Download Magnetic muscle stimulation produces fatigue without effort

J Appl Physiol 103: 733–734, 2007;
doi:10.1152/japplphysiol.00660.2007.
Invited Editorial
Magnetic muscle stimulation produces fatigue without effort
Janet L. Taylor
Prince of Wales Medical Research Institute, University of New South Wales, Sydney, Australia
Address for reprint requests and other correspondence: J. L. Taylor, Prince
of Wales Medical Research Institute, Barker St., Randwick, NSW, Australia
2031 (e-mail: [email protected]).
http://www. jap.org
The article by Swallow and colleagues in the Journal of
Applied Physiology (8) presents a new technique for stimulating human muscle at sufficient levels to produce fatigue without the local pain associated with electrical stimulation. As
such, it presents a practical rather than conceptual advance that
will allow clinical testing of muscle endurance and will aid in
research studies of muscle fatigue. Stimulation of quadriceps
was carried out using repetitive magnetic stimulation (Magstim
Rapid2) via a large, flexible oval coil that could be wrapped
securely over the front of the thigh. The coil was fluid cooled
to prevent overheating. In magnetic stimulation, a quickly
changing magnetic field is generated by a pulse of current
flowing through a coil of wire. The magnetic field in turn
generates a current inside the body, and this depolarizes axons
in the same way as an electrical stimulus (1). The advantage is
that with magnetic stimulation the current does not have to pass
through the relatively high resistance of the skin so that
nociceptors in the skin are not activated. The flexible coil is
also an advance over a stiff coil because it allows better
coupling of the magnetic field with the tissue. It is not clear
how well this technique could be adapted to muscle groups
other than quadriceps. It is likely that the knee flexors could
also be activated successfully, but smaller coils may need to be
developed for other muscles.
Swallow and colleagues (8) chose to stimulate the quadriceps muscle at 30 Hz with an intensity sufficient to produce
30% of the maximal twitch force and an intermittent pattern of
2-s contraction and 3-s rest. By the end of 50 trains of stimuli,
the force produced fell by ⬃35% in control subjects. In
patients with severe chronic obstructive pulmonary disease, the
same protocol resulted in greater fatigue, showing poorer
endurance of the muscle. Muscle biopsy confirmed different
muscle properties in the two groups with a reduced proportion
of type 1 fibers and a reduced oxidative capacity in the
patients’ muscles. Thus the technique provides a noninvasive,
well-tolerated way to determine human muscle properties, in
particular, endurance. A measure of endurance, the time for
force to fall by 30%, had acceptable reliability between days.
Other muscle properties that were not measured but could be
informative during the fatiguing stimulation protocols include
contraction and relaxation rates.
Some uncertainty is introduced into the mechanisms of
fatigue in this study because stimulus artefact prevents recording of the electromyogram (EMG) during stimulation. Thus
decreases in motor axonal excitability, which would reduce the
number of muscle fibers activated (12), and block at the neuromuscular junction or impairment of muscle membrane excitability
because of the frequency of stimulation cannot be excluded (4).
Such mechanisms are rarely important in fatigue in voluntary
contractions but may contribute with this submaximal stimulation
technique. However, combining remote nerve stimulation with
magnetic stimulation over the muscle should allow such contributions to be determined. Other questions, such as whether,
in addition to direct motor axon activation, the stimulus evokes
force reflexly through activation of the Ia afferents, may not be
8750-7587/07 $8.00 Copyright © 2007 the American Physiological Society
733
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IN DISEASE AND OLD AGE, muscle function decreases, and greater
impairments in performance are associated with increased
mortality (6, 9, 10). Although muscle strength and endurance
can be assessed with voluntary exercise, measurements can be
confounded by changes in the way the muscle is driven by the
nervous system and by cardiorespiratory limitations. A means
to measure muscle strength and endurance without volition
could allow useful assessment of muscle properties and their
importance independent of systemic influences.
To determine the fatigue properties of isolated muscles, the
muscle is stimulated at a predetermined frequency, and the decline
in force produced by a constant stimulus to the muscle is measured. To fatigue human muscles is often less straightforward.
They can be fatigued by voluntary activity and the fatigue measured as either a decrease in force produced by a maximal
voluntary contraction or as a decrease in the twitch force produce
by maximal stimulation of the nerve to the muscle (e.g., Ref. 2).
