It is well known that endurance training induces bradycardia: reduction in heart rate (HR) at rest (5). Many previous studies have suggested that bradycardia at rest may be caused by decreased cardiac sympathetic modulation and increased cardiac parasympathetic modulation (5,10,12,27,28). On the other hand, there are very few studies on the effects of endurance training on the cardiac autonomic control measured during a postexercise recovery period as opposed to studies done at rest (10). Darr et al. (9) reported that trained subjects in both younger and older age groups exhibited more rapid HR recovery than their untrained counterparts after exercise at similar relative workloads. During exercise, HR increases through a combined effect of sympathetic activation and parasympathetic withdrawal. Immediately after exercise, HR recovery is mainly attributed to vagal reaction (2). Therefore, there is a possibility that an adaptation of the cardiac autonomic nervous system (ANS) to endurance training contributes to a more rapid HR recovery after exercise. If adaptation in cardiac autonomic modulation is a major contributing factor in the reduction of resting and postexercise HR after endurance-training sessions, then changes in cardiac ANS modulation during training periods should correspond to the changes in HR reduction. However, the changes over time in cardiac ANS modulation and HR during an endurance-training program have never been reported.
HR variability analysis has proven to be a simple noninvasive technique for the evaluation of autonomic modulation of HR through the measurement of instantaneous beat to beat variations in R-R interval length. Thus, it furnishes a tool to noninvasively explore the sympathovagal interaction under varying conditions (19). An additional advantage of this method is the possibility of repeated measurements with the same subject. Using analysis of HR variability, we investigated the changes over time in HR and ANS modulation measured both at rest and during postexercise recovery periods over a 6-wk endurance-training program.
Twelve healthy male students majoring in physical education volunteered for the study. They were assigned to either an endurance-training group (ET, N = 7) or a control group (C, N = 5) and were matched as closely as possible with regard to age, height, weight, and peak oxygen uptake (peak V̇O2). All subjects were nonsmokers. The subjects had no history of any respiratory or cardiac diseases. All subjects provided informed written consent for their participation with the experimental procedures conducted in conformance with the human subjects policy statement published by Medicine and Science in Sports and Exercise. Table 1 shows the physical characteristics of the respective ET and C groups measured before and after the 6-wk training period.
The ET group underwent cycle-endurance training for 6 wk. The C group led normal lives during the 6-wk period. To record changes in HR variability both at rest and during postexercise recovery periods, the ET group was measured five times: before the training, on the 4th day, on the 7th day, on the 28th day, and on the 42nd day of the training period. The C group was measured four times: before the training, and on the 7th, 28th, and 42nd days of the 6-wk period. All measurements were made at the same time of day for each subject. Measurement of HR variability was performed in a quiet, air-conditioned (22–25°C) room. All subjects were instructed to fast for at least 3 h before testing on the day of the experiment. After 15 min of quiet rest in the sitting position, the subject’s electrocardiogram (ECG, CM5 lead, Nihonkoden WEP-7404, Tokyo, Japan) was sampled by a computer that measured and stored each R-R interval over a 5-min period. Then, the subjects performed cycle exercise for 40 min at the individual 80% peak V̇O2. At 10- and 20-min intervals after exercise, the subject’s ECG also was sampled over a 5-min period in the sitting position. Respiration was controlled at frequencies 0.25 Hz during the measurement of HR variability both at rest and during postexercise recovery periods. HR both at rest and during the postexercise recovery period were determined by the average R-R interval over the entire 5-min measurement period. Before and after the training period, left ventricular end systolic (LVESD) and diastolic (LVEDD) diameters were measured by M-mode echocardiography according to the American Society of Echocardiography (23). The echocardiographic measurement was taken in supine position at rest. Additionally, left ventricular end systolic (LVESV) and diastolic (LVEDV) volumes were calculated with Teichholz’s conventional method (32).
Determination of peak V̇O2.
