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Central and Peripheral Fatigue in Sustained Maximum Voluntary Contractions of Human Quadriceps Muscle

Authors:

Abstract

1. The fatigue of force that occurs during the first 60 s of a maximum voluntary contraction of the human quadriceps has been examined by comparing the voluntary force with that obtained by brief tetanic stimulation at 50 Hz in nine healthy subjects. In three subjects the voluntary force declined in parallel with the tetanic force whereas in the remainder it fell more rapidly, suggesting that central fatigue was present. 2. For those subjects who showed little or no central fatigue, surface electromyograph (EMG) activity remained approximately constant while the force declined by about 60%. In the others, EMG activity and force declined in parallel but when an extra effort was made the subjects could briefly increase their force and this was accompanied by a proportionately greater increase in EMG activity (generally up to the original value). 3. It is concluded that in sustained maximum voluntary contractions of the quadriceps (a) central fatigue may account for an appreciable proportion of the force loss, (b) surface EMG recordings provide no evidence that neuromuscular junction failure is the limiting factor determining the loss of force in this muscle.
Clinical Science and Molecular Medicine
(1978) 54,609-614
Central and peripheral fatigue in sustained maximum
voluntary contractions of human quadriceps muscle
B.
BIGLAND-RITCHIE*, D. A. JONES, G. P. HOSKING AND
R. H. T. EDWARDSt
Jerry
Lewis Muscle Research
Centre,
Royal
Postgraduate Medical
School,
London
(Received 9
May
1977;
accepted 4 January
1978)
Summary
1.
The fatigue of force that occurs during the
first 60 s of a maximum voluntary contraction of
the human quadriceps has been examined by com-
paring the voluntary force with that obtained by
brief tetanic stimulation at SO Hz in nine healthy
subjects. In three subjects the voluntary force
declined in parallel with the tetanic force whereas in
the remainder it fell more rapidly, suggesting that
central fatigue was present.
2.
For those subjects who showed little or no
central fatigue, surface electromyograph (EMG)
activity remained approximately constant while the
force declined by about 60%. In the others, EMG
activity and force declined in parallel but when an
extra effort was made the subjects could briefly
increase their force and this was accompanied by a
proportionately greater increase in EMG activity
(generally up to the original value).
3.
It is concluded that in sustained maximum
voluntary contractions of the quadriceps (a) central
fatigue may account for an appreciable proportion
of the force loss, (b) surface EMG recordings pro-
vide no evidence that neuromuscular junction
failure is the limiting factor determining the loss of
force in this muscle.
•Present address: Quinnipiac College, Hamden, Conn.
06518,
U.S.A.
f Present address: Department of Human Metabolism, Uni-
versity College Hospital Medical School, University Street,
London WC1E6JJ.
Correspondence: Professor R. H. T. Edwards, Department of
Human Metabolism, University College Hospital Medical
School, University Street, London WC1E 6JJ.
Key words: fatigue, muscle, quadriceps, voluntary
contraction.
Abbreviations: EMG, electromyograph; MVC,
maximum voluntary contraction.
Introduction
Force fatigue during maximum voluntary muscular
contractions (MVC) may occur from failure either
at the neuromuscular junction or at sites proximal
or distal to this. Failure proximal to the junction
may be the result of a decreased voluntary effort,
change in motor neuron excitability (direct or due
to inhibition of afferents from the muscle) or to pre-
synaptic block. Which, if any, of these may limit
the extent of voluntary contractions has been the
subject of controversy in the last 50 years (Reid,
1928;
Merton, 1954). A failure of transmission at
the neuromuscular junction may arise from either a
loss of excitability of the postjunctional membrane
or from depletion of acetylcholine stores. Distal
failure may arise if action potentials fail to
propagate, if coupling between the action potential
and the release of
calcium
fails within the
fibre,
or if
the contractile elements fail to function correctly.
We have examined the ability of normal subjects to
maintain maximum voluntary isometric con-
tractions of the quadriceps for periods up to 60 s.
Force and surface electromyograph (EMG) ac-
tivity have been measured and the response of part
of the muscle to maximal electrical stimulation at
different times during the MVC and has been used
609
610
B.
