Autonomic responses to exercise: Group III/IV muscle afferents and fatigue

Abstract

Group III and IV muscle afferents originating in exercising limb muscle play a significant role in the development of fatigue during exercise in humans. Feedback from these sensory neurons to the central nervous system (CNS) reflexively increases ventilation and central (cardiac output) and peripheral (limb blood flow) hemodynamic responses during exercise and thereby assures adequate muscle blood flow and O2 delivery. This response depicts a key factor in minimizing the rate of development of peripheral fatigue and in optimizing aerobic exercise capacity. On the other hand, the central projection of group III/IV muscle afferents impairs performance and limits the exercising human via its diminishing effect on the output from spinal motoneurons which decreases voluntary muscle activation (i.e. facilitates central fatigue). Accumulating evidence from recent animal studies suggests the existence of two subtypes of group III/IV muscle afferents. While one subtype only responds to physiological and innocuous levels of endogenous intramuscular metabolites (lactate, ATP, protons) associated with ‘normal’, predominantly aerobic exercise, the other subtype only responds to higher and concurrently noxious levels of metabolites present in muscle during ischaemic contractions or following, for example, hypertonic saline infusions. This review discusses the mechanisms through which group III/IV muscle afferent feedback mediates both central and peripheral fatigue in exercising humans. We also briefly summarize accumulating evidence from recent animal and human studies documenting the existence of two subtypes of group III/IV muscle afferents and the relevance of this discovery for the interpretation of previous work and the design of future studies.

Towards a three-dimensional framework of centrally regulated and goal-directed exercise behaviour: a narrative review

“…In contrast, pain signals and information from metaboreceptors and mechanoreceptors as well as the autonomic nervous system are conveyed by unmyelinated type III and IV fibres and are somatotopically organised in an anterior to posterior manner in nuclei of the thalamus and insular cortex (IC) 35 95. The function of these separable type III and IV somatosensory afferents appears to be to reflexively increase autonomic responses facilitating exercise97 but also to limit intramuscular metabolic disturbance via alteration of spinal motor neurons eventually contributing to central fatigue 98 99…”

Relationship between motor corticospinal excitability and ventilatory response during intense exercise

“…Thus, it is reasonable to consider that any suggestion of a purely cortical involvement is unsupported in the previous study by Sidhu et al (2012). On the other hand, Group III/IV muscle afferent feedback associated with intramuscular metabolic perturbation has been suggested to have an inhibitory effect on the central nervous system (i.e., central fatigue), limiting the output of spinal motoneurons during exhaustive locomotor exercise (Amann et al 2013;Amann et al 2015;Hilty et al 2011;Sidhu et al 2014). Moreover, it has been suggested that decrease in the output from spinal motoneurons is attributed to the inhibitory effect of group III/IV muscle afferents on voluntary descending drive 'upstream' of the motor cortex (Taylor et al, 2006) and/or an afferent-mediated depression of excitability of the corticospinal tract (Hilty et al 2011, Martin et al 2006Martin et al 2008, Sidhu et al 2014.…”

“…Recent studies have suggested that group III/IV muscle afferents originating in exercising muscle play an important role in the development of fatigue during exercise [for review see (Amann et al 2015)]. …”

Sympathetic control of reflex cutaneous vasoconstriction in human aging

“…Alterations in the skin afferent signals mediating reflex cutaneous vasoconstriction during cold stress are methodologically challenging to precisely quantify in humans, because there are few experimental approaches to reduce, or abolish, sensory feedback. The role of muscle afferent sensory fibers in eliciting the neurocardiovascular responses to exercise have been probed using lumbar intrathecal fentanyl to block the central project of -opioid-receptor sensitive group III/IV fibers during lower limb dynamic exercise (1,37); however, this highly invasive experimental paradigm has not yet been used to examine thermosensitive afferent fibers.…”