The peak V̇O2 was measured by an incremental cycle exercise test using a cycle ergometer (Monark, Varberg, Sweden). The incremental cycle exercise began at a work rate of 120 W (60 rpm), and power output was increased by 30 W·min−1 until the subjects could not maintain the fixed pedaling frequency. The subjects were encouraged during the ergometer test to exercise at as high a level of intensity as possible. HR and a rating of perceived exertion (RPE) were monitored minute by minute during exercise. Oxygen uptake (V̇O2) was monitored during the last 30 s of each increase in the work rate after the RPE reached 18. RPE was obtained using the modified Borg scale (7). Subjects breathed through a low-resistance two-way valve, and the expired air was collected in Douglas bags. Expired O2 and CO2 gas concentrations were measured by mass spectrometry (Westron WSMR-1400, Chiba, Japan), and gas volume was determined using a dry gas meter (Shinagawa Dev. NDS-2A-T, Tokyo, Japan). The highest value of V̇O2 during the exercise test was designated peak V̇O2.
The ET group underwent cycle-endurance training for 6 wk. Subjects exercised 4 d·wk−1 at an intensity that elicited 80% of each subject’s peak V̇O2. The pedaling rate was 60 rpm, and the duration of training was 40 min. As each ET, subjects’ peak V̇O2 increased during the training period, exercise intensity was increased every week as required to elicit 80% of the actual peak V̇O2 that was measured every week.
Estimation of the cardiac ANS modulation.
HR variability was sampled at 1000 samples per second with an A/D converter (AD instruments Maclab/400, New South Wales, Australia) from ECG to computer. Before analysis, all R-R intervals were visually inspected for artifacts that could affect the result. The power spectra were estimated from the sampled HR variability for 5 min using fast Fourier transform algorithm (FFT). Sampling points for spectral analysis were 1024 points. Power spectra obtained by spectral analysis were defined as two components: 0.04–0.15 Hz (low frequency: LF) and 0.15–0.4 Hz (high frequency: HF). The very low frequency (0–0.04 Hz) is not addressed in the present study. HF power is almost entirely mediated by the vagal activity in the sinoatrial node directly associated with respiratory activity (1,3,21), whereas LF power reflects the mixed modulation of vagal and sympathetic activities (4). The ratio of LF power to HF power (LF/HF) is considered to reflect the sympathovagal balance, and high values suggest a sympathetic predominance (20). The LF/HF ratio, HF power, and total power (LF power plus HF power) were transformed into their natural logarithms (ln) before statistical analysis. The logarithmic transformations produced approximately symmetric distributions and thus allowed for the use of parametric statistics that require near normal distribution. In addition to frequency domain indices of HR variability, the standard deviation of normal R-R intervals (SDNN) was calculated from sampled HR variability for 5 min.
Complex demodulation analysis.
To standardize physiological and clinical studies, short-term recordings of 5 min should be made under physiologically stable conditions when processed by FFT (31). Cardiac autonomic control and HR are dramatically changed during exercise and immediately after heavy exercise. Thus, it is difficult to estimate cardiac autonomic control when processed by FFT algorithm under these situations, due to the limitation in time resolution of FFT. Therefore, we designed that the postexercise measurements to be made during 10–15 min and 20–25 min after exercise. However, the frequency analysis of HR response during recovery phase should confirm whether sympathovagal balance was dynamically changed during 10–15 min and 20–25 min after exercise in the present study. Complex demodulation (CDM) can measure time-dependent changes in the amplitude of specific frequency domain components (13,14). Thus, the time-dependent changes in ln HF power, obtained from all subject’s ECG data before training period, during postexercise recovery periods were assessed by CDM analysis. For the analysis of HF component of the R-R interval, reference frequency was set at 0.30 Hz. The low-pass corner frequency was set at 0.16 Hz for HF component, so that the frequency band for demodulating the HF component was 0.14–0.46 Hz. Figure 1 shows instantaneous power of HF component obtained by CDM during postexercise recovery periods. The power of HF component did not change during 10–15 and 20–25 min after exercise. In addition, HR decreased ∼3 bpm during 10–15 min and did not change during 20–25 min after exercise. These results show that the 5-min sampling period for FFT analysis was in stable condition at 10 and 20 min during the postexercise recovery phase of the present study.
Values are shown as mean ± SE. The differences between the change in the ET group and change in the C group during the training periods were statistically analyzed using two-way ANOVA with repeated measurements and Scheffe post hoc test. The correlation coefficients between Δ HR and Δ ln LF/HF or Δ ln HF power in the ET group were determined by the Pearson correlation. The Δ HR, Δ ln LF/HF, and Δ ln HF power were estimated as the difference between the measurements before the training and on the 4th, 7th, 28th, or 42nd day of training period. The level of significance was established at P < 0.05.
