Respiratory and cardiac modulation of single sympathetic vasoconstrictor and sudomotor neurones to human skin

Abstract

1. The firing of single sympathetic neurones was recorded via tungsten microelectrodes in cutaneous fascicles of the peroneal nerve in awake humans. Studies were made of 17 vasoconstrictor neurones during cold-induced cutaneous vasoconstriction and eight sudomotor neurones during heat-induced sweating. Oligounitary recordings were obtained from 8 cutaneous vasconstrictor and 10 sudomotor sites. Skin blood flow was measured by laser Doppler flowmetry, and sweating by changes in skin electrical resistance within the innervation territory on the dorsum of the foot. 2. Perispike time histograms revealed respiratory modulation in 11 (65 %) vasoconstrictor and 4 (50 %) sudomotor neurones. After correcting for estimated conduction delays, the firing probability was higher in inspiration for both classes of neurone. Measured from the oligounitary recordings, the respiratory modulation indices were 67. 7 +/- 3.9 % for vasoconstrictor and 73.5 +/- 5.7 % for sudomotor neurones (means +/- s.e.m.). As previously found for sudomotor neurones, cardiac rhythmicity was expressed by 7 (41 %) vasoconstrictor neurones, 5 of which showed no significant coupling to respiration. Measured from the oligounitary records, the cardiac modulation of cutaneous vasoconstrictor activity was 58.6 +/- 4.9 %, compared with 74.4 +/- 6.4 % for sudomotor activity. 3. Both vasoconstrictor and sudomotor neurones displayed low average firing rates (0.53 and 0.62 Hz, respectively). The percentage of cardiac intervals in which units fired was 38 % and 35 %, respectively. Moreover, when considering only those cardiac intervals when a unit fired, vasoconstrictor and sudomotor neurones generated a single spike 66 % and 67 % of the time. Rarely were more than four spikes generated by a single neurone. 4. We conclude that human cutaneous vasoconstrictor and sudomotor neurones share several properties: both classes contain subpopulations that are modulated by respiration and/or the cardiac cycle. The data suggest that the intensity of a multi-unit burst of vasoconstrictor or sudomotor impulses is probably governed primarily by firing incidence and the recruitment of additional neurones, rather than by an increase in the number of spikes each unit contributes to a burst.

Figure 1. Variation of spike amplitude in single unit recordings

Histograms showing the distributions of spike amplitude and of the underlying noise for two cutaneous vasoconstrictor units. For each unit the variances of the noise and spike amplitudes were not significantly different, indicating that variations in the signal can be accounted for by variations in the noise.

Figure 2. Recording from a single cutaneous vasoconstrictor neurone in the cold state

A, five spikes (asterisks) occurring spontaneously. Skin blood flow and spontaneous changes in skin electrical resistance (indicative of sweating) were negligible. B, the unit generated two spikes following an arousal stimulus, associated with a decrease in skin resistance (upward deflection) (due to coactivation of sudomotor neurones) but no further reduction in skin blood flow. C, superimposed spikes from A and B suggest that they were recorded from a single axon.

Figure 3. Distribution of firing rates for all cutaneous vasoconstrictor neurones

A, pooled data from 17 cutaneous vasoconstrictor neurones. * Short intervals from unit firing doublets. Note break of the y-axis. B, number of sympathetic bursts in which a unit fired one or more spikes.

Figure 4. Multiple firing in cutaneous vasoconstrictor neurones

A and C, examples from two units in which multiple spikes were generated in a sympathetic burst. B and D, superimposed spikes from the left panels demonstrating the reproducibility of shapes, suggesting that the respective spikes in each panel derived from a single neurone.

Figure 5. Respiratory rhythmicity in single cutaneous vasoconstrictor neurones

Perispike time histograms showing the distribution of spikes with respect to the peak of inspiration and corresponding diagram showing the time of occurrence of inspiratory peaks. Each unit exhibited temporal coupling to the respiratory cycle.

Figure 6. Cardiac rhythmicity in cutaneous vasoconstrictor neurones

Perispike time histograms showing the distribution of spikes with respect to the R-wave of the ECG and corresponding diagram showing the time of occurrence of R-waves.

Figure 7. Respiratory and cardiac rhythmicity in oligounitary vasoconstrictor recordings

Respiratory (A and B) and cardiac (C and D) rhythmicity in two oligounitary cutaneous vasoconstrictor recordings. Same format as in Figs 5 and 6

Figure 8. Respiratory rhythmicity in single sudomotor neurones

Perispike time histogram between unit firing and the peak of inspiration and corresponding diagrams showing the time of occurrence of subsequent inspiratory peaks. Data from four sudomotor neurones reanalysed from Macefield & Wallin (1996).

Figure 9. Respiratory and cardiac rhythmicity in oligounitary sudomotor recordings

Respiratory rhythmicity (A and B) and cardiac rhythmicity (C and D) in two oligounitary recording sites. Same format as in Fig. 7.