Bigtand-Ritchie et al.
as an index of muscle contractility that is indepen-
dent of central drive.
This work follows our previous studies of
quadriceps muscle function (Edwards, Young,
Hosking & Jones, 1977) and was designed to help
answer the question 'Does the fatigue (i.e. failure to
generate the required force) arise because the
muscle machinery is failing, or because the subject
is not willing to go on driving it with the same
motivation as at the start?'.
Methods
Subjects
We studied nine healthy adult laboratory person-
nel (one female; ages 25-50 years) who were
familiar with the procedures and gave their
informed consent as required by the local Research
Ethics Committee. Both legs were studied and no
consistent differences in the ability to maintain
force were detected.
Measurements of force
The blood supply to leg muscles is occluded
during isometric contractions of more than about
20%
of the maximal voluntary force (Barcroft &
Millen, 1939; Edwards, Hill & McDonnell, 1972),
but since many of the present experiments involved
interruption of the contraction for brief periods of
stimulation, a cuff around the upper thigh was
inflated to 200 mmHg throughout to prevent any
return of blood supply. The force produced by iso-
metric contractions of the quadriceps muscle was
measured with a strain gauge attached to the ankle
while the subject was seated in an adjustable chair
(Edwards et al., 1977) and recorded on a u.v.
oscillograph.
Surface EMG was recorded with two adhesive
cup electrodes filled with electrode paste, one
situated on the skin over the lower third of the
vastus lateralis muscle, the other over the tendon
on the lateral aspect of the knee. An earth electrode
was placed on the lower leg. The EMG activity was
amplified, rectified, smoothed with a time constant
of 0-2 s and displayed on a u.v. oscillograph.
Electrical stimulation
Stimulation of the quadriceps, either per-
cutaneously with surface pad electrodes or by
localized stimulation of the femoral nerve, was
carried out as previously described (Edwards, Hill
& Jones, 1975; Edwards et al., 1977) with a short
stimulus pulse duration (50 ßs) so as to limit
excitation to nerve branches in the muscle. Direct
excitation of human muscle fibres required longer
pulses (100-500 μβ) when studied in vitro (Moulds,
Young, Jones & Edwards, 1977).
Results
To maintain a maximal isometric contraction
(MVC) of the quadriceps for 60 s takes a con-
siderable effort. During the first 30 s discomfort is
mild but between 30 and 45 s pain in the thigh
becomes increasingly severe. There is a pro-
gressive change in the perceived sensations from
the leg with the result that a subject, without visual
feedback, is uncertain of the force exerted towards
the end of the contraction. Pain in the thigh is not
due to ischaemia alone since it largely disappears
as soon as the contraction ceases, even when the
cuff around the thigh remains inflated. To reduce
variation due to pain the results presented here are
all from subjects experienced in the experimental
procedures.
Time course of a sustained MVC
Subjects were first asked to make a series of brief
maximal contractions, the highest of which was
taken as 100% MVC. Aided by visual feedback
subjects were then asked to maintain a contraction
as close as possible to this maximum for 60 s.
During this period force fell to about 30% of the
initial level, but the precise time course varied be-
tween individuals. The consistent performances of
the two subjects with the greatest difference in the
time course are shown in Fig. 1, the records having
been made on several occasions over a 2 months
period.
Central and peripheral fatigue
In one subject the maintained maximum volun-
tary force was compared with the force obtained by
supramaximally stimulating the muscle via the
femoral nerve. In the unfatigued muscle the MVC
was matched by stimulating at 50 Hz, at which
frequency a fully fused tetanus of the quadriceps
develops (Edwards et al., 1977). During each
tetanus the stimulus voltage was increased to con-
firm that nerve stimulation was supramaximal. The
subject then held a MVC which was interrupted
every 15 s for a brief period of stimulation at 50 Hz
(Fig. 2a).
Human muscle fatigue 611
The voluntary and stimulated contractions fell to
a similar extent during the first 30 s. Thus fatigue
during this period could only be due to a failure at
or distal to the neuromuscular junction. After 45 s
the voluntary force was less than the force
produced by the test tetani, indicating that in this
later period a loss of central neural drive con-
tributed to the force fatigue.
