CVS Oscillatory Reactions to RSMT Stimulation at Different Frequencies
The present results indicate that RSMT stimulation elicits oscillations in RRI, PTT, FPA, SC, and RV at all tested frequencies. The amplitude of the oscillations in these functions (spectral power indices), except for RV, significantly depended on the stimulation frequency. RRI and PTT revealed the strongest reaction to 0.1 Hz RSMT stimulation, while FPA and SC response to RSMT was higher for the lower stimulation frequency ().The strongest RRI reaction was in response to 0.1 Hz stimulation, however large individual differences in RRI reactions to various frequency stimulations were observed (), likely reflecting individual differences in baroreflex activity (in the baroreflex gain). Significantly higher RRI response to RSMT at 0.1 Hz than to RSMT at 0.2 or 0.05 Hz appears to be an indicant of the 0.1 Hz resonance in the CVS that is produced by HR - BP interaction in the HR baroreflex closed-loop. This suggests that 0.1 Hz RSMT stimulation triggered resonance in the HR baroreflex closed-loop. Although BP was not assessed in this study, it has previously been shown that 0.1 Hz RSMT elicits high amplitude oscillation in BP, as well as in HR (Lehrer et al., 2009
The dynamics of the PTT oscillations were close to the dynamics of the RRI oscillations, presumably because the same BP oscillation was circulating in both the HR and VT baroreflex closed-loops. We assume that BP oscillation caused forced PTT oscillation in the VT baroreflex closed-loop. FPA, SC, and RV did not react to 0.1 Hz RSMT stimulation stronger than to the other frequencies of RSMT stimulation, likely because they do not relate directly to the HR baroreflex closed-loop. RRI and PTT reflect the dynamics of central cardiovascular processes, whereas FPA and SC are more related to peripheral hemodynamics (Zahedy et al., 2008). We propose that RSMT, as a rhythmical physical load, induced forced oscillation in FPA, SC and RV mechanically and through reflexes, controlling these functions. It is possible that closed-loops of these reflexes also have resonance properties that amplify FPA, SC, and RV oscillations, however their resonance frequencies would be considerably lower or higher than the frequencies tested in the present study.
Gender differences were found only in RRI and FPA reactions. RRI and FPA oscillatory responses to RSMT were significantly higher in men than in women, while PTT, SC, and RV oscillatory responses did not differ between genders (). It is known that in a certain loading range, HR and BP increase proportionally to physical load increase. Future research should measure level of muscle tension during RSMT to determine whether men showed higher RRI oscillatory responses to RSMT because they produced stronger muscle contractions than did women. Gender differences in FPA oscillatory response to RSMT may reflect differences in BP oscillation amplitude in men and women.
CVS Oscillatory Reactions to 0.1 Hz RSMT Versus 0.1 Hz Paced Breathing
We found that in most cases both RSMT and paced breathing procedures caused 0.1 Hz oscillations in all studied functions (RRI, PTT, FPA, SC, and RV). These oscillations were considerably amplified in RRI and PTT due to the resonance in the HR baroreflex closed-loop. The amplitudes of the 0.1 Hz oscillations elicited by RSMT stimulation were almost the same in value as the amplitudes of the 0.1 Hz oscillations elicited by paced breathing in PTT, FPA, and SC, but significantly different in RRI and RV (see ).
Paced breathing caused significantly higher 0.1 Hz RRI and RV oscillations than did the RSMT procedure, however, analysis of gender differences (see and ) showed that this applied only to women. We assume that the amplitude of 0.1 Hz RRI oscillation depended on two conditions: the depth of breathing or the strength of muscle tension, and the power of resonance in the HR baroreflex closed-loop. An increase in rhythmical muscle tension increases the amplitude of 0.1 Hz RRI oscillation. Humans can voluntarily control muscle tension, and consequently, the amplitude of 0.1 Hz RRI oscillation elicited by RSMT. Further research is needed to determine if men and women who perform the RSMT procedure at the same intensity will produce equivalent 0.1 Hz RRI oscillation amplitudes in RSMT tasks, and if these amplitudes are of the same value as generated by paced breathing. It is possible that the amplitude of 0.1 Hz RRI oscillation elicited by paced breathing and the maximal amplitude of 0.1 Hz RRI oscillation elicited by RSMT could be equal for the same person.
