximum shortening velocity and power at baseline to be stable across day 1 and
day 2. The mean bias for velocity (0.19o/s) and power (0.16 Watts) at baseline
suggests there was no practice/learning effect from performing the previous bout.
Adding the element of repeated lengthening contractions over time allows for
potentially more error to affect the true score. There was however only a mean bias
of 3.6o/s and 0.87 Watts for velocity and power, respectively, following the
40
lengthening contractions (Figure 6). The positive mean bias on day 2 following the
lengthening contractions suggests there was less impairment in shortening velocity
and power, thus individuals may have benefited slightly from the previous
experience, such that, the muscle may have adopted a protective mechanism leading
to less impairment in neuromuscular function during the second day of testing,
commonly known as, the “repeated bout effect” (4, 22). For example, the muscle
may have adapted to the previous bout of lengthening contractions with the
addition of more sarcomeres in series (21) and thus, ‘protected’ from subsequent
muscle damage during the second testing day one week later. However, the baseline
values for maximum shortening velocity and peak power were highly consistent
across days (Figure 6), suggesting the muscle had adequate time to recover from the
previous bout of lengthening contractions.
In the present study, the ICC statistics were higher for power than velocity.
This may be attributed to normalization of shortening velocity to a percentage of
one’s MVC (Power (W) = 20% MVC (N·m) x Velocity (rad/s). Reliability methods
based on correlation coefficients, such as ICC, provide a measure of relative
reliability. However, these reliability statistics are influenced by the range of values
measured and give no indication of actual measurement values or systematic
variability within the measure itself (12). Here, the ICC for maximum shortening
velocity was 0.93 while the TEMCV was 3.25%. Although, power had a higher ICC of
0.98 it was associated with more measurement error (5.63%), thus emphasizing the
need for several statistical measures to evaluate reliability effectively. Using the
isotonic mode, in which power is calculated as a percentage of MVC the additional
41
error can be attributed to day-to-day variability of the MVCs and hence emphasizes
the importance of proper control measures to ensure a suitable maximal isometric
effort is obtained prior to isotonic testing.
When performing velocity-dependent contractions strict care ought to be
taken to ensure high reliability. First, the process of obtaining the isometric MVC
must be controlled to achieve a maximal value; depending on the muscle group, this
may require multiple familiarization attempts (9, 13). The current study
investigated the ankle dorsiflexors because of the consistently high voluntary
activation levels reported for this muscle group (15). Secondly, to obtain a
maximal effort (peak velocity) during the velocity-dependent contractions and
reduce the learning effect, participants were required to reach a consistent peak
velocity (no change during five successive attempts) before performing baseline
attempts. A fast, maximal effort can be achieved by providing the participant with
visual feedback of the velocity profile and positioning a horizontal cursor at a
previous personal best. These considerations help to minimize the likelihood of
introducing systematic error into the measurement and ensures high reliability.
Holmback et al. (1999) investigated the isokinetic reliability of the ankle
dorsiflexors of young men and women across a range of velocities (30 – 150o/s).
The ICCs for peak torque when the participants were tested at 120 and 150o/s
(similar to our isotonic velocities) ranged from 0.78-0.80 with a coefficient of
variation of ~13% and a trend of increasing measurement error with increasing
velocity. This is not surprising based upon a study of the mechanical reliability of
the Biodex (6) which showed higher reliability values associated with slower
42
isokinetic velocities. In our study we found high reliability a nd minimal
measurement error associated in determining power before and after lengthening
contractions using the isotonic mode. But, it is unknown in young adults whether
such reliability would be similar when performing isotonic contractions at other
relative workloads which may dictate a faster or slower angular velocity, or place a
greater or lesser demand on rate of torque development. Furthermore, with the
increasing recognition of the isotonic mode for neuromuscular testing (2, 3, 5, 18,
28), reliability should be evaluated in other populations, such as elite athletes,
individuals with athletic injuries or those with musculoskeletal disorders to ensure
the utility of this testing mode.
These measures of relative and absolute reliability indicate velocity-
dependent power is sufficiently reproducible when assessing baseline muscle
characteristics (as in the case of a training intervention) and recovery following an
intervention consisting of lengthening contractions. Acceptability of these values
depends highly on the precision one requires to observe a meaningful difference.
When investigating fatigue-induced changes following an exercise intervention or
over the course of a training study, these day-to-day error fluctuations are relatively
small and should provide reliable measures. To reduce the chance of introducing
systematic error into the measurement when testing under unconstrained velocity
conditions participants must be highly motivated and able to maintain high or at
least consistent voluntary activation of the muscle group involved, and for some
clinical populations this may require multiple practice contractions or separate
familiarization days.
43
2.4 References
1. Atkinson G, Nevill AM. Statistical methods for assessing measurement error
(reliability) in variables relevant to sports medicine. Sports Med 26: 217-238, 1998.
2. Cheng AJ, Rice CL. Fatigue-induced reductions of torque and shortening velocity
are muscle dependent. Med Sci Sports Exerc 42: 1651-1659, 2010.
3. Cheng AJ, Rice CL. Isometric torque and shortening velocity following fatigue and
recovery of different voluntary tasks in the dorsiflexors. Appl Physiol Nutr Metab 34:
866–874, 2009.
4. Clarkson PM, Hubal MJ. Exercise-induced muscle damage in humans. Am J Phys
Med Rehabil 81: S52-69, 2002.
5. Dalton BH, Power GA, Vandervoort AA, Rice CL. Power loss is greater in old
men than young men during fast plantar flexion contractions. J Appl Physiol 109:
1441-1447, 2010.
6. Drouin JM, Valovich-mcLeod TC, Shultz SJ, Gansneder BM, Perrin DH.
Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity,
torque and position measurements. Eur J Appl Physiol 91: 22-29, 2004.
7. Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle
function. J Physiol 586: 11-23, 2008.
8. Feiring DC, Ellenbecker TS, Derscheid GL. Test-retest reliability of the biodex
isokinetic dynamometer. J Orthop Sports Phys Ther 11: 298-300, 1990.
9. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev
81: 1725-1789, 2001.
10. Holmback AM, Porter MM, Downham D, Lexell J. Ankle dorsiflexor muscle
performance in healthy young men and women: reliability of eccentric peak torque
and work measurements. J Rehabil Med 33: 90-96, 2001.
11. Holmback AM, Porter MM, Downham D, Lexell J. Reliability of isokinetic ankle
dorsiflexor strength measurements in healthy young men and women. Scand J
Rehabil Med 31: 229-239, 1999.
12. Hopkins WG. Measures of reliability in sports medicine and science. Sports Med
30: 1-15, 2000.
13. Jakobi JM, Rice CL. Voluntary muscle activation varies with age and muscle
group. J Appl Physiol 93: 457-462, 2002.
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14. Jidovtseff B, Croisier JL, Lhermerout C, Serre L, Sac D, Crielaard JM. The
concept of iso-inertial assessment: Reproducibility analysis and descriptive data.
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contraction with advancing age: a brief review. Eur J Appl Physiol 100: 543-551,
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16. Lund H, Sondergaard K, Zachariassen T, Christensen R, Bulow P, Henriksen
M, Bartels EM, Danneskiold-Samsoe B, Bliddal H. Learning effect of isokinetic
measurements in healthy subjects, and reliability and comparability of Biodex and
Lido dynamometers. Clin Physiol Funct Imaging 25: 75-82, 2005.
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18. McNeil CJ, Rice CL. Fatigability is increased with age during velocity-dependent
contractions of the dorsiflexors. J Gerontol A Biol Sci Med Sci 62: 624-629, 2007.
19. McNeil CJ, Vandervoort AA, Rice CL. Peripheral impairments cause a
progressive age-related loss of strength and velocity-dependent power in the
dorsiflexors. J Appl Physiol 102: 1962-1968, 2007.
20. Meeteren J, Roebroeck ME, Stam HJ. Test-retest reliability in isokinetic muscle
strength measurements of the shoulder. J Rehabil Med 34: 91-95, 2002.
21. Morgan DL, Proske U. Popping sarcomere hypothesis explains stretch-induced
muscle damage. Clin Exp Pharmacol Physiol 31: 541-545, 2004.
22. Nosaka K, Sakamoto K, Newton M, Sacco P. The repeated bout effect of
reduced-load eccentric exercise on elbow flexor muscle damage. Eur J Appl Physiol
85: 34-40, 2001.
23. Pincivero DM, Gear WS, Sterner RL. Assessment of the reliability of high-
intensity quadriceps femoris muscle fatigue. Med Sci Sports Exerc 33: 334-338, 2001.
24. Pincivero DM, Lephart SM, Karunakara RA. Reliability and precision of
isokinetic strength and muscular endurance for the quadriceps and hamstrings. Int J
Sports Med 18: 113-117, 1997.
25. Porter MM, Holmback AM, Lexell J. Reliability of concentric ankle dorsiflexion
fatigue testing. Can J Appl Physiol 27: 116-127, 2002.
26. Porter MM, Vandervoort AA, Kramer JF. A method of measuring standing
isokinetic plantar and dorsiflexion peak torques. Med Sci Sports Exerc 28: 516-522,
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27. Portney LG, Watkins MP. Foundations of clinical research: applications to
practice. Upper Slade River, NJ:Prentice Hall Health 2000.
