Respiratory response to passive limb movement is suppressed by a cognitive task

Abstract

Bell, Harold J., and James Duffin. Respiratory response to passive limb movement is suppressed by a cognitive task. J Appl Physiol 97: 2112-2120, 2004. First published July 23, 2004 doi: 10.1152/japplphysiol.00302.2004.-Feedback from muscles stimulates ventilation at the onset of passive movement. We hypothesized that central neural activity via a cognitive task source would interact with afferent feedback, and we tested this hypothesis by examining the fast changes in ventilation at the transition from rest to passive leg movement, under two conditions: 1) no task and 2) solving a computer-based puzzle. Resting breathing was greater in condition 2 than in condition 1, evidenced by an increase in mean Ϯ SE breathing frequency (18.2 Ϯ 1.1 vs. 15.0 Ϯ 1.2 breaths/min, P ϭ 0.004) and ventilation (10.93 Ϯ 1.16 vs. 9.11 Ϯ 1.17 l/min, P Ͻ 0.001). In condition 1, the onset of passive movement produced a fast increase in mean Ϯ SE breathing frequency (change of 2.9 Ϯ 0.4 breaths/min, P Ͻ 0.001), tidal volume (change of 233 Ϯ 95 ml, P Ͻ 0.001), and ventilation (change of 6.00 Ϯ 1.76 l/min, P Ͻ 0.001). However, in condition 2, the onset of passive movement only produced a fast increase in mean Ϯ SE breathing frequency (change of 1.3 Ϯ 0.4 breaths/min, P ϭ 0.045), significantly smaller than in condition 1 (P ϭ 0.007). These findings provide evidence for an interaction between central neural cognitive activity and the afferent feedback mechanism, and we conclude that the performance of a cognitive task suppresses the respiratory response to passive movement. exercise hyperpnea; wakefulness drive; afferent feedback AT THE ONSET OF EXERCISE, ventilation (V E) increases immediately (25), and the rapid onset of this drive to breathe has led to it being assigned a neural origin, since it is too fast for a humoral source (15,26). This "exercise drive to breathing" is hypothesized to result from two sources: one is "peripheral neurogenic drive," whereby afferent feedback from the exercising limbs leads to increased respiration (21); the other is "central command," whereby motor commands to the limbs initiate a parallel activation of respiration (17,49).In the integrated system, both of these mechanisms are initiated simultaneously; therefore, any interaction between them could affect their respective contributions toward the control of breathing. Indeed, animal model studies have provided evidence of interactions between central motor commands and afferent feedback (2, 13, 37). Such findings support the idea that, at the onset of exercise, neural drives to breathe via distinct mechanisms are incorporated to provide the drive to breathe that is observed in the integrated system.The onset of exercise also involves an increase in central neural activity via cortical brain activity (23, 32) that is not solely related to the motor outflow to the muscles itself. For example, during imagined exercise where both central motor command and afferent feedback mechanisms are absent, significant increases in cortical activity occur and this act...

Central and peripheral hemodynamic responses to passive limb movement: the role of arousal

“…Therefore, monitoring this particular response in people with a SCI during passive movement provides an index of the magnitude of arousal. Indeed, in an elegant study, Bell et al (4) revealed that, in intact humans, afferent feedback from the muscle bed stimulates V E at the onset of passive movement. Interestingly, when a cognitive task was superimposed on the passive movement, the V E response was inactivated, indicating that arousal, and not solely afferent feedback, plays a role in this ventilatory response.…”

“…Indeed, recent research in this area has revealed neural networks in the brain that are involved in centrally mediated cardiovascular activation, which do not appear to require parallel motor activation (21) and thus could play a role in the cardiovascular response to passive movement. However, it is currently not clear if "arousal," defined as an increase in brain activity independent of motor command (4), at the onset of passive movement influences movement-induced central and peripheral hemodynamic responses.…”

Coordination of Breathing with Nonrespiratory Activities

“…Moreover, the entraining influences (whatever they may be in a particular setting) are influenced by cortical activity. For example, completing a mental puzzle reduced dependence of respiratory frequency on the frequency of limb movements (24). This implies that there is some competition among the wide variety of inputs that may affect the respiratory controller so that afferent sensory information from passive leg movement may or may not alter respiratory frequency, depending on the state of the cortical inputs.…”

The respiratory response to passive and active arm movements is enhanced in delayed onset muscle soreness

“…As another possibility, it has been suggested that an arousal response mediated by the limbic system could contribute to the ventilatory response at the onset of exercise (Bell and Duffin 2004;Bell et al 2005;Bell 2006). DOMS sensation and/or discomfort from it during VOL and PAS might have heightened the arousal response at D2.…”

“…It has been established that initial exercise hyperpnea is altered by several factors, such as the modality of exercise (Kelsey and Duffin 1992;Miyamura et al 1992), participation in sports (Sato et al 2004), age (Ishida et al 2000), performing a cognitive task simultaneously (Bell and Duffin 2004;Bell et al 2005), and differences between exercising limbs (Ishida et al 1994). Recently, we also reported that ventilatory response (though not heart rate or blood pressure) at the onset of light leg exercise is enhanced in sore or tender muscles 2 days after eccentric exercise (ECC), in what we call delayed onset muscle soreness (DOMS), relative to that before ECC (Hotta et al 2006(Hotta et al , 2007.…”