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Applied Psychophysiology and Biofeedback, Vol. 28, No.

1, March 2003 ( C 2003)

The Effects of Specic Respiratory Rates on Heart Rate and Heart Rate Variability
Hye-Sue Song1 and Paul M. Lehrer2,3

In this study respiratory rates of 3, 4, 6, 8, 10, 12, and 14 breaths per minute were employed to investigate the effects of these rates on heart rate variability (HRV). Data were collected 16 times at each respiratory rate on 3 female volunteers, and 12 times on 2 female volunteers. Although mean heart rates did not differ among these respiratory rates, respiratory-induced trough heart rates at 4 and 6 breaths per minute were signicantly lower than those at 14 breaths per minute. Slower respiratory rates usually produced higher amplitudes of HRV than did faster respiratory rates. However, the highest amplitudes were at 4 breaths per minute. HRV amplitude decreased at 3 breaths per minute. The results are interpreted as reecting the possible effects of the slow rate of acetylcholine metabolism and the effect of negative resonance at 3 cycles per minute.
KEY WORDS: respiratory sinus arrhythmia; paced breathing; resonance; baroreex.

Slow paced breathing has long been used as a relaxation method and as a nonpharmacological method for stabilizing various problems involving autonomic and emotional dysfunction. It has been used for management of pain (Anonymous, 1998; Jones & Evans, 1980) and anxiety symptoms (Clark & Hirschman, 1990; Salkovskis, Jones, & Clark, 1986). There is evidence that slow paced breathing can also decrease psychophysiological response to experimental threat (Harris, Katkin, Lick, & Habbereld, 1976; McCaul, Solomon, & Holmes, 1979; Sakakibara & Hayano, 1996). Slow paced breathing is a component of protocols for increasing the amplitude of respiratory sinus arrhythmia (RSA). This method has been proposed as a treatment for a variety of problems related to stress and autonomic dysfunction (Chernigovskaya, Vachillo, Petrash, & Rusanovskii, 1991; Lehrer, Smetankin, & Potapova, 2000; Lehrer, Vaschillo, & Vaschillo, 2000). RSA refers to cyclical uctuations in heart rate (HR) coincident with the respiratory cycle, such that increases in HR occur during inhalation and decreases in HR occur during exhalation. Heart rate variability (HRV), of which RSA is a component, has been studied as a measure of autonomic homeostasis and adaptability (Berntson et al., 1997), but much remains unknown about the relationship between specic respiratory strategies and RSA, despite the large number of studies on the
1 Seoul, 2 Department 3 Address

South Korea. of Psychiatry, UMDNJ Robert Wood Johnson Medical School, Piscataway, New Jersey. all correspondence to Paul M. Lehrer, Department of Psychiatry, UMDNJ Robert Wood Johnson Medical School, 671 Hoes Lane, Piscataway, New Jersey 08854; e-mail: lehrer@umdnj.edu. 13
1090-0586/03/0300-0013/0
C

2003 Plenum Publishing Corporation

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topic (Anrep, Pascual, & R ossler, 1936a, 1936b; Berntson et al., 1997) since RSA was rst described in the horse by Stephen Halls, in 1733. RSA usually is reected in high-frequency HR oscillations (0.150.4 Hz), that is, in the typical frequency range of normal adult respiration. It is vagally mediated, and has been used as a noninvasive measure of parasympathetic function (Berntson et al., 1997), although it does not correlate well with vagally induced decreases in tonic HR (Kollai & Mizsei, 1990). Porges (1995) has noted that different central mechanisms may be involved in mediating the two vagal effects. HRV at lower frequencies usually involves greater sympathetic contributions (Berntson et al., 1997), although it is not monotonically related to sympathetic neurohumoral responses (Sloan et al, 1996).4 Respiratory rate affects the amplitude of RSA, with RSA tending to increase as respiration rate decreases. However, this research has mostly used a restricted range of respiratory frequencies, has compared paced with nonpaced breathing within only a narrow band of respiratory frequencies, or has examined bands of respiratory rates rather than specic rates. Hayano et al. (1994) studied only the effects of the relatively low respiratory intervals of 3, 4, 5, and 6 s. Pagani, et al. (1986) compared the effect of paced breathing (0.33 Hz) with voluntary breathing (mean of 0.26 Hz). Jennings, Mcknight, and Van der Molen (1996) divided participants according to their natural respiratory rates (faster breathers [>15 breaths per minute] vs. slower breathers [<15 breaths per minute). However, Vaschillo et al. (2002) found that the effects of specic rates at slower frequencies provide information about the operating characteristics of the systems that control cardiovascular regulation. They found resonance effects in the low-frequency and very low frequency ranges of HRV (respectively, 0.05 0.15 Hz and 0.0050.05 Hz), ranges that are lower than those generally investigated in this previous literature. They found positive resonance at six cycles per minute, where people could use biofeedback to achieve particularly high amplitudes of RSA. They also found negative resonance at three cycles per minute, where biofeedback-produced amplitudes of RSA were particularly low. Although participants in their study did not uniformly use respiration as a method to alter RSA amplitude, respiration was one of the several methods that people did employ in this study. Studies of healthy patients (Cooke et al., 1998) and of Zen monks (Lehrer et al. 1999) show that patients can breathe comfortably and at these slow rates for periods long enough to investigate the effects of these rates on HRV. The purpose of this study was to investigate systematically how respiratory rate modulates HRV at respiratory rates of 3, 4, 6, 8, 10, 12, and 14 breaths per minute, in order to determine whether the effects of resonance can be detected using this procedure. METHODS Participants Five female volunteers participated in this study (mean age = 29) with no history of heart problems or other chronic physical or mental diseases. No participant had any prior
4 At normal respiratory cycles, high-frequency HRV is vagally mediated and usually corresponds to RSA (Berntson