28. Power GA, Dalton BH, Rice CL, Vandervoort AA. Delayed recovery of velocity-
dependent power loss following eccentric actions of the ankle dorsiflexors. J Appl
Physiol 109: 669-676, 2010.
29. Remaud A, Cornu C, Guevel A. A methodologic approach for the comparison
between dynamic contractions: influences on the neuromuscular system. J Athl
Train 40: 281-287, 2005.
30. Remaud A, Cornu C, Guevel A. Neuromuscular adaptations to 8-week strength
training: isotonic versus isokinetic mode. Eur J Appl Physiol 108: 59-69, 2010.
31. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability.
Psychol Bull 86: 420-428, 1979.
32. Sole G, Hamren J, Milosavljevic S, Nicholson H, Sullivan SJ. Test-retest
reliability of isokinetic knee extension and flexion. Arch Phys Med Rehabil 88: 626-
631, 2007.
33. Valour D, Ochala J, Ballay Y, Pousson M. The influence of ageing on the force-
velocity-power characteristics of human elbow flexor muscles. Exp Gerontol 38: 387-
395, 2003.
34. Valour D, Rouji M, Pousson M. Effects of eccentric training on torque-angular
velocity-power characteristics of elbow flexor muscles in older women. Exp Gerontol
39: 359-368, 2004.
46
Chapter 3 – Delayed recovery of velocity-dependent power loss
following eccentric actions of the ankle dorsiflexors 2
3.0 Introduction
Unaccustomed eccentric exercise is known to induce muscle damage and
impair muscle function (19), although little is known regarding this impairment on
concentric muscle power. Power loss is the result of fatigue-related reductions in
both torque and shortening velocity, but the contributions of fatigue-related
declines in shortening velocity to the reduction in power following eccentric
exercise are unknown. Thus, our interest involves investigating the effects of
repeated eccentric contractions on the ability of the muscle to generate velocity-
dependent power.
Eccentric contractions are characterized by an external load overcoming the
torque produced by the agonist resulting in a lengthening of the muscle. For a given
resistance, these contractions are less energetically demanding, cause less metabolic
flux and generally produce greater forces than concentric or isometric contractions
(31, 32). This lengthening can place the muscle fiber under active strain over the
descending limb of the length-tension curve (43, 46), resulting in mechanical
disruption of the actin-myosin bonds, cytoskeletal damage, and a prolonged
reduction in voluntary force evident in studies of both animals (24) and humans
2 A version of this chapter has been published via the American Physiological Society.
Power GA, Dalton BH, Rice CL, Vandervoort AA. Delayed recovery of velocity-dependent power
loss following eccentric actions of the ankle dorsiflexors. J Appl Physiol 109: 669-676, 2010.
47
(50). Impaired torque production following eccentric exercise can be attributed to
impaired calcium release as a result of damage induced dysfunction to structural
components involved in E-C coupling (2, 59). As well, the increase in series
compliance due to overstretched sarcomeres, leads to a shift to longer muscle
lengths for optimal torque production (27) resulting in impaired torque production
at the original muscle length.
The ability of a muscle to generate peak power is dependent on its maximum
shortening velocity at a given load. Many factors contribute to maximum shortening
velocity in an intact muscle, such as; rate of motor unit recruitment (58), muscle
architecture (7) and fiber composition (28) (see Gordon (26) for review). Type II
fibers generally produce ~4x greater power than Type I fibers. Additionally, it has
been suggested that Type II muscle fibers are more susceptible to muscle damage
than Type I (36), and damage may be more closely related to sarcomere length
during contraction (12). Thus, the differences in fatigability following an eccentric
fatigue task may depend upon the muscle group and type of contraction performed.
Neuromuscular fatigue, defined as any exercise-induced reduction in the
generation of torque or power, can be manifested through both central or
peripheral factors (22) and its analysis is further complicated by many influences
such as species, sex and muscle fiber type differences whose interactive effect will
depend on the type of contraction task utilized, muscle group involved and
incidence of muscle damage (2, 6, 11, 12, 18, 19, 24, 34). The fatigue response to
dynamic shortening contractions is similar between sexes (17, 54). However, in
limited studies following eccentric fatiguing contractions women had greater
48
isometric strength loss compared with men (53, 55). Thus it is unknown whether
isotonic power will be impaired differently between the sexes.
One limitation of previous studies is only using a measure of isometric torque
(MVC) to assess fatigue following eccentric contractions, but because of task-
specificity, MVCs may underestimate the functional deficit in muscle performance
(49). Power, the product of both torque and velocity, may serve to exploit different
mechanisms of fatigue to a greater extent than isometric torque. However, only
isokinetic power has been reported following eccentric contractions (23, 44, 47)
with modest reductions. Isokinetic measures are limited by a constant velocity with
varying resistance which therefore cannot assess fatigue-induced alterations in
shortening velocity following a task or exercise.
A less common method used to calculate power, but functionally relevant,
are velocity-dependent contractions, in which the load is held constant and velocity
varies throughout the range of motion and over time (15). Unlike impairments in
force production capacity, the contributions of fatigue-related declines in shortening
velocity to the reduction in power following eccentric exercise are unknown.
Indeed, shortening velocity is known to recover fairly rapidly (< 5 min) after
isometric and concentric contractions (15, 16), but repeated eccentric contractions
result in disintegration and streaming of the Z-disks, disorganized myofilaments,
and hypercontracted and overstretched sarcomeres (40), which could impair cross-
bridge cycling, and hence, affect, to a greater extent, the production of shortening
velocity.
49
Because of the lower metabolic cost of lengthening contractions, but greater muscle
damage compared with isometric or shortening contractions, it remains unclear
whether velocity-dependent power loss is lesser than, greater than, or similar to
repeated isometric or concentric contraction tasks (16). Therefore, the purpose
here was to investigate the effect of high-intensity eccentric contractions on
neuromuscular function and velocity-dependent power in young men and women.
We hypothesized there will be a modest reduction in shortening velocity resulting in
velocity-dependent power loss which will remain reduced throughout recovery. A
secondary purpose of the study was to explore further the equivocal observations in
the literature about differences between the sexes in muscle fatigue and responses
to eccentric exercise.
3.1 Methods
3.1.1 Participants: Ten young men (25.6 ± 2.9 y) and eleven young women
(26.0 ± 1.7 y) from the university population volunteered for the study. The mean
height and mass of the men and women were: 176.4 ± 6.8 cm and 76.8 ± 7.7 kg; and
164.8 ± 5.9 cm and 59.2 ± 10.1 kg, respectively. The study protocol was approved
by the local University’s Review Board for Health Sciences Research Involving
Human Subjects and conformed to the Declaration of Helsinki. Informed, oral and
written consent was obtained prior to testing.
Participants visited the laboratory on 2 occasions separated by seven days.
All participants were recreationally active with no known neurological or
50
cardiovascular diseases. The first session was familiarization to the testing
procedures, and the second during which data were collected. Participants were
asked to refrain from strenuous exercise one day prior to testing and to not
consume caffeine on the day of testing.
3.1.2 Experimental set-up: A Biodex multi-joint dynamometer (System 3,
Biodex Medical Systems, Shirley, New York) was used for testing and calibration
was verified according to Biodex System 3 guidelines. A footplate was attached to
the dynamometer and positioned at an angle of approximately 45o to the floor. The
right foot was strapped tightly to the footplate with the lateral malleolus in line with
the rotational axis of the dynamometer. Extraneous body movements were
minimized using non-elastic shoulder, waist and thigh straps. Participants sat in a
slightly reclined position with hip, knee, and ankle angles at ~110o, ~140o, and ~30o
plantar flexion, respectively. All isometric dorsiflexion contractions were
performed at 30o of plantar flexion. Concentric contractions began from the plantar
flexed position of 30o and ended at the neutral ankle angle (0o). The eccentric
contractions started at the neutral ankle angle and ended at 30o plantar flexion, thus
moving through a 30o range of motion. The dynamic contractions were performed
in the isotonic mode of the Biodex, thus allowing velocity to vary while providing
inertia-free constant torque. In the isotonic mode, participants had to overcome the
pre-programmed torque before the footplate would move during the concentric
movements. Increases in applied torque were absorbed by the dynamometer and
returned as a directly proportional increase in velocity (51). The isotonic mode is
not by the proper definition strictly isotonic. The important point is that the load
51
(resistance) is essentially constant and velocity of movement can vary freely. This is
useful when exploring the effect of velocity changes on movement and power.
Therefore, throughout this paper we will refer to these contractions as velocity-
dependent.
Surface electromyography (EMG) was collected from the tibialis anterior and
soleus muscles using self-adhering Ag-AgCl electrodes (1.5 X 1cm; Kendall,
Mansfield, MA). The skin was rubbed vigorously with alcohol prior to the
application of the electrodes. A monopolar electrode set up was used with an active
electrode positioned on the proximal portion of the tibialis anterior over the
innervation zone (~7 cm distal to the tibial tuberosity and ~2 cm lateral to the tibial
anterior border) and a reference placed over the distal tendinous portion of the
tibialis anterior at the ankle. For the soleus the active electrode was positioned ~2
cm distal to the medial head of the gastrocnemius and a reference placed over the
calcaneal tendon.