Peak V̇O2 after the training program was significantly higher than peak V̇O2 measured before the training program began in the ET group. The increase in peak V̇O2 for seven subjects of the ET group averaged 5.7 mL·min−1·kg−1 (12%, Table 1).
Figure 2 (A–F) illustrates examples of power spectral plots measured at rest (A, D) and at 10-min (B, E) and 20-min (C, F) intervals after 80% peak V̇O2 exercise in a sitting position before and after the 6-wk training program. At rest, there was a higher HF component after training (Fig. 2D) as compared with before the training (Fig. 2A). During postexercise recovery periods, the HF component after training (Fig. 2, E and F) was higher than that before training (Fig. 2, B and C). Conversely, the LF component decreased after the training program.
Figure 3 shows the changes in HR and the indices of cardiac ANS modulation measured both at rest and at 10- and 20-min intervals after 80% peak V̇O2 exercise sessions over a total training program of 6 wk. At rest (Fig. 3, left), HR at 28 d was significantly lower than HR measured before the training program began in the ET group. Furthermore, HR (53.1 ± 2.7) at 42 d was significantly lower than HR (58.8 ± 2.9) at 28 d (P < 0.05). The ln LF/HF tended to decrease with training, but there was no statistical significance (P = 0.09). The ln HF power and SDNN at 7 d were significantly larger than those before the training period began in the ET group. Although HR at 42 d was significantly lower than HR at 28 d, there were no significant differences in the cardiac ANS parameters between those at 28 d and those at 42 d in the ET group.
At 10 min after 80% peak V̇O2 exercise (Fig. 3, center), HR at 7 d was significantly lower than HR before the training program began in the ET group. Although ln LF/HF showed changes similar to HR in the ET group, there was no statistical significance. ln HF power and SDNN at 7 d were significantly larger than those before the training program began. There were no significant changes in any parameters of the ET group between 7 d and 42 d in the training program.
In both ET and C groups measured at 20 min after 80% peak V̇O2 exercise (Fig. 3, right), changes in HR, ln HF power, and SDNN during the training program were similar to those at 10 min after exercise. However, ln LF/HF measured at 7 d was significantly lower than the ln LF/HF before the training program began in the ET group.
At rest, the total power (6.63 ± 0.28 ms2) at 7 d was significantly larger than before (5.99 ± 0.33 ms2) the training period began in the ET group (P < 0.05). Subsequently, the total power slightly increased throughout the remainder of the training program, but there was no statistical significance (before the training, 5.99 ± 0.33 ms2; on the 4th day, 6.45 ± 0.29 ms2; on the 7th day, 6.63 ± 0.28 ms2; on the 28th day, 6.79 ± 0.26 ms2; and on the 42nd day of training period, 6.85 ± 0.24 ms2; mean ± SE). However, when measured at both 10- and 20-min intervals after 80% peak V̇O2 exercise, there were no significant changes in ln total power in the ET group at any time during the 6-wk program. There were no significant changes in any parameter in the C group at any time during the 6-wk program.
Table 2 shows the correlation coefficients of changes during training period between HR and ln LF/HF or ln HF power measured both at rest and at 10 min and 20 min after 80% peak V̇O2 exercise. These were obtained from all measurements of ET group during the training program. There were significant relationships between Δ HR and Δ ln HF power measured at rest and at 10 min and 20 min after 80% peak V̇O2 exercise. Significant relationship between Δ HR and Δ ln LF/HF existed at 20 min after exercise only.
Training state, peak V̇O2, and HR.
The present training program significantly increased peak V̇O2 and LVEDD, and decreased resting HR. In a review of the interactions of intensity, frequency, and duration of exercise training by Wenger and Bell (33), the increase in V̇O2max induced by 70–90% V̇O2max exercise intensity training was as follows: 6.5% when frequency was 4 d·wk−1; 7.8% when duration was 35–45 min and 4.5% when program length was 5–7 wk. The increase in peak V̇O2 of ET group in the present training program of 6 wk, 4 d·wk−1, for 40 min per training session, at 80% peak V̇O2 was 12%. Also, the present training program decreased resting HR of approximately 15 bpm. Recently, Wilmore et al. (34) reported effects of a 20-wk cardiorespiratory endurance-training program at 55–75% of the initial V̇O2max on resting HR as determined under highly controlled conditions. After the training, the resting HR decreased approximately 3 bpm. On the other hand, a reduction in resting HR induced by high exercise intensity training (80% V̇O2max) was reported at approximately 10 bpm (26). Our belief is that the rather large reduction in resting HR in the present study was due to the relatively high training intensity. Thus, the present training program was effective in improving aerobic work capacity and reducing resting HR.
