Inhibition of human muscle sympathetic activity by sensory stimulation

Abstract

Surprising sensory stimuli causing arousal are known to evoke short‐lasting activation of human sympathetic activity in skin but not in muscle nerves; anecdotal observations suggest that there may even be an inhibition of muscle sympathetic nerve activity (MSNA). To test this hypothesis we recorded multiunit MSNA in the peroneal nerve in 19 subjects aged 19–71 years, while sensory stimuli, consisting of either an electrical skin stimulus to a finger or a visual flash, were delivered repeatedly with intervals of approximately 20 s. The stimuli were given either 200 or 400 ms after the R wave of the electrocardiogram. Dummy stimuli, consisting of trigger pulses without sensory stimulation served as controls. Electrical skin resistance reductions were monitored from the palm of a hand as electrodermal signs of arousal‐induced cutaneous sympathetic activity. On a group basis both types of sensory stimuli attenuated the amplitude of one or two bursts of MSNA, while no such effects occurred after dummy stimuli. Individually, the inhibition was evoked by at least one stimulus modality or delay in 16 subjects whereas in three subjects no significant inhibition occurred. Skin resistance responses were evoked in all subjects. Some subjects responded to one, others to both stimulus modalities, and electrical stimuli were more effective than visual stimuli in causing MSNA inhibition as well as skin resistance reduction. On the other hand, electrodermal signs of arousal were equally common in subjects with and without inhibitory responses. We suggest that the MSNA inhibition evoked by sensory stimuli is an arousal effect which varies markedly between individuals.

Sympathetic nerve and cardiovascular responses to auditory startle and prepulse inhibition

“…While eyeblink and limb-withdrawal reflexes are effected through simple and fast reflex pathways, previous studies of MSNA have observed that the onset latency of the inhibition can occur as long as 2 s (i.e., at burst 1) after sensory stimulation depending on the phase relationship between the stimulus and cardiac cycle it was delivered in. Electrical skin stimulation (Donadio et al, 2002a) and transcranial magnetic stimulation (Macefield et al, 1998), delivered at 200 ms latencies from the R-wave, produced MSNA inhibition at burst 0, similar to our findings. But when these stimuli were delivered at a latency of 400 ms, the inhibition often occurred in burst 1, with burst 0 unaffected.…”

“…In the skeletal muscle vasculature on the other hand, sudden somatosensory stimulation induces an immediate and short-lasting inhibition of MSNA in many healthy subjects. This inhibition was most marked when stimuli were applied 200 to 400 ms after the R-wave of the ECG (Donadio et al, 2002a) and was reproducible in repeated recordings with several months interval (Donadio et al, 2002b).…”

Cutaneous Mechanoreceptor Feedback from the Hand and Foot Can Modulate Muscle Sympathetic Nerve Activity

“…Prior investigations have relied primarily on non-noxious electrical cutaneous stimulation to test the influence of cutaneous mechanoreceptor afferent feedback on blood pressure and muscle sympathetic nerve activity (MSNA). These studies demonstrate the capacity of electrical stimuli to modulate mean arterial pressure and/or MSNA (Hollman and Morgan, 1997; Donadio et al, 2002a,b; Gray et al, 2009; Labrunée et al, 2013), as well as highlight the central integration of somatosensory and baroreceptor inputs (Gray et al, 2009). However, the interpretation of results is limited by the observation that electrical stimulation can evoke arousal responses that also modulate efferent peripheral sympathetic activity in a similar manner as flashing light (i.e., not dependent on cutaneous mechanoreceptor afferent activity; Donadio et al, 2002a).…”

“…These studies demonstrate the capacity of electrical stimuli to modulate mean arterial pressure and/or MSNA (Hollman and Morgan, 1997; Donadio et al, 2002a,b; Gray et al, 2009; Labrunée et al, 2013), as well as highlight the central integration of somatosensory and baroreceptor inputs (Gray et al, 2009). However, the interpretation of results is limited by the observation that electrical stimulation can evoke arousal responses that also modulate efferent peripheral sympathetic activity in a similar manner as flashing light (i.e., not dependent on cutaneous mechanoreceptor afferent activity; Donadio et al, 2002a). Cutaneous electrical stimulation can also activate muscle (Goswami et al, 2012) and pain (Nordin and Fagius, 1995) afferents, limiting its use as a tool to understand the selective influence of low threshold mechanoreceptor feedback on cardiovascular control.…”

Forebrain organization representing baroreceptor gating of somatosensory afferents within the cortical autonomic network

“…Specifically, afferent input from arterial baroreceptors is a powerful modulator of the excitatory cardiovascular response evoked by skeletal muscle afferents during muscle contractions (Potts and Li 1998). Furthermore, somatosensory stimuli delivered 200 -400 ms after the R wave of the cardiac cycle inhibits MSNA, whereas no change in MSNA is observed with delivery synchronous with the electrocardiogram (ECG)-R wave (Donadio et al 2002). Thus, ongoing feedback from baroreflex activity plays an important role in the integration of somatosensory stimuli and the resultant effects on autonomic control of cardiovascular function.…”