A computer-triggered stimulator (model DS7A, Digitimer. Welwyn Garden
City, Hertfordshire, UK) provided the electrical stimulation of the dorsiflexors using
a pulse width of 100 µs, 400 V, and current ranging from 20-95 mA. Contractions of
the tibialis anterior were electrically evoked using a bar electrode held distal to the
fibular head over the deep branch of the common peroneal nerve. Through
palpation and careful observation we were confident there was no activation of the
peroneal or plantar flexor muscles during the electrically evoked contractions.
3.1.3 Experimental procedures: Peak twitch torque (Pt) was determined by
increasing the amplitude of the current until a plateau in M-wave amplitude was
52
reached (30-95 mA), followed by a further 10-15% increase in current to ensure
supramaximal stimulation. This stimulation intensity was the same o ne used for
doublet stimulation (two pulses at 10 ms interpulse interval) to assess voluntary
activation. Next, 100 Hz peak torque (P100) was determined by increasing the
current until there was a plateau in P100 (20-65 mA). A torque-frequency
relationship was constructed using 1 s trains of the following frequencies: 1, 5, 10,
20, 30, 40, 50, and 100 Hz. Frequencies were delivered, in random order, at the
current found to evoke P100 with 1 s between trains.
Then, 3 MVCs were performed of 3-5 s duration. Three minutes of rest was
given between all contractions. Participants were provided visual feedback of the
torque via near real time display, and verbally exhorted during all voluntary
contractions. Voluntary activation was assessed during all MVCs us ing the modified
interpolated twitch technique (29). The amplitude of the interpolated torque
evoked during the MVC was compared with a resting twitch doublet torque evoked
~1 s following the MVC. Percent voluntary activation was calculated as voluntary
activation (%) = [1- (interpolated twitch doublet/resting twitch doublet)] x 100.
Values from the peak MVC were used for data analysis. Once MVC torque was
determined, the dynamometer was switched from the isometric to isotonic mode. A
load equal to 20% MVC was programmed into the Biodex and participants were
instructed to perform practice concentric contractions (3-5 contractions) as fast as
possible. The 20% MVC load represents a moderate resistance for dynamic
contractions that all subjects could endure when it is important to have fast
shortening contractions performed throughout the range of motion following a
53
fatiguing protocol. For example, at a load of approximately 60% of MVC many
subjects cannot perform one concentric contraction through a full range of motion
and the speed of movement is very slow. The Biodex was programmed such that the
footplate was automatically returned to 30o of plantar flexion at the end of each
concentric voluntary contraction. Following practice, two contractions wer e
performed to establish values for peak shortening velocity at baseline.
3.1.4 Fatigue and recovery protocol: Participants performed 5 sets of 30
eccentric dorsiflexion contractions separated by 30 s, and performed with a load set
at 80% MVC. Pilot testing showed 80% to be a compromise between very rapid
fatigue but a sufficient contraction intensity to permit several contraction cycles to
occur before achieving task failure. Participants were provided with visual feedback
of velocity and instructed to resist while lowering the foot plate through the 30o
range of motion over a 1 s period. The foot was then returned to the neutral ankle
position by the investigator over a period of 2 s. The voluntary and electrically
evoked responses of the dorsiflexors were recorded at: baseline, during the fatigue
protocol, immediately following each of the 5 sets, and throughout the recovery
period at 0.5 min, 2 min, 5 min, 10 min, 15 min, 20 min, and 30 min (Figure 7).
Measures following the fatigue protocol included, and were performed in the
following order: (1) maximum evoked twitch properties, (2) assessment of MVC and
voluntary activation, (3) post-activation twitch and twitch doublet, (4) A measure of
low frequency torque depression (10:50 Hz ratio), and (5) velocity-dependent
concentric power.
54
Figure 7. Schematic diagram of experimental protocol.
Grey bars are isometric maximum voluntary contractions (MVC). Open profiles are
electrically evoked contractions (twitches (small triangles), doublet (large
triangles), 10 Hz and 50 Hz (bars)). Filled profiles are dynamic contractions;
concentric at 20% MVC (triangles), and dynamic eccentric contractions at 80% MVC
(rectangles). Open arrows are electrically evoked twitches; and filled arrows are
electrically evoked doublets. Recovery time points: Post (task termination), and at
0.5, 2, 5, 10, 15, 20, and 30 minutes.
55
3.1.5 Data reduction and analysis: Torque, position and velocity data were
sampled at a rate of 100 Hz. All data were converted to digital format using a 12-bit
analog-to-digital converter (model 1401 Power, Cambridge Electronic Design,
Cambridge, UK). Surface EMG signals were pre-amplified (x100), amplified (x2) and
band-pass filtered (10-1,000 Hz), and sampled online at 2500 Hz using Spike 2
software (version 6.10, Cambridge Electronic Design Ltd.). Surface EMG from the
MVC was root mean squared (RMS) and values were used from a 1 s time period
about the peak torque. All subsequent MVC RMS values were normalized to the
level obtained during baseline. EMG was collected during the fatigue protocol from
contractions 1-5, 13-17 and 25-30 of each set and averaged for each set. Peak RMS
values of the raw surface EMG was calculated during the lowering phase through the
30o range of motion and then normalized to the M-wave. Post-activation
potentiation was calculated by comparing the twitch following the MVC to the
baseline twitch. Power was calculated as the product of torque (N·m) and the peak
shortening velocity (rad/s) of the fastest contraction attempt. Spike 2 software was
used off line to determine M-wave amplitude, area, duration, the peak twitch torque
(Pt), peak doublet torque (Dt), doublet time to peak twitch (DTPT), half relaxation
time (DHRT) of the doublet, contraction duration (CD=DTPT+DHRT), doublet rate of
torque development, and doublet maximum rate of relaxation. Low frequency
torque depression was calculated using a ratio of peak 10 to peak 50 Hz evoked
torques (10:50 Hz). To account for expected strength differences, all measures were
normalized to baseline and presented as a percent change.
56
3.1.6 Statistical analysis: Using SPSS software (version 16, SPSS Inc. Chicago,
IL) a two-way (sex x time) repeated measures analysis of variance was used to
assess all neuromuscular data over time. Because voluntary activation values are
not normally distributed, a Mann-Whitney U-test was employed to test for
significance between groups. An unpaired t-test was used to assess group
differences for subject characteristics. The level of significance was set at p <0.05.
When a significant main effect or interaction was present, Tukey’s HSD post hoc test
was performed to identify where significant differences existed. Tables are
presented as mean ± standard deviation (SD), and figures as mean ± standard error
(SE).
3.2 Results
3.2.1 Baseline measures: As expected, due to differences in anthropometrics,
men had higher values for absolute measures of: peak twitch torque, MVC torque,
velocity and power than women, ~ 49%, 30%, 16% and 38%, respectively (Table 2).
When absolute values were compared, men were stronger than women (p < 0.05) at
every stimulation frequency, but when the torque frequency curves (Figure 8) were
normalized to 100 Hz torque there were no differences in the relationship between
men and women (p > 0.05). Evoked torque corresponded to approximately 62%
and 50% of MVC torque for the 50 Hz, and 64% and 52% of MVC torque for the 100
Hz, for the men and women, respectively.
57
Table 2. Baseline contractile data.
Women had lower absolute evoked peak twitch torque, maximal voluntary
isometric contraction (MVC) torque, maximum shortening velocity, and peak power
than men (*p < 0.05). Voluntary activation (VA) was not significantly different (p >
0.05) between groups. Time to peak twitch (TPT), half relaxation time (HRT) and
contraction duration (CD) of the twitch were not significantly different (p > 0.05)
between groups. Mean ± SD.
58
Figure 8. Torque-Frequency relationship.
Open triangle (men absolute torque), filled triangle (men relative torque), Open
circle (women absolute torque), and filled circle (women relative torque). Men had
higher absolute torques at all frequencies (1-100 Hz) compared to women (*p <
0.05). Relative torques were similar at all stimulation frequencies (* p > 0.05).
59
3.2.2 Fatigue and recovery measures: All participants were capable of
completing the 5 sets of 30 eccentric contractions, although some subjects had
difficulty lowering the foot plate at a constant velocity for the last few contractions
of each set. This failure to maintain a constant velocity resulted in increased
eccentric velocities which ranged from 37o/s to 41o/s. Despite the variation in
velocity, the duty cycles were similar (p > 0.05) between men and women (0.32 ±
0.04).
When all neuromuscular measures were analyzed with regard to relative
changes over time, no significant differences between men and women were found
(p > 0.05). Thus, data were pooled and normalized to baseline for all subsequent
analyses. Peak dorsiflexor MVC torque decreased to 85% of baseline (p < 0.05),
following the first set of 30 eccentric contractions (Figure 9). The MVC torque
progressively decreased following each successive set to 72% of baseline
immediately following task termination and did not recover fully. There were no
significant changes from baseline (p > 0.05) in RMS EMG of the agonist TA during
MVCs, and voluntary activation was greater than 99% at baseline and did not
change (p > 0.05; Figure 10) throughout fatigue and recovery. Conversely, soleus
RMS EMG during MVCs increased (p < 0.05) to 111 ± 21% of baseline following the
third set of eccentric contractions, resulting in a 13 ± 9% increase in the ratio of
antagonist coactivation where it remained for up to 20 min recovery, but returned
to baseline by 30 min. M-wave properties, including; peak-to-peak amplitude,
duration, and area remained unchanged from baseline (p > 0.05). During the
60
eccentric contractions, RMS EMG of the agonist TA normalized to M-wave did not
differ significantly (p > 0.05) among sets.