et al., 1997); low-frequency HRV is both sympathetically and parasympathetically mediated and correlates highly with baroreex function (Akselrod et al., 1981; Bernardi et al., 1994; Hyndman, Kitney, & Sayers, 1971; Pomeranz et al., 1985); and very low frequency activity is sympathetically mediated and may reect thermoregulation and regulation of vascular tone (Berntson et al., 1997). When people breathe at rates within the low-frequency or very low frequency ranges, however, the processes associated with RSA overlap and sometimes resonate with processes usually associated with lower frequency bands (Vaschillo, Lehrer Rishe, & Konstontinov, 2002).

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experience with respiratory training procedures, but all of them were able to master the task within the rst few minutes of training. The study was approved by the Institutional Review Board of UMDNJ Robert Wood Johnson Medical School. The participants were acquaintances of the experimenters. Two of the participants were paid $100 each for taking part in the study. The other 3 were laboratory personnel involved in this and other studies from our laboratory. Equipment and Data Reduction/Analysis Data were collected between October 1998 and March 1999 and between May 2000 and July 2000 using an I-330 C2 Physiograph (J&J Engineering, Bainbridge Island, WA). ECG data were acquired digitally at 512 samples per second, and were put through a lowpass lter for R-wave detection, after which cardiac interbeat intervals were derived from a level detector. Irregular heart rhythms caused by artifacts or other physiological variables were smoothed using the MXEDIT program (Delta-Biometrics, Inc. Bethesda, MD), a program for graphic display and editing of HRV data. FFT analyses were performed using the Log-a-Rhythm program (Nian-Crae, Inc. Piscataway, NJ), with bin widths of 0.000 0.047 Hz for the very low-frequency band, 0.0470.156 Hz for the low-frequency band, and 0.1560.406 Hz for the high-frequency band (cf. Berntson et al., 1997).4 Respiration was recorded using a strain gauge device fastened at chest or abdomen depending on individual respiratory patterns. Protocol Just prior to each session, participants were seated in a comfortable chair, and EKG electrodes were pasted to their wrists. All procedures were carried out while the participants were seated in an upright position.The procedure involved the following design: 24 sessions were administered to 3 participants with paced breathing tasks at 4, 6, 8, 10, 12, and 14 breaths per minute, and 21 sessions to 2 participants with rates of 3, 4, 6, 8, 10, 12, and 14 breaths per minute. The various breathing frequencies were counterbalanced for order of presentation during the session, and combined systematically with each other using a partially balanced within-participant incomplete Latin Square design. For each participant, each respiratory rate was used the same number of times, but in varied but balanced orders across tasks, with four tasks in each session. Two sessions each included 3, 4, 12, and 14 breaths per minute (one in the reverse of this order), and, similarly, two sessions each, respectively, for 3, 4, 6, and 8 breaths per minute and for 6, 8, 12, and 14 breaths per minute. Each breathing task lasted for 5 min. Tasks were separated by pauses of 25 min. Eventually 3 of the 5 participants had engaged in 16 tasks and 2 of them had engaged in 12 tasks at each respiratory rate. Participants engaged in one to three sessions per day. Each session lasted between 30 and 50 min. The stimuli by which participants paced their breathing were presented on a computer monitor using HRDFT software on the I-330 C2 Physiograph. A moving bar was the stimulus for inhalation and exhalation. Participants were instructed to inhale as the bar rose and to exhale as it fell. The up and down excursions of the bar were at equal intervals. In almost all cases, participants breathed almost exactly at the target breathing rate, (i.e., the rate at which the stimulus bar rose and fell). Where small deviations occurred, the

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participant was coached to follow the moving bar more closely. Before beginning each 5min trial, participants breathed at the target breathing rate for 12 min, in order to establish a regular pattern of HRV corresponding to that particular breathing rate.

