Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans

Abstract

We investigated the role of somatosensory feedback on cardioventilatory responses to rhythmic exercise in five men. In a double-blind, placebo-controlled design, subjects performed the same leg cycling exercise (50/100/150/325 ± 19 W, 3 min each) under placebo conditions (interspinous saline, L(3)-L(4)) and with lumbar intrathecal fentanyl impairing central projection of spinal opioid receptor-sensitive muscle afferents. Quadriceps strength was similar before and after fentanyl administration. To evaluate whether a cephalad migration of fentanyl affected cardioventilatory control centers in the brain stem, we compared resting ventilatory responses to hypercapnia (HCVR) and cardioventilatory responses to arm vs. leg cycling exercise after each injection. Similar HCVR and minor effects of fentanyl on cardioventilatory responses to arm exercise excluded direct medullary effects of fentanyl. Central command during leg exercise was estimated via quadriceps electromyogram. No differences between conditions were found in resting heart rate (HR), ventilation [minute ventilation (VE)], or mean arterial pressure (MAP). Quadriceps electromyogram, O(2) consumption (VO(2)), and plasma lactate were similar in both conditions at the four steady-state workloads. Compared with placebo, a substantial hypoventilation during fentanyl exercise was indicated by the 8-17% reduction in VE/CO(2) production (VCO(2)) secondary to a reduced breathing frequency, leading to average increases of 4-7 Torr in end-tidal PCO(2) (P < 0.001) and a reduced hemoglobin saturation (-3 ± 1%; P < 0.05) at the heaviest workload (∼90% maximal VO(2)) with fentanyl. HR was reduced 2-8%, MAP 8-13%, and ratings of perceived exertion by 13% during fentanyl vs. placebo exercise (P < 0.05). These findings demonstrate the essential contribution of muscle afferent feedback to the ventilatory, cardiovascular, and perceptual responses to rhythmic exercise in humans, even in the presence of unaltered contributions from other major inputs to cardioventilatory control.

Ponto ótimo cardiorrespiratório: uma variável submáxima do teste cardiopulmonar de exercício

“…In younger individuals, the pulmonary capillary recruitment probably occurs with greater efficiency, allowing an expansion of the so-called West zone III to the region of zones I and II, maintaining a more appropriate V/Q ratio 33 . It should be noted that the increased ventilation in exercise is not only related to the CO2 concentration, but also with afferent stimuli from the mechanoreceptors 34,35 . Evidence of that is data from Araujo and Monteiro 36 indicating that there are substantial differences in the VE and also in VE/VO2, with probably different afferent stimuli, when an individual walks or runs for the same velocity on the treadmill.…”

Mental processes and breathing during exercise

“…Therefore, although hyperventilation during heavy exercise is related to perception of effort, it may be an event independent of the traditional model of 'central command' that drives breathing via parallel activation of motor and respiratory centers. Thus, these recent studies [44][45][46][47][48]54,55) collectively emphasize the importance of a cognitive process such as perception of effort in respiratory regulation during heavy exercise. However, the formation mechanism of effort sense during heavy exercise and the role of effort sense in ventilatory control are still not clear 61) .…”

“…For instance, an essential role for muscle afferent feedback in respiratory regulation has been suggested by the observation that blocking somatosensory feedback by fentanyl injection caused hypoventilation during a cycling time trial 44) . Furthermore, using a similar pharmacological method, Amann et al 45) demonstrated that blocking somatosensory feedback substantially attenuated the ventilatory and also perceptual responses to heavy exercise. These findings by Amann et al 44,45) raise the possibility that input of groups III and IV muscle afferents contributes to the central motor command driving respiration during exercise 46) .…”

“…Furthermore, using a similar pharmacological method, Amann et al 45) demonstrated that blocking somatosensory feedback substantially attenuated the ventilatory and also perceptual responses to heavy exercise. These findings by Amann et al 44,45) raise the possibility that input of groups III and IV muscle afferents contributes to the central motor command driving respiration during exercise 46) . In contrast, Marcora et al 47) demonstrated that muscle fatigue per se enhances ventilatory response during heavy exercise, independent of metabolic stress, and they 47,48) argued that ventilatory response during exercise is mediated by the perception of effort, which is derived from corollary discharge [49][50][51] of central motor command, independent of peripheral signals.…”

Role of feedback from Group III and IV muscle afferents in perception of effort, muscle pain, and discomfort

“…TO THE EDITOR: In their recent paper, Amann and colleagues (1) report an experiment in which they used a powerful analgesic, fentanyl, to block afferent feedback from Group III and IV neurons innervating the locomotor muscles. The authors investigated the effects of this experimental treatment on various physiological and perceptual responses to cycling exercise at different power outputs.…”