Figure 9. Maximum isometric voluntary contraction (MVC).
Maximal voluntary strength was reduced following the first set (S1) of eccentric
contractions and continued to decline to ~70% of baseline at Post (task
termination) and it did not recover fully (*p < 0.05) within 30 min. [S represents
‘sets’, R represents ‘recovery’]. Mean ± SE.
61
Figure 10. Torque output and activation for a representative subject at 30min of
recovery.
The vertical bar on the torque tracing represents the evoked doublet. Open arrows
indicate electrically evoked twitches; and filled arrows indicate electrically evoked
doublets. Maximal voluntary isometric contraction (MVC) torque
62
Twitch potentiation increased to 130 ± 16% from baseline following the first
set of 30 contractions and 140 ± 28% of baseline immediately following task
termination (p < 0.05), gradually diminishing to the baseline value at 2 min. Once
the potentiating effects of the fatigue protocol were mitigated, twitch torque was
reduced to 79 ± 24% of baseline at 2 min recovery (p < 0.05) and continued to
decrease to 65 ± 18% of baseline by 30 min of recovery. Twitch doublet torque
decreased (p < 0.05) to 83 ± 15% of baseline following the third set of contractions
and was further reduced to 63 ± 11% of baseline by 30 min. Twitch doublet
contractile properties parameters including DTPT, DHRT, CD, maximum rate of
relaxation and rate of torque development did not differ significantly from baseline
at any time point during fatigue and recovery (p > 0.05). Peak torque of the 10 Hz
was 13.9 ± 5.7 N·m at baseline and was reduced to 64 ± 24% of baseline
immediately following the eccentric exercise (p < 0.05), and did not recover fully. As
well, peak torque of the 50 Hz (Baseline; 24.0 ± 10.2 N·m) was reduced only to 85 ±
16% of baseline following the second set of eccentric contractions (p < 0.05) and to
79 ± 15% of baseline immediately following task termination, and did not recover
fully. The change in the 10:50 Hz ratio was manifested by the greater reduction in
10 Hz evoked torque compared with the 50 Hz. The 10:50 Hz ratio decreased to
28% of baseline immediately following task termination and continued to decrease
to 47% of baseline (p < 0.05) at 10 min of recovery (Figure 11) and remained
reduced. This indicated there was significant low frequency torque depression
following the last set of eccentric contractions.
63
Figure 11. Low-Frequency torque depression (10:50 Hz).
A significant increase in low frequency torque depression as shown by the
decreased 10:50Hz ratio was present at Post (task termination), with a continued
decrease in 10:50 Hz until 10 min and remained depressed for 30 min (*p < 0.05). [
S represents ‘sets’, R represents ‘recovery’]. Mean ± SE.
64
Figure 12. Velocity-dependent power
Velocity-dependent concentric power was reduced by 8% at Post (task termination)
compared with baseline and did not recover fully within 30 minutes (*p < 0.05).
Mean ± SE.
65
All participants were capable of completing the 30o range of motion during
baseline measures and following the eccentric fatigue protocol for all velocity-
dependent shortening contractions. Absolute values for baseline velocity and
power measures are presented in Table 2. Maximum shortening velocity and
subsequently velocity-dependent power were reduced to 92% of baseline
immediately following the fatigue protocol (p < 0.05; Figure 12) and neither
recovered fully.
3.3 Discussion
We tested the hypotheses that following a bout of high-intensity eccentric
contractions of the ankle dorsiflexors, there would be a modest reduction in
shortening velocity resulting in velocity-dependent power loss, which would remain
reduced throughout recovery. The main findings indicate velocity-dependent
power loss occurred immediately following the eccentric exercise, and did not
recover fully. Furthermore, despite baseline differences the fatigue and recovery
profiles were not different between men and women. These results indicate
following a bout of eccentric muscle contractions there is a reduction in velocity-
dependent power driven by impairment in maximum shortening velocity.
When normalized to pre-fatigue values, there was no sex-related difference
for fatigue and recovery. This is an interesting finding because studies on animals
support a sex-related difference in fatigability following eccentric exercise (5, 57).
However, equivocal results are found in humans (8, 11, 33, 52, 53, 55). The
normalized torque-frequency curves (Figure 8), and twitch contractile speeds (time
66
to peak twitch, half-relaxation time and contraction duration) (Table 2), were not
different between the men and women. Thus, both groups may have similar muscle
properties (i.e., architecture and fiber type composition) of the ankle dorsiflexors
which would lead to a comparable fatigue response. In turn, these findings
corroborate reports that suggest human single fiber shortening velocity is similar
between sexes (38).
Voluntary ankle dorsiflexor strength was reduced by 28% following
eccentric exercise and did not recover fully. Evidently, the mechanisms of fatigue in
this study originate peripherally as voluntary activation (>99%) and RMS EMG of
the agonist tibialis anterior did not change throughout the entire protocol, which is
similar to previous reports on the ankle dorsiflexors (9, 48). However, this is not
always the case when other muscles are investigated, for example voluntary
activation of the elbow flexors has been shown to decrease by ~11-22% following
eccentric exercise (25, 40). Thus, the ability to fully activate the dorsiflexors, even
when the muscle is stressed severely or in this case undergone damaging
lengthening contractions is unique.
A recent investigation (30) found muscle fiber conduction velocity in the
quadriceps was decreased following eccentric exercise due to sarcolemmal damage.
However, excitation failure of the sarcolemma cannot account for the torque and
power depression in the ankle dorsiflexors, as similar to o ther reports (48), M-wave
properties (area, duration, amplitude) did not change during and following task
termination. This was further corroborated with the findings from the electrically
evoked contractions. For example, peak twitch torque declined by 21% 2 min
67
following task termination. Concomitantly, twitch potentiation, which could offset
the initial fatigue response in peak twitch torque, was no longer measurable at that
time and peak twitch torque remained depressed. Similarly, the 10 Hz and 50 Hz
evoked torques were reduced following the eccentric exercise and did not recover
fully. As previously observed (9, 48) following eccentric exercise of the ankle
dorsiflexors, the contractile speeds (time to peak twitch, half-relaxation time and
contraction duration) of the evoked twitch doublet did not change. Because
eccentric muscle actions are less metabolically demanding than other contraction
types (1, 10) metabolic accumulation and alterations to blood chemistry may not
have been responsible for the impairment in torque production (3). Subsequently,
mechanical disruption of the link between the t-tubule and the sarcoplasmic
reticulum lead to excitation-contraction (E-C) uncoupling, which remains as the
likely peripheral impairment responsible for the immediate torque and power loss
(2, 35, 59). The most plausible stage of E-C coupling which was impaired following
the eccentric exercise was the release of calcium from the sarcoplasmic reticulum
(39), evident by the decrease in electrically evoked torque at low-frequency
stimulation. In addition to impaired calcium release, muscle damage or some
structural impairment to the contractile machinery likely occurred, which is
represented by the decrease and incomplete recovery of the 10:50 Hz ratio, and
MVC. The 10:50 Hz ratio decreased immediately following eccentric exercise and
continued to decrease into recovery, but at 10 min it stabilized at ~50% of baseline
throughout the remainder of recovery. The change in the 10:50 Hz ratio was
manifested by the greater reduction in 10 Hz than 50 Hz evoked torque. This
68
further supports an impairment in E-C coupling leading to low frequency torque
depression (21). Ultimately, this finding was a result of the primary insult of
eccentric exercise and not due to secondary effects of muscle damage which
typically occur 1-2 hr after the initial injury (56).
The incomplete recovery of MVC torque following the eccentric exercise
suggests strongly that damage to muscle fibers had occurred (6). Prolonged torque
loss following unaccustomed eccentric exercise is often considered to be a reliable
indirect marker of muscle damage (19, 40, 60). Although MVC torque is less
impaired immediately following high-intensity eccentric actions than concentric or
isometric exercise (37, 41, 48), when reassessed day(s) later, voluntary isometric
torque loss following concentric contractions recovers, whereas following eccentric
contractions torque loss is still present (53). Incomplete recovery of both voluntary
and evoked torque cannot be attributed to metabolic fatigue. Thus, muscle damage
and the subsequent impairment of the contractile machinery may have been
responsible for the prolonged torque loss in the present study.
Velocity-dependent power, calculated here as the product of 20% MVC
torque and maximum angular velocity of the contraction, was reduced by 8%
following eccentric exercise and did not recover fully. These observations are unlike
previous reports which used shortening velocity as the criterion measure of fatigue
following contractions of the ankle dorsiflexors, and other muscles (14, 15) in which
velocity-dependent power recovered within ~5 min following concentric
contractions. For example, Cheng & Rice (16) fatigued the dorsiflexors to 50% of
peak shortening velocity, but velocity recovered within 5 min. In the present study,
69
velocity-dependent power was reduced by 8%, but did not recover within 30 min.
Mechanisms of impaired neuromuscular functioning differ between fatigue and
damage, and can be distinguished by the time course of recovery. Thus, the
reduction and prolonged recovery of power following eccentric fatigue may result
from different mechanisms than during a concentric fatigue task (discussed below).