Changes in cardiac autonomic control induced by endurance training measured at rest.
In the ET group, the present training program significantly decreased HR and increased ln HF power and SDNN measured at rest with a simultaneous increase in aerobic work capacity. Cardiac neural control was first evaluated in athletes by spectral analysis of HR variability of short length recordings by Dixon et al. (10). These investigators observed a higher cardiac vagal control and lower cardiac sympathetic control in endurance athletes than in sedentary controls. Goldsmith et al. (12), using HR variability analysis by 24-h Holter monitoring, also found greater parasympathetic modulation of HR in trained than untrained subjects. Other investigators (5,28) have reported that cardiac vagal modulation, which was assessed by either respiratory sinus arrhythmia or pharmacologic maneuvers, was enhanced at rest in long-term physically trained athletes. They have speculated that enhanced cardiac vagal modulation might in part contribute to resting bradycardia in these athletes. These findings support the present results. On the other hand, the ln LF/HF tended to decrease with present training, but there was no statistical significance (P = 0.09). Shin et al. (27) reported that the index of parasympathetic modulation in R-R interval spectra was significantly higher in athletes than in nonathletes, whereas the index of sympathetic modulation tended to be lower in athletes than that in nonathletes, but there was no statistical significance. Furthermore, present training program increased ln total power. An increased total power of HR variability, i.e., LF power plus HF power, induced by endurance training indicates both improved cardiac sympathetic and parasympathetic modulation (11,16). These findings suggest that endurance training may either increase both cardiac sympathetic and parasympathetic modulation at rest, or that it has no effect on sympathetic modulation and only increases parasympathetic modulation. In either situation, this causes a predominance of parasympathetic control in the sympathovagal balance.
We investigated the contributory rates of alteration in ln LF/HF and ln HF power to bradycardia induced by the present training methodology. As shown in Table 2, there was a significant relationship between Δ HR and Δ ln HF power measured at rest during the training program. However, significant correlation was not found between Δ HR and Δ ln LF/HF. Significant difference before and after the training program was not found in the ln LF/HF. These findings suggest that the enhanced parasympathetic modulation contributes in part to decreased resting HR due to endurance training and the ln LF/HF has no effect on resting bradycardia.
Other mechanisms have been proposed to explain resting bradycardia induced by endurance training. Katona et al. (17), using sympathetic and parasympathetic blocking agents, found that the lower HR in athletes results from a reduction in intrinsic cardiac rate and not from an increase in parasympathetic tone and decrease in sympathetic tone. Bonaduce et al. (6) reported that detrained athletes showed a higher cardiac parasympathetic modulation with slower HR than controls, but after vigorous training no further increase in parasympathetic modulation was detectable in athletes despite further decreases in HR and increases in LVEDD. In the present study, after the 28th day of training, no further changes in the indices of cardiac ANS modulation were detectable despite a continued decrease in HR. The present training program also significantly increased LVEDD and LVEDV, which is corrected for individual body surface area when measured at rest. Taken together, these observations support the hypothesis that resting bradycardia induced by endurance training was, in part, a consequence of a decrease in intrinsic HR.
Changes in cardiac autonomic control induced by endurance training measured during postexercise recovery periods.
The ln LF/HF measured 10 min after cessation of exercise tended to decrease with continued endurance training, but there was no statistical significance. However, HR was significantly decreased and the ln HF power and SDNN were significantly increased by endurance training when measured 10 min after cessation of exercise. These findings indicate that enhanced cardiac parasympathetic modulation is a major contributor to the decrease in HR measured 10 min after cessation of exercise in the present study. On the other hand, the ln LF/HF measured 20 min after exercise cessation was significantly decreased by the endurance training with a decrease in HR and increases in the ln HF power and SDNN. As shown in Table 2, Δ ln HF power measured both 10 min and 20 min after exercise was correlated with Δ HR. The relationship between Δ HR and Δ ln LF/HF existed only when measured 20 min after exercise. These data suggest that the effects of cardiac autonomic controls on a more rapid recovery in HR induced by endurance training may be different when measured 10 min and 20 min after exercise cessation.
