Partial reduction of parasympathetic nerve activity during sleep after endurance exercise under hypoxic conditions
Article information
Abstract
[Purpose]
The present study compared changes in sympathetic and parasympathetic nervous activities during sleep following endurance exercise under either normoxic or hypoxic condition.
[Methods]
Ten young men (20.5 ± 0.2 years) were recruited for the study. All of them carried out three trials on different days: [1] pedaling exercise in hypoxia (FiO2: 14.5%; HYP), [2] pedaling exercise in normoxia (FiO2: 20.9%; NOR), and [3] rest in normoxia (REST). Each trial was separated at least one week, with randomized orders. The exercise in HYP and NOR trials consisted of 60 min of pedaling exercise at 60% of maximal oxygen uptake. During exercise, heart rate (HR), rating of perceived exertion and arterial oxygen saturation (SpO2) were determined. Also, HRV was continuously monitored until next morning (17:00-8:00) to evaluate frequency domain HRV parameters and time domain HRV parameters. On the following morning, the scores of fatigues, sleepiness, vitality, and quality of sleep were measured by visual analog scale.
[Results]
During sleep, majority of frequency domain HRV parameters (LF, HF, LF/HF, Total Power) or time domain HRV parameters (SDNN, RMSSD, NN50) did not differ significantly among three trials, although the average of pNN50 was significantly lower in NOR and HYP trials.
[Conclusion]
Evening endurance exercise under hypoxic conditions did not exacerbate autonomic nerve activity during sleep compared to the same endurance exercise under normoxic conditions. However, despite different inspiratory oxygen levels during exercise (FiO2: 20.9% or 14.5%), evening endurance exercise may partially suppress parasympathetic nerve activity during sleep. These findings would apply to people who are involved in endurance exercise under hypoxic conditions.
INTRODUCTION
Endurance exercise under hypoxic conditions offers significant health benefits to various populations. For instance, moderate-intensity endurance training (90-min sessions, 3 days/week for 8 weeks) under normobaric hypoxic conditions (fraction of inspired oxygen [FiO2] 15%) leads to a greater reduction in body weight compared to equivalent training under normoxic conditions [1]. Similarly, Mai et al. [2] reported improved insulin sensitivity in 32 obese men with metabolic syndrome following 6 weeks of walking (3 × 15-min sessions, 3 days/week at 50–60% of maximum heart rate [HR]) under hypoxic conditions (FiO2 15%). Furthermore, Park et al. [3] demonstrated that combined endurance and resistance training (60-min sessions, 3 days/week) under hypoxic conditions (FiO2 14.5%) improves body composition, physical fitness, and pulmonary function. Similarly, Park et al. [4] found that 6 weeks of interval training (10 × 5-min runs at 90–95% of maximum HR, with 1-min rest intervals, 3 days/week) under hypoxic conditions (FiO2 16.5%) improved arterial stiffness and endothelial function compared with identical training under normoxic conditions. Wiesner et al. [5] revealed that endurance running (60-min sessions, 3 days/week for 4 weeks) at 65% of maximal oxygen uptake (V̇O2max) under hypoxic conditions (FiO2 15%) resulted in a greater reduction in body fat mass compared to identical training under normoxic conditions. These findings indicate that endurance training under hypoxic conditions is a nonpharmacological approach to reducing the risk of cardiovascular diseases [6].
Autonomic nerve activity, including the sympathetic and parasympathetic components, plays a critical role in physiological and psychological functions. Exercise stimulates sympathetic nerve activity, increasing epinephrine and norepinephrine secretion, thereby elevating blood pressure, HR, and gluconeogenesis to meet metabolic demands [7-[9]. Conversely, enhanced parasympathetic activity promotes insulin secretion, leading to a reduction in the plasma glucose concentration. Sympathetic nerve activity increases during endurance exercise under hypoxic conditions [10]. In addition, endurance exercise under hypoxic conditions leads to sustained elevations in epinephrine and norepinephrine concentrations for at least 30–60 min post-exercise, whereas identical exercise under normoxic conditions elicits significantly lower levels [11]. Although this study evaluated sympathetic nerve activity for 60 min after exercise, the overnight changes in sympathetic nervous activity after endurance exercise under hypoxic conditions remain unclear. In addition, sleep quality decreases with sympathetic nerve activity disorder [12] at altitude (hypobaric hypoxic conditions), leading to increased risk of acute mountain sickness (AMS) [13,14]. However, sleep quality under normoxic conditions following exercise under hypoxic conditions remains unclear. Therefore, we compared the overnight changes in sympathetic and parasympathetic nervous system activities following a single session of endurance exercise under normoxic or hypoxic conditions. We hypothesized that endurance exercise under hypoxic conditions in the evening would impair autonomic nerve activity during sleep compared to endurance exercise in the evening under normoxic conditions.
METHODS
Participants
Ten healthy young men participated in the study. The mean age, height, weight, body fat percentage, body mass index, V̇O2max, and workload (60% V̇O2max) of the participants were 20.5 ± 0.7 years, 171.1 ± 4.4 cm, 65.6 ± 8.0 kg, 14.3 ± 5.4 %, 22.4 ± 2.5 kg/m2, 43 ± 4 ml/kg/min, and 114 ± 15 W, respectively. The sample size was calculated using G-power (G*Power version 3.1.9.7; Heinrich-Heine University, Dusseldorf, Germany). The results indicated that the minimum sample size was 9 (effect size = 0.5, α = 0.05, power [1-β] = 0.8). Therefore, we recruited 10 participants considering the dropout rate. All participants were healthy with no medical conditions or regular exercise habits at the start of the study. Considering the impact of the menstrual cycle on autonomic nerve regulation [15], we recruited only male participants. Exclusion criteria were 1) history of cardiovascular disease and smoking, 2) medication use, and 3) sleep disorders. The participants were informed about the experimental design and potential risks associated with the study. Written informed consent was obtained from all participants. The present study was approved by the Research Ethics Committees of Ritsumeikan University, Japan (BKC-LSMH-2022-024).