Although MVC torque yields valuable insight regarding the contractile state
of the muscle, it assesses only a single aspect of muscle performance. The unique
study design employed here involved testing participants using the isotonic mode of
the Biodex to evaluate eccentric fatigue-induced reductions in shortening velocity
which would remain masked when tested isokinetically. We observed a significant
decrease of 8% and 28% in velocity-dependent power and MVC following the
eccentric fatigue task, compared with baseline, respectively. Despite a 3.5 fold
greater loss of torque production capacity (MVC) over shortening velocity, it would
seem MVC is more sensitive to perturbations to the system following eccentric
exercise. Because power was calculated at 20% MVC the observed loss of torque
production capacity may only contribute minimally to the loss of power, as peak
shortening velocity was reached not at the onset of movement but rather
throughout the range of motion (~15o plantar flexion). Hence, the torque developed
to overcome the resistance was not as critical in determining peak power as the
speed of shortening.
A metabolic explanation (20, 61) may account for the initial decrease in
shortening velocity, where excessive ADP surrounding the contractile proteins actin
and myosin result in slower cross-bridge cycling. However, due to the time
70
sensitive nature of metabolic perturbations this slowing does not account for the
incomplete recovery of shortening velocity and, hence, power. The delayed
recovery of power, as seen here is most likely due to damage induced EC
uncoupling, resulting in reduced calcium release (4, 35), and damage to the
contractile machinery imposed by the lengthening contractions. Increased
sarcomere instability following eccentric exercise leads to a reduction in the
number of functional sarcomeres in series, hence the number of ‘force generators’
are reduced (45, 46) resulting in a reduced shortening velocity, as well, a change in
optimal muscle length for torque production to longer lengths (13, 42, 49). Thus,
structural impairments in EC coupling and the contractile machinery imposed via
the eccentric actions is responsible for power loss and reduced recovery following
eccentric exercise.
Although the current study cannot determine the specific mechanisms of
reduced power, we found significant E-C coupling perturbations as evidenced by the
presence of low frequency torque depression. The damaging eccentric contractions
impaired shortening velocity and reduced power for up to 30 min following task
termination. In summary, when velocity-dependent contractions are used as the
criterion measure to calculate power, we demonstrated that following eccentric
exercise maximal shortening velocity was reduced, which contributed to the
observed reduction in power. Further research on velocity-dependent contractions
is warranted, as it relates to human movement where the load is fixed and velocity
is variable.
71
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uncoupling: major role in contraction-induced muscle injury. Exerc Sport Sci Rev 29:
82-87, 2001.
60. Warren GL, Lowe DA, and Armstrong RB. Measurement tools used in the
study of eccentric contraction-induced injury. Sports Med 27: 43-59, 1999.
61. Westerblad H, Dahlstedt AJ, and Lannergren J. Mechanisms underlying
reduced maximum shortening velocity during fatigue of intact, single fibres of
mouse muscle. J Physiol 510 ( Pt 1): 269-277, 1998.
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Chapter 4 – Power loss is greater following lengthening contractions in
old versus young women 3
4.0 Introduction
Research on age-related muscle fatigue has focused primarily on isometric
and shortening contractions. Far less is known in older adults regarding
neuromuscular function and short-term recovery following repeated high-intensity
lengthening contractions which can provoke long lasting impairments in
neuromuscular performance (11, 49). Furthermore, we are interested in the
velocity component (i.e., voluntary shortening velocity) of power, following
lengthening contractions. This contraction mode in which the load is fixed and
velocity of movement is unconstrained allows for alterations in shortening velocity
to be elucidated which in older adults already is impaired and is a strong indicator
of age-related muscle fatigability (22, 41, 47, 56).
By the eighth decade of life, the senescent adult has undergone alterations to
both the structure and function of the neuromuscular system that lead to impaired
muscle performance (17, 44, 57). These alterations include: muscle atrophy
(preferentially Type II muscle fibers), and the death and remodeling of motor units
(MUs) resulting in a greater relative composition of slow type muscle fibers (57),
and architectural changes to the muscle and musculotendinous unit (44).
3 A version of this chapter has been published. Used with permission from Springer.
Power GA, Dalton BH, Rice CL, Vande rvoort AA. Power loss is greater following lengthening
contractions in old versus young women. Age 34: 737-750, 2012.
77
Additionally, neural changes can include greater antagonist coactivation (34) and
lower maximal MU discharge rates (21). The combined consequence of these
structural and neural age-related manifestations are a slowing of intrinsic muscle
contractile properties (59), lower rates of torque development and reduced cross-
bridge kinetics (1). Hence, older adults exhibit impairments in maximal voluntary
shortening velocity, torque production and especially muscle power (41). Despite
the negative implications of age-related changes to the neuromuscular system, there
is a relative preservation of eccentric strength (31, 48, 58). Although older adults
can experience similar (18), less (38), or more (24) muscle damage than young
adults, it is unknown whether maintained eccentric strength is an advantageous
mechanism with which to maintain effective neuromuscular performance during
and following a bout of repeated lengthening contractions.
It seems well established that older adults are more fatigue resistant than
young adults during isometric tasks (33), yet the fatigue response during and
following dynamic shortening contractions is equivocal and depends upon the task.
Older adults can experience less (37, 53), similar (12, 35), or more (8, 40, 47) fatigue
than young. However, tasks which are performed with an unconstrained velocity
component (i.e., velocity-dependent) always yield a greater fatigue response in
older adults than young (22, 40, 47). Moreover, the effects of repeated lengthening
contractions on age-related muscle fatigue are less well understood. The only study
investigating age-related fatigability following lengthening contractions (8),
reported that the reduction in maximum voluntary isometric contraction (MVC)
torque did not differ between old and young adults during or following repeated
78
isokinetic (60o/s) lengthening contractions, but isokinetic torque loss during the
lengthening contractions was greater in older adults than the young. However,
power was not assessed following the protocol, and thus it is unknown whether
repetitive lengthening contractions affect concentric power differently in old and
young adults, and which component of power (torque or shortening velocity) is
more compromised.
Voluntary maximal loaded shortening velocity is known to recover rapidly (<
5 min) in young adults after voluntary isometric and concentric fatigue tasks (14,
15). However, repeated lengthening contractions result in muscle damage which
can take multiple days to recover fully (19, 51), and it is unclear how this damage
may affect velocity-dependent power during short-term recovery in older adults.
Impaired isometric torque production following lengthening contractions can be
attributed to a mechanical disruption of the link between the t-tubule and the
sarcoplasmic reticulum impairing calcium (Ca2+) release (32, 60), and also, to the
redistribution of sarcomere lengths [see popping sarcomere hypothesis (43)],
resulting in a length-tension relationship shift to longer muscle lengths for optimal
torque production. As well, dynamic performance following multi-joint lengthening
contractions is known to be impaired (11, 55) although the mechanisms are not
entirely understood. Recently, we (49) reported that MVC torque and velocity-
dependent power did not recover fully up to 30 min following 150 lengthening
contractions in healthy young men and women. Although lengthening contractions
are less energetically demanding than isometric and dynamic shortening
contractions (2, 54), they are known to induce muscle fatigue (8, 16, 42, 45).
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Because excitation-contraction (E-C) coupling is compromised in older adults (46)
and maximal unconstrained shortening velocity is indeed slower (22, 41, 47)
compared with young adults, the old may be energetically disadvantaged during this
task. Thus, older adults may experience a greater perturbation in ATP homeostasis,
consequently exacerbating their fatigue response (33) and resulting in a greater
reduction in shortening velocity and subsequent velocity-dependent power than
young adults.
Therefore, the purpose here was to investigate the effect of repeated high-
intensity lengthening contractions on neuromuscular function in old and young
women with a particular emphasis on the short-term recovery of velocity-
dependent power. As a result of similar muscle damage, MVC torque will be
reduced similarly in both old and young women and remain reduced throughout a
30 min recovery period. However, when tested under dynamic conditions (velocity-
dependent shortening), we hypothesize that the older women will have a larger
reduction in velocity-dependent power than the young owing to a greater
impairment in shortening velocity and impairments in E-C coupling, which are
known to be compromised in older adults and may not be observable during
isometric testing. As a result of muscle damage neither group will recover by 30
min.
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4.1 Methods
4.1.1 Participants: Nine old (68.3 ± 6.1 y) and nine young women (25.1 ± 1.3
y) from the university population and local community groups, who were free from
musculoskeletal disorders which would impair their ability to perform the task,
volunteered for this study. All participants were recreationally active. The mean
height and mass of the old and young women were: 162.0 ± 7.3 cm and 67.7 ± 8.5 kg,
and 167.1 ± 7.0 cm and 63.7 ± 10.4 kg, respectively. All participants were asked to
refrain from strenuous exercise one day prior to testing and to not consume caffeine
on the testing day. This study was approved by the local University’s Review Board
for Health Sciences Research Involving Human Subjects and conformed to the
Declaration of Helsinki. Informed, oral and written consent was obtained from all
participants prior to testing.
4.1.2 Experimental arrangement: All testing was conducted on a Biodex
multi-joint dynamometer (System 3, Biodex Medical Systems, Shirley, New York).
