Cutaneous warmth, but not touch, increases muscle sympathetic nerve activity during a muscle fatigue hand-grip task

Abstract

In homeostasis, somatosensory C fibre afferents are hypothesised to mediate input to the brain about interactions with external stimuli and sympathetic efference provides the output that regulates bodily functions. We aimed to test this hypothesis and whether different types of innocuous somatosensory input have differential effects. Healthy volunteers performed a muscle fatigue (hand-grip) task to exhaustion, which produces increased muscle sympathetic nerve activity (MSNA), as measured through microneurography. Participants completed the muscle fatigue task without concurrent cutaneous sensory stimulation (control) or we applied skin warming (heat pack) as a C fibre stimulation, slow brush stroking as C and Aβ fibre stimulation, or vibration as Aβ fibre stimulation, to the participant's forearm. We also measured heart rate, the duration of the hand-grip task, and ratings of pain at the end of the task. Concurrent skin warming showed increased MSNA compared to the other conditions. Tactile stimuli (brushing, vibration) were not significantly different to the control (no intervention) condition. Warming increased the pain from the muscle contraction, whereas the tactile stimuli did not. We interpret the effect of warming on MSNA as providing relevant afferent information during muscle contraction, which needed to be counteracted via vasoconstriction to maintain homeostasis. Brushing and vibration were less homeostatically relevant stimuli for the muscle contraction and hence had no significant effect. The findings add sensory specificity to our current understanding of homeostatic regulation through somatosensory afferent and sympathetic efferent pathways.

Keywords: C-fibre; Homeostasis; MSNA; Touch; Vibration; Warmth.

Fig. 1

Examples of integrated MSNA, ECG, and heart rate. 30 s of continuous recordings from near the end of the task for integrated muscle sympathetic nerve activity (MSNA), electrocardiography (ECG), and heart rate (HR) in beats per minute (bpm) from four experiments, during (from left-to-right) rest (baseline), hand-grip only, and hand-grip with concurrent warmth, brushing, or vibration applied to the forearm. The data are from participant CB971121 (top row; rest, control, vibration), participant F07030 (top row; warmth, brush), participant ES071105 (bottom row; rest, brush, vibration) and participant AN100423 (bottom row; control, warmth)

Fig. 2

End-point MSNA responses to evoked muscle pain over the conditions. Microneurographic recordings of muscle sympathetic activity showing the normalised mean sympathetic a burst frequency, b burst incidence and c burst area. The responses were taken in the last minute of the hand-grip task for each participant and normalised to each participant’s pre-task resting baselines (100%). There was a significant increase in all of the MSNA measures over the conditions, as compared to the resting baseline (all p < 0.001). The significances shown indicate the between-condition effects from the separate measures (*p < 0.05, **p < 0.01). Error bars are +SEM

Fig. 3

Heart rate, duration of hand-grip and end-point pain ratings over the conditions. a Normalised mean heart rate was taken in the last minute of the hand-grip task for each participant and normalised to each participant’s pre-task resting baselines (100%). There was a significant increase in heart rate over all of the conditions, as compared to the resting baseline (all p < 0.001), but not between-condition effects. b Mean pain ratings on a visual analogue scale ranging from 0 to 100 obtained at the end of each condition. There was a significant effect of condition on the pain ratings and between-condition significances are shown (*p < 0.05, **p < 0.01). Error bars are +SEM. c Mean hand-grip duration showed no significant effect of condition on the task duration (participants were instructed to continue to grip until exhaustion)