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 ischemic 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 the 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 to the interpretation of previous work and the design of future studies.

Keywords: Central fatigue; Circulation; Exercise pressor reflex; Neural feedback; Ventilation.

Figure 1

Discharge frequency [impulses per 2 seconds; (Imp/2 s)] of group III (panel A) and group IV (panel B) muscle afferents recorded from dorsal root before, during, and after locomotor exercise evoked by electrical stimulation of the mesencephalic locomotor region in decerebrate cats. The horizontal bar denotes the exercise period. Note the immediate increase of both group III and IV locomotor muscle afferent discharge at the onset of exercise and the maintained response until the exercise is terminated. From Adreani et al. (1).

Figure 2

Reduction in quadriceps maximal voluntary contraction strength (MVC) induced via 9 minutes of constant-load single leg knee-extensor exercise (25/50/80% of peak workload, 3 min each) in patients with chronic heart failure. The exercise was performed with intact (Control) and blocked (Fentanyl) neural feedback from the lower limb. From Amann et al. (12).