For a detailed explanation and experimental timeline of the testing set-up and
procedures please refer to (49). The right foot was strapped tightly to the Biodex
ankle attachment footplate, aligning the lateral malleolus with the rotational axis of
the dynamometer. Extraneous movements were minimized using non -elastic
shoulder, waist and thigh straps. Participants sat in a slightly reclined position with
the hip, knee, and ankle angles set at ~110o, ~140o, and ~30o plantar flexion,
respectively. All voluntary and evoked isometric dorsiflexion contractions were
performed at an ankle joint angle of 30o of plantar flexion. Shortening contractions
began from the plantar flexed position of 30o and ended at the neutral ankle angle
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(0o). The lengthening contractions commenced at the neutral ankle angle (0o) and
ended at 30o plantar flexion, thus both dynamic actions moved through a 30o range
of motion. All dynamic contractions were performed using the isotonic mode of the
Biodex. However, due to inherent mechanical limitations of the dynamometer
(unable to maintain an exact constant external load throughout an entire range of
motion), these contractions are not purely isotonic and neither are they iso-inertial
as the load is fixed (mechanically) and not influenced by gravity but rather the
braking of the dynamometer. And therefore, we refer to these contractions as
“velocity-dependent”. A velocity-dependent movement is characterized by a
participant producing a dynamic contraction as fast as possible in which the angular
velocity is unconstrained while the load or resistance is fixed at a pre-determined
value (i.e., 20%MVC).
Surface electromyography (EMG) was collected from the tibialis anterior and
soleus muscles using self-adhering Ag-AgCl electrodes (1.5 X 1 cm; Kendall,
Mansfield, MA). The skin was cleaned forcefully with an alcohol swab prior to the
application of the electrodes. A monopolar electrode configuration was used with
the active electrode positioned on the proximal portion of the tibialis anterior over
the innervation zone (~7 cm distal to the tibial tuberosity and ~2 cm lateral to the
tibial anterior border) and a reference electrode was placed over the distal
tendinous portion of the tibialis anterior at the malleoli. The active electrode for the
soleus was positioned ~2 cm distal to the lower border of the medial head of the
gastrocnemius and a reference was placed over the calcaneal tendon.
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Stimulated contractions of the dorsiflexors were evoked electrically using a
bar electrode held distal to the fibular head over the deep branch of the common
peroneal nerve. A computer-triggered stimulator (model DS7AH, Digitimer,
Welwyn Garden City, Hertfordshire, UK) set at 400 V provided the electrical
stimulation using a pulse width of 50-100 µs.
4.1.3 Experimental procedures: Peak twitch torque (Pt) was determined by
increasing the current until a plateau in dorsiflexor Pt and tibialis anterior M-wave
amplitude were reached, and then the current was further increased by 10-15% to
ensure activation of all motoneurons via supramaximal stimulation. This
stimulation intensity was used for the evoked doublet (Pd) (2 pulses at a 10 ms
interpulse interval), and to assess voluntary activation. Next, a 1 s train at 50 Hz
was delivered to assess peak tetanic torque by increasing the current until there
was a plateau in evoked torque. This was tolerated by all young women and 4 of the
older women.
Three isometric MVCs were then performed; each of 3-5 s duration. Three
min of rest was given between all contractions. To ensure MVC attempts were
maximal, participants were provided visual feedback of the torque tracing on a
computer monitor, and exhorted verbally during all voluntary efforts and voluntary
activation was assessed using the modified interpolated twitch technique (26). The
amplitude of the interpolated torque evoked during the peak plateau of the MVC
was compared with a resting Pd evoked ~1 s following the MVC when the muscles
were relaxed fully. Percent voluntary activation was calculated as voluntary
activation (%) = [1- interpolated Pd /resting Pd] x 100. Values from the MVC with
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the highest peak torque were used for data analysis. Next, 10 pulses and 50 pulses
were delivered over a 1 s period to determine a 10 Hz to 50 Hz relationship in all 9
young and 4 old participants using the current required to evoke peak 50 Hz torque.
Once MVC torque was determined, the dynamometer was switched from the
isometric to isotonic mode and a load equal to 20% MVC was programmed to allow
for determination of maximal shortening velocity with this load, and velocity-
dependent power. The 20% MVC resistance was chosen because it represents a
moderate load for the fast shortening contractions, and one that all subjects could
perform through the entire range of motion even after a bout of repeated high-
intensity lengthening contractions. Before the footplate moved during the velocity-
dependent shortening contractions, participants had to overcome the pre-
programmed resistance. The dynamometer absorbs this increase in applied torque
resulting in a directly proportional increase in angular velocity. This is a helpful
feature to explore the effect of damaging lengthening contractions on alterations in
velocity of unconstrained movement and power. The dynamometer was
programmed to allow the footplate to return to 30o of plantar flexion at the end of
each shortening voluntary contraction while the participant relaxed fully.
Familiarization with these ‘fast’ shortening contractions involved participants
performing several (typically 5) velocity-dependent shortening contractions until a
stable value was obtained (no change in maximal shortening velocity). To ensure a
maximal effort (peak velocity) contraction, all participants were instructed to move
the load “as hard and as fast as possible throughout the entire range of motion”. To
assist participants in reaching their maximal shortening velocity, visual feedback of
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the velocity profile was provided via a computer monitor, and a horizontal cursor
was positioned at the previous plateau in peak velocity. Participants rested for 3
min and then performed 2 consecutive contractions which were used to establish
baseline values for maximum shortening velocity and peak power.
4.1.4 Fatigue and recovery protocol: With a load of 80% MVC, participants
performed 5 sets of 30 eccentric dorsiflexion contractions with each set separated
by 30 s of rest. Participants were provided visual feedback of the torque and
instructed to resist the lowering of the foot plate through the 30o range of motion
over a 1 s period. After the lengthening contraction, the foot was returned to the
neutral ankle starting position by the investigator over a 2 s (15o/s) period while
the participant relaxed fully. The participant was then instructed to resist the
lowering of the footplate immediately again until the protocol was complete. The
voluntary and electrically evoked responses of the dorsiflexors were recorded at
baseline, during the fatigue protocol immediately following each of the 5 sets, and
during recovery at 0.5 min, 2 min, 5 min, 10 min, 15 min, 20 min, and 30 min after
task termination. Measures following the fatigue protocol included, and were
performed in the following order: (1) maximum evoked twitch properties, (2)
assessment of MVC and voluntary activation, (3) post-activation twitch and twitch
doublet, (4) measure of low frequency torque depression (10:50 Hz ratio; LFTD),
and (5) velocity-dependent shortening power.
4.1.5 Data reduction and analysis: Torque, position and velocity data were
sampled at a rate of 100 Hz. All data were converted to digital format using a 12-bit
analog-to-digital converter (model 1401 Power, Cambridge Electronic Design,
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Cambridge, UK). Surface EMG signals were pre-amplified (x100), amplified (x2) and
band-pass filtered (10-1,000 Hz), and sampled online at 2500 Hz using Spike 2
software (version 6.10, Cambridge Electronic Design Ltd.). Surface EMG from the
MVC was expressed as root mean squared (RMS) and values were obtained from a 1
s time period about the peak torque. All subsequent MVC RMS values were
normalized to the level obtained during baseline. Peak RMS values of the raw
surface EMG during the fast shortening contractions was calculated through the 30o
range of motion from the onset of movement to the end of the range of motion and
then normalized to the fastest baseline contraction. Power was calculated as the
product of torque (Nm) and the peak shortening velocity (rad/s) of the fa ster of 2
contraction attempts. Post-activation potentiation was determined by calculating
the ratio between the amplitude of the peak twitch torque recorded before and
following the isometric MVC. Spike 2 software was used off line to determine M-
wave amplitude, area, duration, the peak twitch torque (Pt), peak doublet torque
(Pd), doublet time to peak twitch (DTPT), half relaxation time (DHRT) of the doublet,
and doublet rate of torque development (DMRTD). Low frequency torque
depression was calculated using a ratio of peak 10 to peak 50 Hz evoked torques
(10:50 Hz).
4.1.6 Statistical analysis: Using SPSS software (version 16, SPSS Inc. Chicago,
IL) a two-way (age x time) repeated measures analysis of variance was performed
to assess all neuromuscular data. Because voluntary activation values are not
normally distributed, a Mann-Whitney U-test was employed and an unpaired T-test
was used for subject characteristics and baseline measures to assess group
86
differences. The level of significance was set at p<0.05. When a significant main
effect or interaction was present, Post hoc analysis using unpaired T-tests was
performed with a Bonferroni correction factor to determine where significant
differences existed. Effect sizes (ES) were calculated using the partial eta-squared
method to explore the magnitude of apparent statistical effects. Due to the small
sample size of old women for LFTD (n=4) unpaired t-tests were performed for this
parameter. The table is presented as means ± standard deviations (SD), and figures
as mean ± standard errors (SE) values, normalized to baseline (pre-test).
4.2 Results
4.2.1 Baseline measures: As shown in Table 3 the old women as compared
with the young women were ~21% weaker for MVC torque (p=0.021, ES=0.292)
despite similar high voluntary activation (~95%, p=0.682, ES=0.012). Peak loaded
shortening velocity (Figure 13) was ~21% slower for the old women than the young
(p<0.001, ES=0.522), which lead to power (calculated as the product of peak loaded
shortening velocity at 20% MVC) to be ~39% less in the old compared with the
young women (p=0.006, ES=0.383). Both groups had a similar Pd (p=0.685,
ES=0.011), while DTPT was ~16% slower (p=0.023, ES=0.284), and DHRT was ~33%
longer in old compared to young, respectively (p=0.012, ES=0.337). Despite similar
Pt (p=0.735, ES=0.007) for the old (3.9 ± 1.6 N·m) and young (4.0 ± 0.9 N·m) women,
the older adults had a reduced capacity for potentiation (105.8 ± 6.0%) compared to
the young (124.6 ± 17.2%) (p=0.023, ES=0.339).
