Interindividual differences in sympathetic and effector responses to arousal in humans

Abstract

Surprising sensory stimuli have been found to attenuate one or two sympathetic discharges in human muscle nerves of some, but not all subjects, an effect suggested to be due to arousal. The aims of the present study were: (1) to provide evidence for or against an arousal mechanism by searching for evidence of habituation, and (2) to investigate if the presence or absence of inhibitory response is reproducible. To this end we recorded peroneal muscle sympathetic nerve activity (MSNA), electrocardiogram (ECG), finger blood pressure and changes of skin electrical resistance in 17 awake healthy subjects, while sensory stimuli consisting of five electrical pulses were delivered to a finger. The electrical pulses were triggered on five consecutive R waves of the ECG after a delay of 200 ms. Dummy stimuli, consisting of five trigger pulses without electrical pulses were used as controls, and the interval between two successive stimuli (real or dummy) was 30 s. On a group basis, the stimuli attenuated two initial and one late MSNA bursts. On an individual basis, significant attenuation of one or two initial bursts occurred in eight subjects, whereas in nine subjects there was no significant inhibition. In nine subjects the experiments were repeated once and in three subjects they were repeated twice. The effects on MSNA were reproducible in 11 of the12 subjects. In the group of subjects without significant MSNA inhibition the stimuli induced a small, transient increase in mean blood pressure, which was not present in the group with significant MSNA inhibition. Heart rate did not change in either group. In conclusion, the inhibitory effect on MSNA of five repeated electrical pulses to a finger is largely similar to that previously shown for one pulse, i.e. there is rapid habituation of the response, compatible with an arousal-induced effect. The inhibitory responsiveness shows marked interindividual differences, which are reproducible over several months and associated with different effects on blood pressure.

Figure 1. Relationship between sympathetic bursts, cardiovascular parameters and stimulus

Definitions and terminology for the relationship between mean voltage neurogram, cardiovascular parameters and electrical stimulus consisting of five repeated square wave pulses triggered with a delay of 200 ms from the R wave of the ECG (note stimulus artefacts in mean voltage neurogram). Pulses 1–5 delivered in cardiac intervals 1–5 (CI 1-5). Baroreflex latency defined as time from R wave 1 of the ECG (R1) to peak of burst 1 in mean voltage neurogram, i.e. bursts 1–5 are terminated by the afferent baroreceptor discharges induced by the systolic pressure waves occurring in CI 2-6.

Figure 2. Artefact elimination

Technique for removal of artefacts induced by the electrical pulses. Upper left trace, mean voltage neurogram distorted by artefacts from five pulses. Average artefact (upper right trace) was obtained from sections of the neurogram without bursts (as in association with pulse 2). Lower trace, the same mean voltage neurogram after subtraction of averaged artefact.

Figure 3. Stimulus-induced effects of MSNA in two subjects

Examples of subjects (A and B corresponding to nos 2 and 12, respectively, in Table 2) showing amplitude reduction of burst 1 (A) or 0 and 1 (B) in the averaged mean voltage neurograms. Results of dummy and real stimuli shown by dashed and continuous lines, respectively. Note good agreement in all recordings between control bursts in records from dummy and real stimuli, and also similarity between inhibitory effects in first and second recordings.

Figure 4. Stimulus-induced cardiovascular effects

Average effects of five electrical pulses on burst amplitude, mean blood pressure and cardiac interval in all subjects with (A) or without (B) significant inhibition of burst 0 or 1 (or both) in first recording. All values expressed as percentages of mean values in bursts or cardiac intervals −4 to −2. *P < 0.05.

Figure 5. Comparison of stimulus-induced responses in repeated recordings

Relationship between degree of inhibition in subjects in whom repeated recordings were made. ○, comparison of first and second recordings; □, comparison of second (abscissa) and third (ordinate) recordings. Filled symbols indicate subjects in whom the amplitude reduction of burst 0 and/or 1 was statistically significant in both recordings. Amplitude reduction is expressed as percentage of mean amplitude of bursts −4 to −2 preceding the stimuli. The continuous line is the regression line and the dashed line is the line of identity.