Comparison of changes in cardiac autonomic control measured at rest and during postexercise recovery periods.
It is interesting that endurance training resulted in no significant changes in any parameters measured during the postexercise recovery periods from the 7th day to the 42nd day of the training period despite the measured-at-rest changes which occurred between that time. This result suggests that adaptations of HR and cardiac ANS modulation measured during postexercise recovery periods may be achieved in the short term, such as the first 7 d of the training program. In all measurements taken at rest and 10 min and 20 min after exercise cessation, the amount of change in HR before and after the training period was about 15 bpm. In other words, the amount of change in HR during the postexercise recovery periods for the first 7 d of the training program corresponded to the adaptation, which was needed for 42 d at rest. Obviously, the adaptations of HR and cardiac ANS modulation that occur during the postexercise recovery period occur quickly when compared with those measured at rest. These results suggest that under conditions of endurance training there are differences in the adaptabilities of cardiac autonomic control between at rest and postexercise recovery periods.
Although the factors that exerts an influence on cardiac autonomic control are central command and afferent stimulation from chemoreflex or baroreflex functions, the mechanisms of cardiac autonomic adaptation at rest and during postexercise recovery periods after endurance training remain unclear. Training-associated changes in baroreflex control of HR have been proposed. Although the experimental findings have been remarkably inconsistent (22,24,25), the possibility of the adaptation in baroreflex function cannot be removed as a possible factor in the differences between the cardiac autonomic adaptation at rest and during recovery. Furthermore, previous studies (18,29) suggest that endurance training induces a lower level of muscle chemoreflex stimulation as the result of the increased oxidative metabolic capacity of the exercising muscle during exercise. We, therefore, speculate that the difference in the adaptabilities of cardiac autonomic control at rest and during recovery phases is due to the difference in the mechanism of the adaptation between these phases.
Methodological limitations in the present study.
The present study used HR variability analysis for estimation of cardiac ANS modulation. A major advantage of this method is the possibility of repeated measurements with the same subject, because it can explore noninvasively the sympathovagal interaction under different conditions. The present study observed changes in HR and cardiac ANS modulation measured at rest and during postexercise recovery periods over the training program of 6 wk. However, breathing patterns and changes in tidal volume can affect a respiratory sinus arrhythmia, i.e., the HF power as index of parasympathetic modulation (8,15). Also, Strano et al. (30) concluded that because athletes usually breathe slowly, and because slow breathing influences spectral LF component, HR variability power spectra in athletes should be assessed under controlled respiration, which does not alter ANS modulation. In the present study, the breathing pattern does not affect the HF power because all subjects maintained respiratory rates of 0.25 Hz during all measurements. However, ventilatory tidal volumes were not directly measured. When measured during the postexercise recovery periods, the effect of changes in tidal volume on the HF power may be larger than that at rest. Because there is the possibility that the acceleration of ventilation is retained during the recovery phase after intense exercise as used in the present study. Thus, if the tidal volume is controlled, cardiac ANS modulation could be measured more accurately both at rest and during the postexercise recovery periods.
The present study, using analysis of HR variability, longitudinally examined the effects of endurance training on HR and cardiac ANS modulation measured at rest and during postexercise recovery periods. With endurance training, changes in cardiac ANS modulation partly contribute to a decrease in HR measured at rest and during postexercise recovery periods. The effects of adaptability of the cardiac autonomic control to endurance training occurs sooner in immediate postexercise recovery periods than at rest.
The authors gratefully acknowledge Dr. Junichiro Hayano (Nagoya City University Medical School) for advice on this research. This study was partly supported by grant-in-aid for scientific research (A) of the Ministry of Education, Science, Sports, and Culture (No. 09308002). We are grateful to Mr. Mitch Breece for his generous help in the writing of the English manuscript.
Address for correspondence: Motohiko Miyachi, Ph.D., Department of Health and Sports Sciences, Kawasaki University of Medical Welfare, Kurashiki, Okayama 701–0193 Japan; E-mail miyachi@ mw.kawasaki-m.ac.jp.
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