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Table 3. Voluntary and evoked participant baseline characteristics.
Old women had slower absolute evoked doublet twitch torque (Pd) contractile
properties for time to peak twitch (DTPT) (p=0.023, ES=0.284), half-relaxation time
(DHRT) (p=0.012, ES=0.337), and maximum rate of torque development (DMRTD)
(p=0.031, ES=0.258) compared to young. Maximal voluntary isometric contraction
(MVC) torque (p=0.021, ES=0.292), maximum shortening velocity (p=0.001,
ES=0.522), and peak power (p=0.006, ES=0.383) were lower in the old than young
women. Voluntary activation (VA) (p=0.682, ES=0.012) and doublet twitch torque
(p=0.685, ES=0.011) was not significantly different between groups. * Denotes a
significant difference between old and young women.
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Figure 13. Representative unprocessed data
A young and older woman performing a fast velocity-dependent shortening
contraction at baseline and 30 s following (Post) the lengthening contraction task.
The EMG amplitude is presented with arbitrary values (AV). The dashed vertical
line indicates peak velocity.
89
4.2.2 Fatigue and recovery measures: All participants were capable of
completing all contractions, although as reported previously using this contraction
mode some subjects had difficulty lowering the foot plate at a steady pace for the
last few contractions of each set (49). This failure to maintain a constant velocity
resulted in increased eccentric velocities which ranged from 36o/s to 42o/s. Despite
the variation in velocity, the duty cycles were similar (p=0.295, ES=0.680) between
old and young women 0.33 ± 0.07. For the velocity-dependent shortening
contractions, all participants were capable of completing the 30 o range of motion
during baseline measures and following the lengthening contraction task.
Neuromuscular fatigue measures were analyzed with regard to relative changes
over time. For maximum loaded shortening velocity and subsequently peak power
(Figure 14), there were main effects for time (p<0.001, ES=0.681) and age (p=0.007,
ES=0.396) and an interaction (p=0.004, ES=0.244). Thus, at task termination the old
women had a greater loss of power (~19%) than the young (~8%). This difference
persisted until 10 min of recovery and did not recover by 30 min post intervention.
90
Figure 14. Velocity-Dependent Power
Short-term recovery of velocity-dependent power calculated at 20% MVC and
maximal shortening velocity normalized to 100% of baseline values for old (open
symbols) and young women (solid symbols). The dashed lines represent the
lengthening contraction intervention during which time only isometric measures
were obtained. Significant effects for Time (*p<0.05) and Age (†p<0.05). Values are
means ± SE.
91
For dorsiflexor MVC torque there was only a significant effect for time
(p<0.001, ES=0.696). Isometric MVC torque decreased similarly in the old and
young by ~19% following the first set of 30 eccentric contractions and following
each successive set it continued to decrease until it was reduced by ~28%
immediately following task termination. By the end of the 30 min recovery period
the MVC regained 9% but was still significantly less than baseline (Figure 15).
Voluntary activation was maintained greater than 95% at baseline and did not
change (p=0.910, ES=0.022) throughout fatigue and recovery. The incomplete
recovery of MVC by 30 min post intervention suggests similar muscle damage had
occurred in young and old women.
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Figure 15. Maximum voluntary isometric contraction (MVC)
Maximal voluntary isometric strength during and following lengthening
contractions normalized to 100% of baseline values for old (open symbols) and
young women (solid symbols). Significant effects for Time (*p<0.05). Values are
means ± SE.
93
Low frequency torque depression (10:50 Hz) presented a significant effect
for time (p<0.001, ES=0.960) and age (p=0.032, ES=0.225). Over time, the
alterations in the 10:50 Hz ratio were manifested by the greater reduction in 10 Hz
evoked torque compared with the 50 Hz. This indicated there was significant low
frequency torque depression following the lengthening contractions for both
groups. Low frequency torque depression persisted in both groups throughout the
30 min recovery period. However, at task termination the 10:50 Hz ratio was
reduced by 40% in the four old, but only 20% in the young, suggesting there was an
initial greater impairment in E-C coupling in the old women. This age-related
difference was present up to 10 min in the recovery period (Figure 16) at which
time both groups were reduced by 50% and did not change during the final 20 min
of the recovery period.
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Figure 16. Low Frequency torque depression (10:50 Hz)
Low frequency torque depression during and following lengthening contractions
normalized to 100% of baseline values for old (n=4) (open symbols) and young
(n=9) women (solid symbols). The decrease in the 10:50 Hz ratio was driven
primarily by the progressive decline in 10 Hz torque (40% decrease at task
termination, and 60% decrease by 30 min of recovery) with a minimal decrease in
50 Hz (20% decrease at task termination and throughout recovery). Significant
effects for Time (*p<0.05) and Age (†p<0.05). Values are means ± SE
95
There were main effects for time (p<0.001, ES=0.646) and age (p=0.005,
ES=0.437) and an interaction (p<0.001, ES=0.409) for Pt (Figure 17). Twitch torque
decreased by ~21% in the old women following the first set of 30 lengthening
contractions, while the young women had a potentiation of Pt, which increased to
~130% of baseline following Set 1. At task termination the values for the old
women were reduced by 50%, whereas Pt for the young women was not different
from baseline values. Once the potentiating effects of the fatigue protocol were
mitigated in the young, both groups were reduced similarly (~ 50%) 5 min into
recovery. For the Pd torque there was only a significant effect for time (p<0.001,
ES=0.648). Pd continued to decrease (Figure 17) during the lengthening
contractions and remained reduced in both groups by ~40% throughout the 30 min
recovery period For doublet twitch contractile speeds there were only main effects
for time for DTPT (p<0.001, ES=0.544), and DHRT (p<0.001, ES=0.475), meaning
doublet twitch contractile properties slowed similarly in both groups by ~15-20%.
However, there was a main effect of time (p<0.001, ES=0.356) and age (p=0.003,
ES=0.429) and an interaction (p=0.05, ES=0.118) for the DMRTD which was reduced
~15% greater in old women than young women at task termination but was no
longer significantly different between groups 30 s later.
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Figure 17. Peak twitch torque (Pt)
Peak twitch torque during and following lengthening contractions normalized to
100% of baseline values for old (open symbols) and young women (solid symbols).
Significant effects for Time (*p<0.05) and Age (†p<0.05).
97
Tibialis anterior M-wave properties, including: peak-to-peak amplitude,
duration, and area showed a main effect for time (p=0.004, ES=0.190), meaning M-
wave properties were reduced similarly in both old and young women by ~10-15%
at task termination, and returned to baseline value by the end of the 30 min
recovery period. For both the old and young women there were no significant
changes from baseline for (p=0.064, ES=0.151) RMS EMG of the agonist tibialis
anterior during MVCs throughout the protocol. As well, RMS EMG of the soleus
muscle did not differ for time or age from baseline (p=0.222, ES=0.0125). During
the velocity-dependent shortening contractions RMS EMG of the agonist tibialis
anterior or antagonist soleus showed no effect for time (p=0.135, ES=0.125) or age
(p=0.426, ES=0.070) meaning there was no difference in ‘neural drive’ from baseline
contractions.
4.3 Discussion
This investigation tested the hypothesis that neuromuscular function of the
dorsiflexors following repeated lengthening contractions would be impaired more
in the old women than young. Specifically, velocity-dependent power would be
reduced more in the old than young and neither would remain depressed
throughout the 30 min period of recovery following task termination. Indeed, peak
power was reduced by 19% for the older women after the lengthening contractions,
whereas the young women only incurred an 8% decrement at task termination, and
neither recovered. In contrast, isometric MVC torque was reduced similarly (28%)
in both the old and young and did not recover fully. Despite similar muscle damage
98
as indicated by incomplete recovery of MVC torque (61), these findings suggest old
women have greater decrements in velocity-dependent power than their younger
counterparts following repeated lengthening contractions. Therefore, the greater
power-loss in the old than young women is driven more by fatigue mechanisms
influencing impairments in whole muscle loaded shortening velocity following
lengthening contractions than those affecting torque generation per se.
4.3.1 Baseline. The old women in this study were weaker and slower (Table
3) for whole muscle shortening velocity, leading to a greater reduction in power
when compared with young women. The 39% reduction in velocity-dependent
power compared with the young is greater than that reported previously for
velocity-dependent contractions of the dorsiflexors (25%) of old men (41) and
similar to the plantar flexors (38%) of old men (22), and elbow flexors (41%) (56)
and knee extensors (45%) (47) of old women. As well, older women rely more on
the velocity component of power than torque production when compared with old
men and younger adults (56). Valour et al. (2003) reported that when peak muscle
power was compared among various loads (i.e., % MVC) older women reached peak
power at a lower percentage of MVC torque than older men and women. In the
current study we used a relative load of 20% MVC which relies strongly on the
velocity component of power (49). Factors discussed below that impair whole
muscle shortening velocity in older women may greatly impair their ability to
generate power more so than older men and younger individuals.
