Central vs. peripheral determinants of sympathetic neural recruitment: insights from static handgrip exercise and postexercise circulatory occlusion

Abstract

Sympathetic outflow is modified during acute homeostatic stress through increased firing of low-threshold axons, recruitment of latent axons, and synaptic delay modifications. However, the role of central mechanisms versus peripheral reflex control over sympathetic recruitment remains unknown. Here, we examined sympathetic discharge patterns during fatiguing static handgrip (SHG) exercise and postexercise circulatory occlusion (PECO) to study the central vs. peripheral reflex elements of sympathetic neural coding. Muscle sympathetic nerve activity (MSNA; microneurography) was measured in six males (25 ± 3 yr) at baseline (3 min) and during 5 min of SHG exercise completed at 20% maximal voluntary contraction. Isolation of the peripheral metaboreflex component was achieved by PECO for 3 min. Action potential (AP) patterns were studied using wavelet-based methodology. Compared with baseline, total MSNA increased by minute 3 of SHG, remaining elevated throughout the duration of exercise and PECO (all P < 0.05). The AP content per burst increased above baseline by minute 4 of SHG (Δ4 ± 2), remaining elevated at minute 5 (Δ6 ± 4) and PECO (Δ4 ± 4; all P < 0.05). Similarly, total AP clusters increased by minute 4 of SHG (Δ5 ± 5) and remained elevated at minute 5 (Δ6 ± 3) and PECO (Δ7 ± 5; all P < 0.01), indicating recruitment of latent subpopulations. Finally, the AP cluster size-latency profile was shifted downward during minutes 4 (-32 ± 22 ms) and 5 (-49 ± 17 ms; both P < 0.05) of SHG but was not different than baseline during PECO (P > 0.05). Our findings suggest that central perceptual factors play a specific role in the synaptic delay aspect of sympathetic discharge timing, whereas peripheral reflex mechanisms affect recruitment of latent axons.

Keywords: action potential; exercise pressor reflex; metaboreflex; microneurography; sympathetic nerve activity.

Fig. 1.

Representative sample of data collected from 1 subject at baseline (BSL) and during static handgrip exercise and postexercise circulatory occlusion (PECO). HR, heart rate; BP, blood pressure; MSNA, muscle sympathetic nerve activity; AP, action potential. *Denotes noise spikes not included in analysis.

Fig. 2.

Hemodynamic responses to static handgrip (HG) exercise and postexercise circulatory occlusion (PECO). Dashed lines represent individual data. Values are means ± SD. MAP, mean arterial pressure; HR, heart rate; SV, stroke volume; CO, cardiac output; TPR, total peripheral resistance. *P < 0.05, significantly different from baseline (BSL).

Fig. 3.

Integrated muscle sympathetic nerve activity (MSNA) responses to static handgrip (HG) exercise and postexercise circulatory occlusion (PECO). Dashed lines represent individual data. Values are means ± SD. AU, arbitrary units; hb, heartbeats. *P < 0.05, significantly different from baseline (BSL).

Fig. 4.

Sympathetic action potential (AP) responses to static handgrip (HG) exercise and postexercise circulatory occlusion (PECO). Dashed lines represent individual data. Values are means ± SD. *P < 0.05, significantly different from baseline (BSL).

Fig. 5.

Action potential (AP) cluster latency as a function of AP cluster size at baseline (BSL), minutes 1-5 of static handgrip (HG), and postexercise circulatory occlusion (PECO). No significant upward or downward shift was seen in the AP cluster size-latency profile during HG1 (range −14 to 36 ms; range represents individual data), HG2 (range −18 to 35 ms), or HG3 (range −53 to 10 ms), whereas a significant downward shift in the profile was observed during HG4 (range 4 to −136 ms) and HG5 (range −9 to −198 ms). Finally, no significant upward or downward shift was seen during PECO (range −28 to 22 ms). *P < 0.05, significantly different from BSL.