RESULTS A one-way repeated measures analysis of variance was performed using the SAS GLM procedure, with participants nested in respiratory rates as the error term. This procedure was used to test the effects of respiratory rates on each measurement. Tukeys HSD test was employed for post hoc comparisons between specic respiration rates. Means and SDs of each measure are presented in Table I. The Effects of Respiratory Rates on Heart Rate Figure 1 depicts the mean HR, and respiratory-induced trough and peak HR at respiratory rates of 3, 4, 6, 8, 10, 12, and 14 breaths per minute.5 There were no significant differences for mean or peak HRs among respiratory rates, but signicant differences were found for the mean of trough HRs recorded during each respiratory cycle, F (6, 25) = 3.35, p < .05. Tukeys studentized range test showed that trough HRs at the respiratory rates of 4 and 6 breaths per minute were signicantly lower than those at 14 breaths per minute. The Effects of Respiratory Rates on Heart Rate Variability Total HR oscillation amplitudes (across frequency bands) at each respiratory rate were signicantly different among respiratory rates, F(6, 25) = 34.57, p < .001. They were highest at 4 breaths per minute. Amplitude at this respiratory rate was signicantly higher than for 8, 10, 12, and 14 breaths per minute. Signicant respiratory rate effects were also found in amplitudes of HRV, within both the low-frequency, F (6, 25) = 30.45, p < .0001, and high-frequency bands, F (6, 25) = 10.71, p < .0001. Post hoc tests showed that HRV was highest within the frequency band at which participants breathed during each task Thus, low-frequency amplitude of HRV was signicantly higher at respiratory rates of three and four breaths per minute than at higher respiratory rates (10, 12, or 14 breaths per minute), and high-frequency HRV was higher at 10 breaths per minute than at 3, 4, or 6 breaths per minute (Fig. 2). Within each frequency band, the highest amplitudes almost always occurred at lower frequencies, when participants breathed within that frequency band. The highest amplitudes of HRV in the high-frequency band occurred at a respiratory rate of 10 breaths per minute, which is at the low end of the high-frequency range. However, there was one exception to this pattern: The greatest amplitude within the low-frequency band was at four breaths per minute, not at three per minute.
5 Peak

HR is the highest HR reached during inhalation. Trough HR is the lowest HR reached during exhalation.

Table I. Means and (SDs) of HR and HRV 4 6 8 10 12 14 F 0.43 3.35 0.36 3.23 30.45 10.71 34.57 18.44 P< ns .0146 ns .05 .0001 .0001 .0001 .0001

Respiratory Rate and Heart Rate Variability

HRV

Mean HR Trough HR Peak HR VLF LF HF Total variability Peak power

76.51 (6.37) 78.42 (7.33) 76.51 (6.37) 77.65 (6.89) 77.91 (6.57) 79.53 (7.70) 81.10 (8.05) 63.27a (6.18) 64.36a (6.77) 65.58 (6.05) 67.22 (7.29) 69.88b (7.46) 60.94 (5.87) 62.27a (6.21) 93.78 (5.70) 96.38 (8.11) 94.61 (8.03) 92.87 (7.75) 92.07 (7.37) 93.23 (8.57) 93.83 (8.71) 8.54 (3.85) 3.96 (2.19) 3.45 (2.29) 4.28 (3.40) 4.64 (3.27) 4.78 (3.80) 4.04 (2.83) 64.90b (21.85) 48.45 (21.96) 29.10 (13.95) 4.88a (2.45) 4.62a (3.38) 3.45a (2.38) 51.37b (16.11) 2.02a (1.06) 3.31a (2.27) 3.37 (2.99) 15.68b (8.89) 9.17 (5.07) 6.22 (3.32) 1.52a (0.61) 57.17 (20.34) 38.59a (14.52) 26.99a (9.02) 20.58a (7.91) 15.72a (6.65) 61.52 (17.16) 72.51b (21.36) 4102.08 (1488.24) 4663.47 (1690.29) 3072.99 (1531.49) 1725.63 (980.32) 1076.56 (710.52) 643.81 (446.10) 404.54 (263.76)