4.3.2 Lengthening contraction intervention. In the current study, following
150 high-intensity lengthening contractions the old women incurred (up to 10 min)
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a greater loss of velocity-dependent power (19%) than the young (8%) following
task termination, whilst both the old and young women experienced similar
reductions in isometric MVC torque at task-termination (28%). This is similar to
findings from isovelocity fatigue studies in which older adults incur a greater
decline in eccentric isokinetic torque than young, while still maintaining isometric
strength (8). Interestingly, the reduction in MVC torque at 30 min recovery (~19%)
is similar to the reduction following the first 30 lengthening contractions (Figure
15), suggesting the primary insult of muscle damage occurred during the first set of
contractions and the further decrease in MVC torque to task termination can be
attributed to fatigue processes (16, 42). Despite similar reductions in isometric
MVC torque following the lengthening contractions, low-frequency torque
depression was greater in the old than the young women (~25% difference)
following the second set of lengthening contractions and for up to 5 min into
recovery, and neither recovered during the 30 min period of recovery .
The development of fatigue can manifest through central or peripheral
mechanisms (4, 26), or both. In the current study voluntary activation and RMS
EMG amplitude of the tibialis anterior during the isometric MVCs was not reduced
from baseline and did not differ between age groups. In accord with previous
investigations utilizing velocity-dependent contractions, RMS EMG amplitude of the
agonist tibialis anterior during velocity-dependent shortening contractions did not
differ throughout the study (49) or between young and old. Hence, the main site of
fatigue is likely peripheral in nature. Voluntary activation failure can account for
torque loss following muscle damage in other limb muscles (50) however,
100
maintained voluntary activation to the tibialis anterior is a common finding
following lengthening contractions (8, 45, 49). Furthermore, in the present study,
M-wave parameters (i.e., p-p amplitude, area, duration) were reduced similarly in
old and young indicating that muscle damage may have disturbed sarcolemmal
excitability in both age groups equally. However, findings are equivocal; some
studies show a decrease in M-wave properties (30) while others using similar
lengthening contraction protocols do not (45, 49). The reason for this disparity
among studies is unclear, but it may be related to rest intervals between
contractions or because of different aged populations tested.
4.3.3 Fatigue and muscle damage. Although lengthening contractions are less
energetically demanding than isometric and dynamic shortening contractions (2,
54), they are known to induce muscle fatigue in addition to muscle damage (8, 16,
42, 45). A commonly accepted indirect measure of muscle damage is the reduction
and incomplete recovery of isometric MVC torque (6, 19, 61). The concomitant
existence of fatigue and damage may account for the greater initial decline in MVC
torque than either factor alone, however because MVC torque did not recover fully,
this observation may represent muscle weakness (26) and suggest muscle damage
occurred. The long term deficits in force production may be due to damage induced
impairments in E-C coupling (32, 60). In the present study, it seems the old had an
initial greater perturbation in E-C coupling as shown by the reduced twitch torque
and greater low-frequency torque depression compared to the young (Figures 16
and 17). As well, following lengthening contractions a shift to longer muscle lengths
for optimal torque production represents an increase in series compliance of the
101
muscle (29, 64). The presence of overstretched, disrupted sarcomeres in series with
still functional sarcomeres results in an immediate shift in optimum length and is
considered to be a reliable indicator of muscle damage, as it relates to the number of
overstretched sarcomeres (9, 13). An immediate shift in muscle length for optimal
torque production following 120 lengthening contractions has been previously
observed in the ankle dorsiflexors (39). With our study design utilizing a velocity-
dependent contraction task we were not able to record optimal muscle torque-
length per se, however based on the same muscle tested and a similar protocol of
repeated lengthening contractions we would expect a similar increase in the optimal
muscle length-tension relationship as is known to be induced by muscle damage.
The mechanisms responsible for force loss that occur following muscle
damage have been reviewed extensively (3, 20), whereas the processes responsible
for impairments in shortening velocity have received little attention (16, 42, 64).
Data from our study highlight that the effects of fatigue on loaded shortening
velocity are independent of muscle damage and the coexistence of fatigue and
damage is evident by the time course of the transient effects of fatigue and long-
lasting effects of damage. Hence, the combined effects of fatigue and muscle damage
more greatly affect the production of shortening velocity and subsequently power
than either variable alone following this task. Indeed, voluntary maximal shortening
velocity is known to recover rapidly (< 5 min) in young adults after isometric and
concentric fatigue tasks (14, 15). Interestingly, following repeated lengthening
contractions the velocity component of power does not recover fully (49, 64). In a
recent study of young men and women, following repeated lengthening
102
contractions, power remained reduced up to 30 min following task termination
(49). Therefore, long lasting muscle damage appears to limit power production (10,
49) following lengthening contractions 30 min into recovery.
Both the old and young women possibly incurred a similar amount of muscle
damage (i.e., prolonged reduction in isometric MVC), yet the old were more fatigable
than young as indicated by the greater power-loss up to 10 min into the recovery
period. Once the transient effects of fatigue were recovered both groups had a
similar reduced power and for this reason, we can argue both groups experienced
similar impairments in muscle function owing to muscle damage. However, the old
women incurred more fatigue than the young women which can account for the
greater power-loss immediately following the lengthening contractions. The loss of
power in the old women in the current study following 150 lengthening
contractions is less than that observed in studies using protocols of shortening
contractions (8, 22, 40). For example, in older men, McNeil et al. (2007) found a
20% loss of power for the dorsiflexors following 25 fast shortening contractions and
Dalton et al. (2010) found a 26% reduction following 50 fast shortening plantar
flexion contractions. The greater mechanochemical efficiency for lengthening
compared to isometric and shortening contractions result in less perturbation of
intracellular high-energy phosphate (Pi) energetics (16, 54). Thus, despite the
greater number of contractions in this study than the others, the disparate results
can be explained by the task-dependent nature of fatigue (23).
4.3.4 Young vs. old metabolic (dis)advantage. It is well known that older
adults are more fatigue resistant than young when performing isometric tasks,
103
owing to their slower contracting muscle and lower motor unit discharge rates
required to reach fused tetanus as indicated by a shift to the left in the force-
frequency relationship (5). That is to say, under isometric conditions the lower
glycolytic flux in old compared with young is less energetically costly (lower ATP
required) with a greater energy turn over through oxidative processes (36),
resulting in less metabolic acidosis and accumulation of inorganic phosphates thus
mitigating the reduction in isometric MVC torque (33). However, when ‘stressed’
with repeated dynamic shortening contractions this apparent fatigue resistance in
older adults is abolished and in some situations older adults are more fatigable than
young (12). This is found exclusively during tasks which allow velocity to be
unconstrained (i.e., velocity-dependent) (22, 40, 47). Furthermore, it appears based
on the greater power-loss incurred by the old women in this study we now show
older adults may be ‘energetically’ disadvantaged following repeated lengthening
contractions, thus further exacerbating fatigue mechanisms related to whole muscle
shortening velocity and the subsequent generation of power. The greater
accumulation of muscle metabolites during the lengthening contraction protocol in
older women impairs E-C coupling and may limit crossbridge function while
performing a subsequent fast shortening contraction.
A greater initial impairment in E-C coupling is supported further by the
reduced 10:50 Hz ratio and an already impaired capacity for potentiation may have
disadvantaged the older adults for the performance of subsequent ‘fast’ velocity-
dependent contractions (Figure 14) compared with the young. By contrast, the
young had a greater twitch potentiation and were less influenced by LFTD in the
104
first 5 min into recovery (Figures 16 and 17). Post-activation potentiation, due to
myosin light-chain phosphorylation, can compensate for impaired E-C coupling by
increasing myofibrillar calcium sensitivity in spite of the presence of LFTD (28, 52).
In our current study, this suggests the young had less of a reduction in myofibrillar
calcium sensitivity (27) compared with old, meaning they were less adversely
affected by cellular mechanisms of fatigue. This could include: increased H+ and Pi
which directly reduce force output, and can result in a decline in the number and/or
force per unit of the strongly bound cross bridges (25) as well as impaired ADP
dissociation from the myosin head (25) limiting peak shortening velocity. Following
lengthening contractions a failure of the dihydropyridine receptors to stimulate
sarcoplasmic reticulum Ca2+ release (32), and reduced myofibrillar Ca2+ sensitivity
together with minimal potentiation capability might have heightened the effects of
the ‘potentially greater’ metabolite accumulation in older adults effect on the
impaired generation of velocity-dependent power (25, 62, 63). Whereas, velocity-
dependent power in both the old and young women reached a similar value by 10
min into recovery, the greater potentiation in young may have helped offset the
initial perturbations in E-C coupling, thus mitigating the reduction in shortening
velocity (7) and power at task termination. The greater power loss in older women
is likely a result of greater LFTD and E-C coupling failure in the muscles of older
compared with young women, as this is also supported by our observation of a
greater reduction in doublet twitch rate of torque development in the old women
than the young at task termination.
105
In summary, the damaging lengthening contractions impaired shortening
velocity and thus power in both the old and young women, with a greater reduction
in the old for up to 10 min into recovery at which time subsequently both remained
reduced for the duration of the 30 min recovery period. The observations were not
related to neural drive changes but to peripheral alterations primarily affecting E-C
coupling. The mechanisms responsible for the reduction in shortening velocity
following muscle damage may include decreases in the number of functioning
sarcomeres in series, Ca2+ kinetics and myofibular Ca2+ sensitivity. The greater
fatigue in older women can be attributed to their blunted potentiation, a factor in
the young which may have helped offset initial fatigue-induced impairments in
shortening velocity. Furthermore, our findings highlight the value of investigating
changes in the velocity-component of power (i.e., shortening velocity) following
perturbations to the neuromuscular system.
106
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