Sympathetic neural recruitment strategies: responses to severe chemoreflex and baroreflex stress

Abstract

This study tested the hypothesis that neural coding patterns exist within the autonomic nervous system. We investigated sympathetic axonal recruitment strategies in humans during chemoreflex- and baroreflex-mediated sympathoexcitation using a novel action potential (AP) analysis technique. Muscle sympathetic nerve activity (microneurography) was collected in 11 young individuals (6 females) during baseline and two subsequent protocols: 1) severe chemoreflex stimulation (maximal end-inspiratory apnea following rebreathe), and 2) severe baroreceptor unloading (-80 mmHg lower body negative pressure; LBNP). When compared with each respective baseline, apnea and LBNP increased AP frequency and mean AP content per sympathetic burst (all P < 0.01). When APs were binned according to peak-to-peak amplitude (i.e., into "clusters"), total clusters detected increased during both apnea (Δ7 ± 5; P = 0.0009) and LBNP (Δ11 ± 8; P = 0.0012) compared with baseline. This was concomitant to an increased number of active clusters per burst during apnea (Δ3 ± 1; P < 0.0001) and LBNP (Δ3 ± 3; P = 0.0076). At baseline and during apnea (R(2) = 0.98; P < 0.0001) and LBNP (R(2) = 0.95; P < 0.0001), a pattern emerged whereby AP cluster latency decreased as cluster size increased. Furthermore, the AP cluster latency profile was shifted downward during apnea (∼53 ms) and upward during LBNP (∼31 ms). The data indicate that variations in synaptic delays and latent subpopulations of larger axons exist as recruitment strategies for sympathetic outflow. The synaptic delay component appears to express reflex specificity, whereas latent subpopulation recruitment demonstrates sensitivity to stress severity.

Keywords: action potential detection; baroreflex; chemoreflex; muscle sympathetic nerve activity; sympathetic neural recruitment patterns.

Fig. 1.

Schematic representation of action potential (AP) detection and classification. MSNA, muscle sympathetic nerve activity.

Fig. 2.

Representative sample of data from one subject collected at baseline, during rebreathe, maximal end-inspiratory apnea, and recovery.

Fig. 3.

Total detected clusters (A) and active clusters/burst (B) at baseline and during maximal end-inspiratory apnea. *Significantly different from baseline, P < 0.001.

Fig. 4.

Histogram representing AP content as a function of normalized cluster number at baseline and during maximal end-inspiratory apnea.

Fig. 5.

Mean action potential cluster latency across participants as a function of normalized cluster number at baseline and during maximal end-inspiratory apnea. Sample size for clusters in which not all 11 subjects are included are indicated in parentheses. Sample sizes <11 at baseline represent subjects in whom these clusters were not present at baseline but were recruited during apnea.

Fig. 6.

Representative sample of data from one subject collected at baseline and during −80 mmHg lower body negative pressure (LBNP) and recovery.

Fig. 7.

Total detected clusters (A) and active clusters/burst (B) at baseline and during −80 mmHg LBNP. *Signficantly different from baseline, P < 0.01.

Fig. 8.

Histogram representing AP content as a function of normalized cluster number at baseline and −80 mmHg LBNP.

Fig. 9.

Mean action potential cluster latency across participants as a function of normalized cluster number at baseline and −80 mmHg LBNP. Sample size for clusters in which not all 11 subjects are included are indicated in parentheses. Sample sizes <11 at baseline represent subjects in whom these clusters were not present at baseline but were recruited during LBNP.