0.1 Hz RV (i.e., tidal volume) oscillations in the paced breathing task were significantly higher than in RSMT task in both men and women. The difference in RV oscillatory reactions to 0.1 Hz RSMT and 0.1 Hz PB may be related to differences in minute volume ventilation during muscle tension versus paced breathing. Tidal volume may vary in both tasks, while rate (0.1 Hz frequency) of respiration is necessarily constant in paced breathing, yet may vary in RMST. In order to support the necessary minute volume ventilation in the 0.1 Hz paced breathing task, participants need to breathe deeply, whereas in the RSMT task, physical load increases the participant’s respiration rate, but not necessarily tidal volume. Respiratory effort to produce RRI oscillation in the PB task is limited in two ways: breathing too deeply at a rate of 0.1 Hz causes hyperventilation, whereas shallow breathing at this rate cannot provide the needed minute volume ventilation. When participants find a comfortable breathing depth between these two extremes, respiratory tidal volume becomes automatically set. Thus, the amplitude of 0.1 Hz RRI oscillation elicited by paced breathing cannot be voluntarily controlled. In contrast, humans can voluntarily control muscle tension, and consequently, the amplitude of 0.1 Hz RRI oscillation elicited by RSMT.
High-amplitude 0.1 Hz oscillation in the CVS elicited by 0.1 Hz PB and RSMT procedures appears to have worthwhile clinical application. Therapeutic effects from rhythmical stimulation at 0.1 Hz have been explained in terms of high-amplitude oscillation in autonomic functions which trained homeostatic reflexes and provided inhibitory modulation of the brain via the baroreceptors (Chernigovskaya et al., 1990
; Lehrer et al., 2003
). Comparison of RMST versus breathing effects on cardiovascular functions may be useful for further development of clinical applications. It is known that paced breathing at 0.1 Hz synchronizes respiration with HR oscillation. Synchronization improves the blood gas exchange since during the inhalation, when lungs are fully oxygenated, HR increases and intensifies oxygen utilization in blood (Yasuma, & Hayano, 2004
; Giardino, Chan, & Borson, 2004
). Paced breathing at 0.1 Hz increases baroreflex gain during the procedure (Lehrer et al., 2003
; Chacko et al., 2005
). Systematic use of the 0.1 Hz paced breathing procedure cumulatively increases baroreflex gain and peak expiratory flow over time in healthy people via training autonomic reflexes and restoring autonomic balance (Lehrer et al., 2003
). RSMT at 0.1 Hz does not synchronize respiration with HR oscillation, but significantly increases cerebral oxygenation (France, France, & Patterson, 2006
). Physical load decreases parasympathetic and increases sympathetic activity, considerably increases mean HR and relatively suppresses HRV during the procedure. Although RSMT elicits resonance oscillation in HR, total HRV remains at baseline levels, while total BP variability increases (Lehrer et al., 2009
). As a result, HR baroreflex gain does not increase during the procedure. However, beneficial effects can still be expected due to high-amplitude oscillations in cardiovascular functions and increased blood flow. Also it is known that baroreflex gain decreases during physical load (exercise), but increases to higher than baseline levels after the load, resulting in a cumulative increase in baroreflex gain over time (Cottin et al., 2008
; Potts et al., 1993
; Pagani et al., 1988
SC Oscillatory Reactions to RSMT and 0.1 Hz Paced Breathing Stimulation
The main SC focus in this study was on oscillations elicited by RSMT and PB stimulation. Although the mean value of SC was of secondary interest, we did find that RSMT and PB stimulation significantly increased mean SC compared to baseline (see ). We acknowledge that spectral analysis is not the typical method for analyzing SC data, however this approach is consistent with the design of our study, and our results suggest that this approach may offer additional insight into the interconnected control of autonomic functions.
We found that PB and RSMT at all stimulation frequencies caused SC oscillations manifested by the peaks in SC spectra at corresponding frequencies. SC has been most studied as a function that relates to emotion regulation and does not react directly to peripheral muscle tension or blood vessel activity. Lader and Montagu (1962)
, for example, showed that pharmacological blockage of peripheral vessel regulation did not suppress SC reaction to emotional stimuli. The present study did not involve emotional stimulation, but rather likely reflected SC as a thermal and perspiration regulatory function. RSMT and 0.1 Hz breathing modulated ANS activity by eliciting high amplitude oscillation in the CVS. Accordingly, we propose that modulation of sympathetic nervous system activity caused by RSMT or 0.1 Hz breathing can impose oscillation in various autonomic functions including SC.