Femoral nerve stimulation is painful and carries
a risk of dislocating the patella, whereas per-
cutaneous stimulation of about 50% of the quad-
riceps with large pad electrodes is quite acceptable
(Edwards et al., 1977). Heat measurements during
stimulated and maximal voluntary contractions
indicate that percutaneous stimulation can maxi-
mally activate a portion of the muscle (Edwards,
1975).
The experiment was repeated with the same
subject but, instead with percutaneous stimulation
of the quadriceps at 50 Hz, activating 48% of the
muscle (Fig.
2b,
initial value).
During the first part of
the
MVC voluntary and
stimulated force fell to a similar degree. Thereafter
the voluntary force fell more than the tetanic force
so that the stimulated contraction became 80% of
the voluntary force after 60 s (Fig.
2b).
The relative
changes in the voluntary and stimulated forces
were very similar to those seen in the same subject
with femoral nerve stimulation (Fig. 2a). This
indicates that percutaneous stimulation of
a
portion
of the muscle can be used to determine function
independently of central drive.
Possible fatigue of the central neural drive during
60 s MVC was assessed, with percutaneous
stimulation, in all subjects. Central fatigue was
considered to be present when the MVC force
declined more rapidly than did the tetanic force
produced by the brief stimulated contractions.
Of
the
nine subjects studied, four showed little or
no central fatigue. In five it amounted to between
24 36
Time (s)
FIG.
1. Time course of uninterrupted maximum voluntary con-
tractions (MVC) of the quadriceps. Subjects were asked to hold
a MVC for 1 min. Points are the mean1
SD)
of four separate
contractions for subject D.O. (#), and six contractions for
subject G.H. (O). Force is expressed as a percentage of the
initial value.
60
3
140
(a)
500
(W
15
30
Time (s) 60
FIG.
2. Comparison of the force obtained by electrical stimulation with the voluntary force during a sustained
maximum voluntary contraction (MVC) of the quadriceps, (o) Femoral nerve stimulation: stimulus marker (shaded
area) gives a record of the stimulation voltage and duration.
(A)
Percutaneous stimulation. Duration of stimulation (at
constant voltage) is indicated by the shaded areas. Force (newtons) and time scales apply to both
records.
Values given
just below the stimulus markers are the tetanic force as a percentage of the voluntary force measured immediately
before the tetani. Results in (a) and (6) are from the same subject.
612
B.
Bigland-Ritchie et al.
30
Time (s) 45
100
400
g 300
U
£
200
100
150
100
o
s
in
50 W5
20 30
Time (s) 50
FIG.
3. Force and smoothed, rectified EMG (SREMG) during sustained maximum voluntary contraction (MVC) of
quadriceps in (a) a subject (D.O.) with no central fatigue and (4) in subject D.J. with central fatigue; 'extra efforts'
were made at times shown by the arrows. Force scale is in newtons. The smoothed, rectified EMG is given as a per-
centage of the value at the start of
the
MVC.
10 and 30% of the force loss after 60 s of sustained,
uninterrupted contraction. With practice, the de-
gree of central fatigue generally became less though
these subjects were not able completely to over-
come it.
Surface EMG activity during sustained MVC
The smoothed, rectified EMG activity and force
were measured at intervals throughout the con-
traction in seven of the subjects (Fig. 3). To show
how these vary the ratio of the smoothed, rectified
EMG divided by the force (here called the E/T
ratio) as first used by Stephens & Taylor (1972) is
shown in Fig. 4. The subjects could be divided into
two groups. In group 1, where the smoothed,
rectified EMG declined roughly in proportion to
the fall in force (resulting in relatively constant
E/T
ratios), all the four subjects showed central
fatigue when previously tested, as described above.
In group 2 the smoothed, rectified EMG increased
during the first 10-15 s and then remained high
while the force fell to between 20 and 35% of the
5 ·
Si
Group 2
Group 1
FIG.