Note. RR = respiratory rate; mean HR = beats per minute (bpm); trough HR = mean of lowest HR in respiratory-linked HR oscillations during the 5-min task; peak HR = mean of highest HR in respiratory-linked HR oscillations during the 5-min task; VLF = very low frequency HR oscillations (0.0000.047 Hz), (bpm)2 /Hz; LF = low-frequency HR oscillations (0.0470.141 Hz), (bpm)2 /Hz; HF = high-frequency HR oscillations (0.1410.406 Hz), (bpm)2 /Hz; total variability = total HR oscillation amplitude, across frequencies (0.0000.5000 Hz), (bpm)2 /Hz; peak power = frequency power of HRV at the target respiratory frequency, (bpm)2 /Hz. Signicant individual cell differences ( p < .05) by Tukeys HSD test: Cells with superscript a have lesser values than cells marked with superscript b.

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Fig. 1. Heart rates at each respiratory rate.

The Effects of Respiratory Rates on Peak Power The peak power measured at each respiratory frequency also differed signicantly among respiratory rates, F (6, 25) = 18.44, p < .001. In the large majority of cases the frequency at which peak HRV occurred was the same as the respiratory frequency. In only two tasks in a single individual (across all participants and breathing tasks) did the peak frequency differ from the target respiratory frequency. This occurred in a single session, while the individual breathed at 12 and 14 breaths per minute. In both of these cases a second frequency peak in HRV also occurred at the target respiratory frequency. In these cases, the peak at target respiratory frequency was chosen for analysis. The power at the frequency with peak oscillatory variability was highest at 4 breaths per minute, and was signicantly higher at this rate than at 8, 10, 12, and 14 breaths per minute (see Fig. 3).

Fig. 2. The amplitude of heart rate variability at each respiratory rate. Note. HF = high-frequency heart rate variability, LF = lowfrequency heart rate variability, and VLF = very low frequency heart rate variability.

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Fig. 3. The amplitude of the power peak in heart rate variability at each respiratory rate.

DISCUSSION The principal nding in our study is the inverse relationship between HRV amplitude and respiratory frequency, with one exception: Low-frequency amplitude, total amplitude, and peak power amplitude, all peak at four breaths per minute, but they all are lower at three breaths per minute. Other studies also have shown the frequency-dependent nature of HRV, such that HRV decreases as respiration rate increases (Brown, Beightol, Koh, & Eckberg, 1993; Cooke et al., 1998; Ritz, Thons, & Dahme, 2001; Stark, Schienle, Walter, & Vaitl, 2000). The increased HRV at slower respiration rates was accompanied by lower trough HRs with each breath and a greater spectral frequency peak at the respiratory frequency. The frequency peak data replicate ndings by Hayano et al. (1994) that paced breathing produces a high-frequency peak at respiratory frequency. Although these data could suggest greater vagal activation at lower respiratory frequencies, Eckberg and Eckberg (1982) suggest that it may also be due to more complete hydrolyzation of acetylcholine at lower respiration rates. According to this theory, hydrolyzation of acetylcholine is a relatively slow process, and thus is more complete at slower respiration rates, before the next inhalation blocks expression of acetylcholine. As such, then, the increased RSA at lower respiratory frequencies would not necessarily represent increased vagal trafc.6
6 The theory of Eckberg and Eckberg (1982) is based on observations that although respiration gates vagalcardiac

nerve activity (such that vagal ring is greater in expiration than in inspiration), hydrolysis and inactivation of acetylcholine by acetylcholinesterase proceed at a xed rate that is unrelated to breathing frequency. The consequences of this are that during longer breathing intervals, acetylcholine is more completely hydrolyzed and inactivated, vagal inhibition is less, and respiratory-rate intervals are shorter (Raczkowska, Eckberg, & Ebert, 1983). It seems likely that breathing inuences the timing of vagal inhibition, but not the absolute quantity: over a wide range of breathing frequencies, average R-R intervals are constant (Brown et al., 1993). Thus, a bolus of acetylcholine is released during each exhalation, thereby accounting for the decrease in HR in this phase of breathing. According to Eckbergs theory, the oor of the acetylcholine valley during respiration is higher during more rapid breathing due to incomplete hydrolyzation, producing a smaller amplitude of respiratory sinus arrhythmia than during slow breathing. This theory would account for higher amplitudes of respiratory sinus