In spite of the fact that SC response to a stimulus is a slow process that sometimes lasts for about 60 s, SC oscillations in our study were caused by 0.1 Hz paced breathing and 0.2, 0.1, or 0.05 Hz RSMT stimulations (i.e., when stimulation was applied every 5, 10, or 20 s). The ability to impose SC oscillations in response to rhythmical stimulation in a range of 0.2 – 0.05 Hz is supported by Edelberg’s (1970
findings. He showed that the duration of SC response to a stimulus is determined by the shape of the recovery limb of the response. Recovery rates do not depend on the response amplitude, but they are different in response to an alerting signal versus an execution signal for a task. SC responses to execution task signals have significantly faster recovery rates and slower habituation than SC responses to alerting signals. Consequently, the task signals in our study could cause relatively short SC responses and slow habituation, the two conditions needed to impose SC oscillatory response.
The present study results support this idea given that the amplitude of imposed SC oscillations significantly depended on the frequency of stimulation. The 0.1 and 0.05 Hz RSMT elicited almost equivalent amplitude oscillations in SC, while the relatively faster 0.2 Hz RSMT elicited significantly lower SC oscillatory responses (see and ). These findings suggest that 0.1 Hz oscillation in the CVS elicited by RSMT can spread to other autonomic functions, potentially activating and training reflexes that control these functions.
Limitations and Future Directions
Despite the statistical significance of the results, the small sample size of the present study may limit the generalizability of our findings, especially in regard to gender differences. Another limiting factor is the narrow age range of the participants. In line with our aim of investigating the intact mechanism of baroreflex resonance, only young and healthy participants were selected. Further research is needed to examine the influence of gender, age and other salient individual difference characteristics on the RSMT procedure for eliciting high-amplitude CVS oscillation. In addition, future studies should quantify values of muscle tension to evaluate task performance, especially in regard to gender differences. In the current study, we know that participants were able to spare the muscles of the right arm during RSMT, as instructed, because the physiological records from the finger pulse sensor and SC electrode attached to the right hand were artifact-free. However, we did not measure individual differences in muscle tension. Future research should also assess beat-to-beat BP to more fully characterize the involvement of the baroreflex mechanism. Finally, in line with our primary goal to evaluate resonance due to muscle tension, the paced breathing condition was always administered after the randomized RSMT tasks were completed because of the known effects of PB on cardiovascular functions. Thus, we cannot describe how participants’ completion of the muscle tension tasks may have affected the magnitude of oscillation due to resonance paced breathing.
Potential Clinical Application of Rrhythmical Muscle Tension Techniques
Physical activity strongly affects the CVS. We found that RSMT procedures may trigger 0.1 Hz resonance in the CVS. Human’s ability to voluntarily produce high amplitude oscillations in the CVS at resonance frequencies makes rhythmical muscle tension techniques potentially valuable for developing clinical applications. Previously, RSMT procedures at 0.1 Hz were effectively used to avert vasovagal reaction (France et al., 2006
). France’s RSMT technique was a single session intervention for use immediately prior to an event that could induce syncope. We suggest that other kinds of 0.1 Hz RSMT procedures can be exploited by researchers and clinicians for the development of novel approaches to correct abnormal autonomic regulation and enhance health. For example, systematic daily use of 0.1 Hz paced RSMT may produce a cumulative and long lasting therapeutic effect in the same way as paced breathing does in HRV biofeedback (Lehrer et al., 2003
; Cowan, Pike, & Budzynski, 2001
; Del Pozo et al., 2004
;, Nolan et al., 2005
; Karavidas et al., 2007
; Hassett et al., 2007
). The contribution of physical exercise to health promotion is well known. It is possible that including rhythmical elements at the HR resonance frequency in exercise may enhance its beneficial cardiac effects via training autonomic reflexes and increasing brain oxygenation. Such procedures could conceivably improve sports performance and prove especially useful in the rehabilitation process of patients following a cerebral stroke or myocardial infarction, where light physical exercises are prescribed (Buch, Coote, & Townend, 2002
) because exercise effects may be enhanced by high-amplitude oscillations in the CVS.