4. Relationship between smoothed, rectified EMG
(SREMG) and force during prolonged maximum voluntary con-
traction (MVC) in seven subjects. The SREMG is divided by
force (E/T ratio, ordinate) and the value at the start of
the
con-
traction expressed as 1·0. Group 2 subjects exhibited no central
fatigue but were in brief extra efforts able to achieve E/T ratios
close to those found in group 2 subjects.
fresh MVC. This gave E/T ratios three to five times
the control value at the end of the contraction. The
three subjects in this group had previously shown
no central fatigue.
Human
muscle fatigue 613
Subjects were asked to maintain a MVC and, at
15 s intervals, to make a brief extra effort. Subject
D.O.,
typical of those exhibiting little or no central
fatigue, showed the initial rise in smoothed,
rectified EMG to a value which was then main-
tained until near the end of the contraction (Fig.
3a).
When asked, he could produce virtually no
extra force nor was there any increase in the
smoothed, rectified EMG. The second subject
(DJ.),
in whom approximately 10% central fatigue
had been demonstrated, showed the same initial
rise in smoothed, rectified EMG but after about 10
s the smoothed, rectified EMG and force fell at the
same rate (Fig. 3b). When this subject made an
extra effort both smoothed, rectified EMG and
force increased momentarily but with a greater pro-
portional increase in the electrical activity. If the
ElT ratio was expressed as 1-0 at the start of the
contraction, it became
1
4
just before the
first
extra
effort, increasing to 1-7 during this brief effort.
After 30 s the value before was again 1-4,
increasing to 2-0 during the brief effort and for the
last effort the values were 1-7 and 2-9 respectively.
Although the 'before' values are similar to those
seen for the group 1 subjects shown in Fig. 4,
values during the brief extra efforts approached
those maintained by group 2 subjects. All the
subjects showing a fall in smoothed, rectified EMG
during the contraction could increase the level pro-
portionately more than the increase in force during
the extra efforts, thus briefly increasing the ElT
ratio.
Discussion
Our studies show that changes occurring proximal
to the neuromuscular junction (i.e. central fatigue)
can consistently account for up to 30% of
the
total
force loss even in apparently well-motivated sub-
jects during sustained contractions of the quad-
riceps. All subjects who showed evidence of central
fatigue could overcome this in brief extra efforts.
The results demonstrate that fatigue cannot be all
attributed to factors at, or distal to, the neuro-
muscular junction, without first ascertaining, par-
ticularly when studies are done on naive subjects,
that central components are not also present.
In experiments on the first dorsal interosseous
muscle Stephens & Taylor (1972) found that the
smoothed, rectified EMG and force declined in
parallel, resulting in a constant ElT ratio
(smoothed, rectified EMG divided by force) during
the first 60 s of the contraction. They interpreted
this to show that fatigue was mainly due to failure
of neuromuscular transmission, having excluded
central fatigue because the evoked synchronous
muscle action potential was also shown to de-
crease.
Although
a
number of
our
subjects showed a
constant ElT ratio with contractions of the
quadriceps, we believe that for these subjects this
constancy could be accounted for by central
fatigue. For subjects without central fatigue the
smoothed, rectified EMG, after an initial rise,
remained fairly constant at a time when the force
was falling, so that the ElT ratio increased
throughout the contraction. Those subjects with
evidence of central fatigue could briefly increase
their ElT ratios to about the same level by making
brief extra efforts. Our findings for the quadriceps
therefore differ in this respect from those of
Stephens & Taylor (1972) for the first dorsal
interosseous.
The smoothed, rectified EMG signal recorded
during a contraction depends on the number, size
and distribution of active units in the muscle, the
size of the individual fibre action potentials, the
firing frequency and the degree of synchronization
of motor unit activity. The influence of
these
on the
surface recorded signal is not known, and we are
therefore reluctant to speculate about the site of
failure on the basis of smoothed, rectified EMG
data.
It was noticed that towards the end of a
sustained MVC subjects with little central fatigue
appeared actually to improve their voluntary per-
formance as compared with their response to
stimulation at 50 Hz. However, this effort seems
likely to arise from a diminished response to
stimulation at 50 Hz rather than an improvement
in voluntary performance. Parallel studies on the
adductor pollicis (B. Bigland-Ritchie, R. H. T.