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We also note that the frequency-dependent changes in HRV found in this study probably do not result from differences in depth of breathing at various frequencies. Cooke et al. (1998) studied HRV in response to a similar range of paced respiration rates used in the current study, and found patterns of HRV differences among respiratory rates that were similar to those in the current study, whether or not depth of respiration was controlled, despite the well-known HeringBreuer reex, a vagally mediated autonomic effect stimulated by stretching of the lung tissues during respiration. In addition, consistently with other studies (Brown et al., 1993; Cooke et al, 1998; Grossman, Karemaker, & Wieling, 1991; Hayano et al., 1994; Pitzalis et al., 1998) respiratory rate did not signicantly alter average HRs over the respiratory ranges studied. The lack of relationship between mean HR and respiration rate gives further support to the notion that higher amplitudes of RSA at slower respiratory rates does not result from increased vagus nerve output. There were some exceptions to the negative relationship between respiration rate and HRV. HRV outside the frequency range of respiration invariably was at a lower amplitude than for HRV within the band of the participants respiration. Thus HRV at slower oscillation rates was lower than at higher rates when participants breathed within the high-frequency range. Also, HRV amplitude at three breaths per minute tended to be less than at four breaths per minute. Although this difference was not signicant, there were fewer signicant differences between higher rates of breathing and breathing at three breaths per minute than at four breaths per minute. The latter nding suggests that a second process is at work. Vaschillo et al. (2002) found negative resonance between baroreex effects and voluntary effects on HRV at approximately three cycles per minute. At this frequency, oscillations in HR and blood pressure tend to be in phase with each other (zero degree phase relationship). Thus, as respiration (or other voluntary processes) produce increases in HR, baroreex activity triggered by the simultaneous increases in blood pressure would tend to depress the changes in HR. Thus, respiratory effects on HRV would resonate negatively with baroreex effects. This would be consistent with a decrease in total HRV as well as at the particular frequency peak.7 Our study did not, however, nd evidence for positive resonance at six breaths per minute, as might be predicted by the ndings of Vaschillo et al. (2002). It is possible that the hydrolyzation effects overrode any possible resonance effects at this frequency. These data thus suggest a complex relationship between respiratory rate and amplitude of HRV, involving at least two independent processes. The increased HRV found in previous literature at lower frequencies was replicated here, but does not extend to the rate of three breaths per minute, and does not necessarily represent greater vagal tone.

arrhythmia at lower respiratory frequencies, even if each breath released approximately an equal-sized bolus of acetylcholine, unrelated to respiration rate, and is consistent with the decreased troughs but not peaks in HR found in this study. This theory explains how increased respiratory sinus arrhythmia during slow breathing could occur without any changes of trafc in the vagus nerve. 7 Angelone and Coulter (1964) rst described cardiovascular system resonance in the low respiratory frequency range (at about ve to six breaths per minute. in their study). Vaschillo et al. (2002) conrmed these ndings and also showed that there was negative resonance at three breaths per minute where participants blood pressure and HR have a zero degree phase relationship. Therefore, at three breaths per minute, respiratory-induced increases in HR occur simultaneously with baroreex-induced decreases in HR, that is, the HR effects of the two processes begin to cancel each other out.

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Limitations of This Study The restricted sample size, all women, necessarily limits generalizability of our results. These limitations particularly apply to respiration at three breaths per minute, where we studied only two participants. However, the adjustment for unequal cell sizes using the GLM procedure and the great consistency both within and between participants in this study and in relation to other studies both suggest that the relationships found in this study are reliable and interpretable. Studying people in other age groups, in men, and among individuals with various pathologies affecting the cardiorespiratory system may allow us to explore various characteristics that may affect the relationships found in this study. Implications for Biofeedback Treatment These results conrm the ndings of a mostly inverse relationship between RSA and respiration rate during paced breathing maneuvers. They indicate that the relationship between respiration and RSA amplitude is inuenced by several causal pathways, and suggest that increases in RSA amplitude produced by slow breathing probably do not reect increases in vagal tone or parasympathetic arousal. The implications for the mediating role of resonance in RSA biofeedback are unclear. The results are consistent with the occurrence of negative resonance for HRV at approximately three cycles per minute, but did not show effects of positive resonance at six cycles per minute. It is unclear whether this suggests that positive resonance does not occur at six cycles, whether other processes, such as the effects of acetylcholine hydrolyzation, obscure resonance effects, or whether such interaction between hydrolyzation and resonance effects has any practical signicance for the practice of biofeedback. Further research is needed on the relationship between respiration and resonance characteristics of the cardiovascular system, and on ways that biofeedback and respiratory control methods interact with these various possible mediators, and the inuence of these mediators on the clinical effects of biofeedback.

ACKNOWLEDGMENTS This research was supported in part by grant # R1HL58805A to Paul Lehrer from the National Heart Lung and Blood Institute. The authors are indebted to Dwain Eckberg for assistance in interpreting his theory of acetylcholine hydrolization, and to Elora Roy for testing some of the participants and assisting in data analysis.

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