Valerie Gladwell
Department of Biological Sciences, University of Essex, Colchester, UK

https://doi.org/10.36866/pn.62.35

The brain’s command to exercising skeletal muscles undoubtedly simultaneously initiates appropriate cardiovascular changes (Secher, 1999). However, feedback from the contracting muscles also contributes significantly. Recent data suggest a special role for one type of afferent fibre in inhibiting cardiac vagal activity.

Studies in animals show that stimulation of the small afferent nerve fibres within the muscle cause increases in heart rate and blood pressure (Coote et al. 1971). Similar effects have been shown in humans with electrical stimulation to induce muscle contraction. This evokes changes in heart rate and blood pressure of a similar magnitude to those contractions which are voluntary in nature. Furthermore, when circulation is occluded at the end of involuntary contraction, blood pressure remains elevated, whereas heart rate falls rapidly to baseline levels (Bull et al. 1989). (Fig. 1).

Two types of slow conducting muscle afferent fibres (type III and IV) have been shown to contribute to the cardiovascular changes via feedback mechanisms; type IV have been shown in humans and animals to respond to accumulation of metabolites, whereas type III respond to mechanical stimuli. It is likely that there is some overlap between these receptors with some responding to both types of stimuli. As heart rate increases rapidly at the initiation of contraction and rapidly falls to baseline at the end of contraction, particularly if metaboreceptors continue to be stimulated at the end of the contraction (by occlusion of the blood supply and thus trapping metabolites), it is unlikely that the metaboreceptors are the major contributing factor to the changes in heart rate. It is more probable that mechanoreceptor stimulation is responsible for the rapid rise at the initiation of contraction, with the removal of stimulation causing the fall in heart rate at the termination of contraction.

Although experiments have been conducted in animals to look at the selective influence of type III afferents, it has proved to be more difficult in humans. However, recent experiments in humans have been conducted to try to stimulate mechanoreceptors selectively. Leg compression to increase intramuscular pressure has been used and caused increases in both heart rate and blood pressure (Williamson et al. 1994). This stimulus is likely to stimulate both type III and IV afferents or polymodal afferents.

We considered that a ’purer‘ method of muscle mechanoreceptor stimulation would be to use sustained passive stretching of the muscle whilst the subject was in a semi-supine position (Gladwell & Coote, 2002). Heart rate increased rapidly and the increase was sustained during the stretching period, whilst there was only a transient increase in blood pressure. Additionally, it was identified that rhythmic passive stretching did not elicit any cardiovascular response, suggesting that larger afferent spindles and Golgi tendon organs did not play a role. Interestingly, the cardiovascular response to stretch performed following muscle contraction with occluded circulation was not sensitized by the metabolic conditions within the muscle. (Fisher et al. 2005).

In animal models, passive stretch of the muscle has been shown to elicit a reduction in cardiac vagal activity (Murata & Matsukawa, 2001). In humans, the increase in heart rate brought about by the stimulation of mechanoreceptors is also likely to be vagally-mediated, judged by the rapidity of the change and a decrease in heart rate variability, which is an index of vagal activity. Further, as animal experiments have shown that the baseline level of vagal activity is important in the heart rate response to contraction, we performed additional experiments which altered the level of vagal activity just prior to the stretching period. Drug induced vagal blockade and rhythmic hand-grip, both of which reduce vagal activity, significantly decreased the response to passive stretch (Gladwell et al. 2005).

An additional way of altering vagal activity is to alter the input from the baroreceptors using brief pressure or suction over the baroreceptors which are located in the carotid sinus in the neck. An increase in pressure mimics a decrease in blood pressure, leading to a decrease in vagal activity, whereas suction mimics an increase in blood pressure causing an increase in vagal activity. Interestingly, neck suction which results in a decrease in heart rate significantly reduced the increase in heart rate caused by passive stretching. This suggests that the increase in vagal activity brought about by the neck suction is not overcome by the stimulation of the mechanoreceptors. It is likely that this indicates that the stimulation of the mechanoreceptors is not great enough to overcome the increase in cardiac vagal activity by the baroreceptor afferents. Neck pressure, on the other hand, resulted in a slight augmentation of the response to stretch. The results of both neck pressure and neck suction may provide additional evidence to support an argument that the two opposing inputs (mechanoreceptor and baroreceptor afferents) interact at a common neuronal pool.

Studies to date have shown that the stimulation of muscle afferents has a specific functional role in exercise, with mechanoreceptors (alongside central command) inducing the rapid increase in heart rate at the onset of exercise by a reduction in vagal activity (Fig. 2).

The mechanoreceptors that are probably responsible for this immediate reduction in vagal activity are likely to be those Group III afferent fibres that respond to stretch. We suggest that these could be called ’tentonoreceptors‘ (from the Greek ’tentono‘ meaning stretch) to distinguish them from other types of mechanoreceptors found elsewhere. The stimulation of these tentonoreceptors is likely to be important to ensure close matching of cardiac output and oxygen delivery to the exercising muscle in the early stages of exercise, prior to the re­distribution of blood flow.

References

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Fisher JP, Bell M, White MJ et al. (2005). Cardiovascular responses to human calf muscle stretch during varying levels of muscle metaboreflex activation. Exp Physiol 90, 773-781.

Gladwell VF & Coote JH (2002). Heart rate at the onset of muscle contraction and during passive stretch in humans: a role for mechanoreceptors? J. Physiol 540, 1095-1102.

Gladwell VF, Fletcher J, Patel N, Elvidge L, Lloyd D, Chowdhary S & Coote JH (2005). The influence of small fibre muscle mechanoreceptors on cardiac vagus in humans. J Physiol 567, 713­721.

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