Edwards & D. A. Jones, unpublished work) have
shown that fatigued muscle responds to stimulation
at 20 Hz better than at 50 Hz. As a practical con-
sideration, if muscle contractility is to be tested
during the course of a prolonged MVC, a 50 Hz
tetanus is appropriate at the start of the con-
traction but after about 30-45 s stimulation at a
lower frequency (20 Hz) is a better match to the
force of the voluntary contraction, so giving more
reliable information. This suggests that in order to
maintain optimum force during a fatiguing con-
traction the
firing
frequency of motor neurons must
decline, as has been observed (Marsden, Meadows
& Merton, 1971). The smoothed, rectified EMG
might therefore be expected to fall somewhat even
without any neuromuscular block.
In any investigation involving prolonged MVC
614
B.
Bigland-Ritchie et al.
of the quadriceps the possibility
of
central fatigue
must
be
taken into account. We suggest that this
should
be
checked
by
comparing
the
voluntary
force with tetani
at
50 Hz during the first 30
s of
the contraction,
and at a
lower frequency there-
after.
It
would appear that central neural drive pro-
gressively falls during sustained MVC
but
that
subjects
can
overcome this tendency
to
various
degrees.
Acknowledgments
This work was supported
by
the Wellcome Trust
and
the
Muscular Dystrophy Group
of
Great
Britain and also
in
part by grant NS 09960 from
the U.S.P.H.S. to B.B.-R.
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Heat-induced hypo-hydration (hyperosmotic hypovolemia) can reduce prolonged skeletal muscle performance; however, the mechanisms are less well understood and the reported effects on all aspects of neuromuscular function and brief maximal contractions are inconsistent. Historically, a 4-6% reduction of body mass has not been considered to impair muscle function in humans, as determined by muscle torque, membrane excitability and peak power production. With the development of magnetic resonance imaging and neurophysiological techniques, such as electromyography, peripheral nerve, and transcra-nial magnetic stimulation (TMS), the integrity of the brain-to-muscle pathway can be further investigated. The findings of this review demonstrate that heat-induced hypo-hydration impairs neuromuscular function, particularly during repeated and sustained contractions. Additionally, the mechanisms are separate to those of hyperthermia-induced fatigue and are likely a result of modulations to corticospinal inhibition, increased fibre conduction velocity, pain perception and impaired contrac-tile function. This review also sheds light on the view that hypo-hydration has 'no effect' on neuromuscular function during brief maximal voluntary contractions. It is hypothesised that irrespective of unchanged force, compensatory reductions in cortical inhibition are likely to occur, in the attempt of achieving adequate force production. Studies using single-pulse TMS have shown that hypo-hydration can reduce maximal isometric and eccentric force, despite a reduction in cortical inhibition, but the cause of this is currently unclear. Future work should investigate the intracortical inhibitory and excitatory pathways within the brain, to elucidate the role of the central nervous system in force output, following heat-induced hypo-hydration.
... Bien que partiellement remis en question au cours des dernières années, les causes de la fatigue p. 105 ont été longtemps divisées en deux groupes : les causes centrales désignant les modifications ayant lieu en amont de la jonction neuromusculaire et les causes périphériques qui désignent les modifications en aval de la jonction neuromusculaire (Amann et al., 2013;Babault et al., 2006;Bigland-Ritchie et al., 1978;Gandevia, 2001;Lambert et al., 2005). Les causes centrales regroupent généralement les modifications de la commande nerveuse qui vont avoir pour résultat une diminution de l'influx nerveux descendant en direction du muscle. ...