To produce fatigue, subjects can be asked to contract the
muscle group maximally or to a submaximal target force. In
both cases, neural drive to the muscle, as determined by
voluntary and reflex inputs to the motoneurons, plays a part in
determining the activity of the muscle. During maximal efforts,
muscle is rarely driven to generate its maximal force, and as
fatigue develops the ability to drive the muscle falls further.
Hence, some of the loss of force of fatigue is not due to muscle
properties but reflects failure within the nervous system (for
review, see Ref. 5). Furthermore, even if muscle is driven
maximally, this does not mean that the frequency of motor unit
firing is the same in different subjects. For example, women
tend to have slower muscle kinetics than men for biceps brachii
(e.g., Ref. 7). Thus full force from the muscle should be
generated by lower motor unit firing rates, so that after the
same period of maximal exercise, muscle fibers in men will
have been activated more times than those in women. When
fatigue develops during the performance of submaximal exercise, volitional drive is increased so that the target force is
maintained by recruitment of more motor units (2, 11). This
means that across the muscle, some muscle fibers will have
undergone a lot more activity than others. It is also possible to
treat a human muscle like an “isolated” muscle and electrically
stimulate the nerve to the muscle or the intramuscular nerve
fibers. Functional electrical stimulation is used frequently in
people with spinal cord injury to produce high-force fatiguing
contractions. However, in neurologically intact subjects, the
major deterrent to producing fatigue through electrical stimulation is discomfort. While some subjects will tolerate the
intensity and frequency of nerve or muscle stimulation required
to produce fatigue, most will not. This is even more problematic in patient groups where subjects may be old or frail.
Invited Editorial
734
J Appl Physiol • VOL
when changes in voluntary forces are confounded by altered
neural drive.
REFERENCES
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NJ, Rothwell JC, Wassermann EC, Puri BK. London: Arnold, 2002,
p. 3–17.
2. Bigland-Ritchie B, Furbush F, Woods JJ. Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. J Appl
Physiol 61: 421– 429, 1986.
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with plateau-like behavior of human motoneurons. J Neurosci 21: 4059 –
4065, 2001.
4. Fuglevand AJ, Keen DA. Re-evaluation of muscle wisdom in the human
adductor pollicis using physiological rates of stimulation. J Physiol 549:
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5. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue.
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7. Hunter SK, Butler JE, Todd G, Gandevia SC, Taylor JL. Supraspinal
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NS, Schols AM, Moxham J, Polkey MI. A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl
Physiol (June 14, 2007). doi:10.1152/japplphysiol.00025.2007.
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Moore AJ, Moxham J, Polkey MI. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary
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10. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH,
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103 • SEPTEMBER 2007 •
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answerable (3). Similarly, it may be difficult to determine
whether antagonist muscles are also stimulated and contributing to force measurements.
The stimulation probably activates the intramuscular fibers
of the nerves innervating quadriceps. This suggests that the
muscle fibers that are stimulated will be a random cross-section
of fiber types with the likelihood of stimulation largely
dependent on the location of the innervating axons relative
to the magnetic coil. The current generated by the magnetic
pulse should be strongest under the edges of the coil rather
than in its center and will reduce with depth (1). Thus a
submaximal contraction produced by this stimulus will not
mimic a voluntary contraction that preferentially recruits
slower fatigue-resistant fibers. Stimulation should recruit a
subset of fibers that are reasonably representative of the
whole muscle.
Apart from clinical testing of muscle endurance, possible
uses for nonvolitional muscle activation without discomfort
include as a substitute for functional electrical stimulation to
preserve muscle mass and improve muscle strength and endurance in patients with intact sensation. Of course, feasibility
may be limited by the cost of the stimulator. In research, the
technique is likely to allow much better comparison of findings
in isolated muscle with those in human subjects. It should
allow the same protocols to be applied in both conditions so
that the behavior of the stimulated human muscle in vivo can
act as a step toward translating findings from isolated muscles
to voluntary contractions. A proviso here is that the effects of
axonal excitability changes and afferent stimulation are
considered. Magnetic muscle stimulation may also have an
advantage over electrical stimulation in comparing muscle
performance from day to day. Careful positioning of the coil
may allow forces to be evoked reproducibly with the same
stimulus intensity. This could be helpful in determining
changes in tetanic forces, as well as changes in other muscle
properties with pathology, after exercise, or with training,