More pain, less gain: Can painful, fatiguing exercise of one muscle impair the exercise performance of its neighbours?


senior-citizen-gymWe have all experienced the effects of muscle fatigue. Whether carrying groceries or luggage that extra bit further, playing sport or hitting it hard at the gym. For people with conditions such as multiple sclerosis, congestive heart failure, or peripheral vascular disease just going to collect the mail can be fatiguing. The ability of our muscles to produce force during fatiguing exercise is limited by processes within the muscle. However, changes in the ability of the central nervous system to drive muscle also contribute significantly to fatigue. Performing exercise that is perceived as hard or exercise that is painful, like it is for patients with intermittent claudication, may be especially limited by actions of the central nervous system. Sensory nerves in the muscles, called group III and IV afferents, respond strongly to metabolites such as lactate and hydrogen ions that accumulate with muscle work. Feedback from these nerves travels to many areas of the brain and acts to reduce the central nervous system’s ability to voluntarily drive the fatigued muscle (Gandevia et al., 1996, Kennedy et al., 2011). In spite of the subject’s willingness to give a maximal effort, this decrease in voluntary drive results in reduced force and thus, impaired exercise performance. Given that muscle sensory feedback is processed in many areas of the brain and spinal cord, we wondered if their actions could affect muscles other than the fatigued ones. This would mean that feedback from fatigued muscles could impair the performance of muscles not involved in the fatiguing task.

In a series of experiments we fatigued different muscles of the arm and leg and then tested whether voluntary drive and force of another muscle in the same limb were affected by group III and IV muscle afferent feedback. We maintained muscle afferent feedback by occluding blood flow of the fatigued muscle for two minutes. Transcranial magnetic stimuli (TMS) over the motor cortex or peripheral nerve stimulation over the femoral nerve during brief maximal efforts evoked force which was used to calculate voluntary drive.

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WHAT DID WE FIND?

In the upper limb we tested the central nervous system’s ability to drive the muscles that flex the elbow (e.g. biceps) after fatiguing contractions of the muscles that extend the elbow (triceps) and a muscle in the hand that moves your thumb (adductor pollicis).  Below is an outline of what we found when we tested unfatigued muscles that flex the elbow when muscle afferent feedback was maintained after fatiguing contractions of the elbow extensor muscles and the adductor pollicis muscle.

1)  Elbow extensors fatigue:

– 10% reduction in elbow flexor force
– 14% reduction in voluntary drive to elbow flexors

2) Adductor pollicis fatigue:

– 8% reduction in elbow flexor force
– 6% reduction in voluntary drive to elbow flexors

In the lower limb we saw a much greater effect compared to the upper limb when we tested muscles of the same limb (quadriceps and hamstrings) but there was no effect when we tested the same muscles from the other leg (right and left quadriceps). Below is an outline of what we found when we tested unfatigued quadriceps when muscle afferent feedback was maintained after fatiguing hamstring and contralateral quadriceps contractions.

1) Same limb hamstrings fatigue:

– 30% reduction in quadriceps force
– 25% reduction in voluntary drive to quadriceps

2) Opposite limb quadriceps (contralateral leg) fatigue:

– no change in force
– no change in voluntary drive

 

SIGNIFICANCE AND IMPLICATIONS:

3c20233eca4ba70d46dc2c4d96a43aabThese findings mean that sensory feedback from a fatiguing muscle can reduce the central nervous system’s ability to drive another unfatigued muscle of the same limb. This decrease in voluntary drive contributes to reduced force production and thus, impaired motor performance. For patients with congestive heart failure or peripheral vascular disease, group III and IV muscle afferents are even more active either because they become more sensitive to or there is more build-up of the metabolites of muscle work. Thus, these patients are particularly susceptible to motor impairment not only from mechanisms of the cardiovascular system, but also from sensory feedback from fatigued muscles (central nervous system mechanisms).

In summary, the ability to perform exercise that is perceived as hard or exercise that is painful can be limited by feedback from fatigued muscles that acts widely to limit our performance of not only the fatigued muscles themselves but also of other muscles of the same limb despite our willingness to perform at our best.

PUBLICATION:

 

KEY REFERENCES:

Gandevia SC, Allen GM, Butler JE, Taylor JT (1996). Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490: 529-536.

Kennedy DS, McNeil1 CJ, Gandevia SC, Taylor JL (2013). Firing of antagonist small-diameter muscle afferents reduces voluntary activation and torque of elbow flexors. J Physiol 591: 3591-3604.

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