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La drépanocytose est une maladie caractérisée par la production d’une hémoglobine mutée, l’hémoglobine S, dont les formes les plus répandues sont la forme homozygote S/S et double hétérozygote composite S/C. L’hémoglobine S possède la capacité de polymériser au sein du globule rouge en condition désoxygénée modifiant sa morphologie provoquant ainsi des complications cliniques multi-organiques. Ces patients présentent une capacité à l’exercice réduite dont les causes sont des altérations cardio-vasculaires cependant l’implication du muscle squelettique n’est pas encore totalement caractérisée dans la drépanocytose. En effet, le muscle squelettique drépanocytaire présente une amyotrophie, un remodelage profond de la microcirculation et une diminution de sa capacité à produire de la force cependant la présence d’une dysfonction musculaire à l’exercice n’a pas encore été décrite. Plusieurs études suggèrent que le stress oxydatif pourrait être élevé dans le muscle drépanocytaire expliquant ainsi en partie les altérations observées. Chez les sujets sains, l’exercice chronique aérobie est connu pour améliorer la capacité antioxydante musculaire notamment par l’augmentation de l’activité des enzymes antioxydantes. Cependant, les effets de ce type d’exercice sur le stress oxydatif n’ont pas encore été caractérisés dans la drépanocytose. Ainsi, les objectifs de cette thèse sont de 1) mettre en évidence une dysfonction musculaire chez des patients drépanocytaires S/S et S/C et de 2) déterminer les modifications induites par un exercice chronique aérobie sur le stress oxydatif au sein du muscle squelettique dans un modèle murin drépanocytaire. Lors d’une première étude, des sujets sains (A/A) et patients drépanocytaires S/S et S/C ont effectué un exercice mono-articulaire sous-maximal du quadriceps à une intensité correspondant à 25% de leur force maximale isométrique (Fmax) suivi d’un test de marche de 6 minutes (T6M). Fmax a été mesurée avant et après cet exercice mono-articulaire, et après le T6M et la perte de Fmax a été utilisée pour quantifier la fatigabilité musculaire. Au cours du protocole, les activités électromyographiques du Vastus Lateralis (VL) et du Vastus Medialis ainsi que l’oxygénation musculaire par spectroscopie proche infrarouge du VL ont été mesurés au cours de l’exercice. Le principal résultat de cette étude est que les patients drépanocytaires S/S et S/C présentent une fatigabilité musculaire accrue comparés aux sujets A/A. Cette fatigabilité accrue semble être provoquée par des altérations musculaires plutôt qu’une modification de l’oxygénation musculaire. De plus, il semblerait que les mécanismes d’apparition de la fatigue musculaire soient différents entre les S/S et S/C comme le suggère les modifications des paramètres électromyographiques. Ainsi, le muscle des patients S/C semble moins altéré que celui des patients S/S. Dans une seconde étude, des souris Townes A/A et S/S ont suivi un exercice chronique aérobie d’intensité modérée de 8 semaines puis la mesure de marqueurs permettant de caractériser la balance pro/anti-oxydant a été effectuée dans le gastrocnemius, le plantaris et le soleus. A l’issue de ces 8 semaines, nous avons observé des modifications uniquement dans le gastrocnemius des souris S/S entraînées. En effet, l’activité de la NADPH oxydase ainsi que de la superoxyde dismutase et de la catalase étaient plus élevées chez les souris S/S entraînées. Ces résultats suggèrent une altération de la balance pro/antioxydante en réponse à un exercice chronique aérobie d’intensité modérée au sein du muscle squelettique drépanocytaire. Enfin, contrairement aux souris S/S entraînées, nous n’observons pas de modifications de la balance pro/antioxydante dans les souris S/S sédentaires indiquant que le stress oxydatif ne serait pas augmenté dans le muscle drépanocytaire.
... It stems from active skeletal muscles that are involved in the peripheral processes as well as supraspinal mechanisms within the brain, thus comprising physiological and psychological aspects (Gandevia, 2001;Berchicci et al., 2013). The fatigue processes at or distal to the neuromuscular junction is referred to as peripheral fatigue and those attributed to the central nervous system affecting the neural drive to the muscle as central fatigue (Bigland-Ritchie et al., 1978). ...
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... Yorgunluk, bir kasın verilen bir aktiviteyi gerçekleştirmek için istenen ya da beklenen kuvveti devam ettirmede başarısızlığı olarak tanımlanır (37). Fizyolojik olarak maksimal güç üretme kapasitesindeki düşüşün zaman ile ilişkili bir olgusudur (38). ...
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