Experimental protocol
We used a crossover study with a randomized design; all participants completed three distinct trials, including endurance exercise under hypoxic conditions (HYP), endurance exercise under normoxic conditions (NOR), and rest under normoxic conditions (REST). Participants visited the laboratory on four separate occasions. The initial visit involved a V̇O2max assessment using a cycle ergometer (AEROBIKE 75XLⅢ; KONAMI, Tokyo, Japan) under normoxic conditions (FiO2 20.9%).
Figure 1 illustrates the experimental design of the second through fourth sessions. During these sessions, all participants completed three distinct trials: HYP (FiO2 14.5%, a simulated altitude of 3,000 m), NOR (FiO2 20.9%), and REST (FiO2 20.9%). In the NOR and HYP trials, participants performed a 60-min cycling exercise on a cycle ergometer (AEROBIKE 75XLⅢ) at an intensity of 60% V̇O2max (70 rpm). In the REST trial, the participants remained seated for 60 min under normoxic conditions, matching the exercise duration of the HYP and NOR trials. To minimize psychological effects, the participants were blinded to the oxygen concentration (20.9% or 14.5%). The participants were instructed to avoid caffeine and alcohol consumption and vigorous exercise at least 24 h before the measurements of each trial. Sufficient sleep was also ensured during the last night of the measurements.
The trials were conducted 7 days apart. A standardized meal (2,663 kcal, 14.7% protein, 28.4% fat, and 56.5% carbohydrates) was provided in all three trials. On the main experimental days, participants were restricted to the prescribed exercise. During the 60-min exercise period (NOR and HYP) and the equivalent rest period (REST), heart rate (HR), peripheral arterial oxygen saturation (SpO2), and rating of perceived exertion (RPE) were continuously monitored. Autonomic nerve activity was continuously monitored overnight. The next morning, the participants assessed their subjective fatigue, sleepiness, vitality, and sleep quality using a 100-mm visual analog scale.
Measurements
V̇O2max (preliminary assessment)
V̇O2max was assessed under normoxic conditions by using a cycle ergometer (AEROBIKE 75XLⅢ; KONAMI, Tokyo, Japan). The participants maintained a constant cadence at 70 rpm. The incremental exercise test was initiated at a workload of 70 W, with subsequent 30 W increments every 2 min until volitional exhaustion. Exhaustion was defined as the inability to maintain the target cadence for 5 s. Expired gases were collected breath-by-breath and analyzed using an automatic gas analyzer (AE300S; Minato Medical Science, Tokyo, Japan). Respiratory data were averaged every 30 s. HR was monitored continuously using a wireless HR monitor (Accurex Plus; Polar Electro Oy, Kempele, Finland). In addition, RPE was evaluated every 2 min using a 0–10 Borg scale [16].
Autonomic nerve activity assessment
Autonomic nerve activity was evaluated based on HR variability (HRV) using a wearable heartbeat monitor (my-Beat WHS-1; Union Tool, Tokyo, Japan). This sensor has been previously utilized to evaluate HRV [17-19]. The participants wore the sensor on their left chest (approximately 10 cm below the clavicle bone) overnight until the following morning (8:00 AM). All autonomic nerve activity data were processed using automatic filtering software (RRI analyzer 2; Union Tool). The frequency-domain (low-frequency power [LF], high-frequency power [HF], LF/HF ratio, and total power) and time-domain (standard deviation of NN intervals [SDNN], root mean square of successive differences in RR intervals [RMSSD], number of differences in successive RR intervals greater than 50 ms [NN50], and proportion of NN50 relative to all NN intervals [pNN50]) parameters were calculated.
HR, SpO2, and RPE
HR was continuously monitored using a wireless HR monitor (Accurex Plus; Polar Electro., Kempele, Finland) 10 min before the onset of endurance exercise or rest. SpO2 was continuously monitored using a finger pulse oximeter (ATP-W03; Fukuda Denshi, Tokyo, Japan) during the same period. The RPE was evaluated every 10 min during the endurance exercises using a 0–10 Borg scale [16].
Subjective scores
In the morning following the trials, the participants rated their subjective feelings of tiredness, sleepiness, vitality, and sleep quality using a 100-mm visual analog scale.
Statistical analyses
All data are presented as means ± standard deviation (SD). Shapiro–Wilk and Levene tests were utilized to confirm the normality of the data distribution and homogeneity of variance. For the comparison of data among the three trials, one-way repeated-measure analysis of variance (ANOVA) was used. When a significant main effect was observed, post hoc comparisons were conducted using the Tukey–Kramer test. P-values < 0.05 were considered statistically significant.
RESULTS
HR, SpO2, and RPE during the exercise
Table 1 presents the mean HR, SpO2, and RPE during the exercise. No significant differences were observed in the HR and RPE between the HYP and NOR trials (P > 0.05). However, SpO2 was significantly lower in the HYP trial than in the NOR trial (P < 0.001).
Autonomic nerve activity
Figure 2 shows the mean LF/HF ratio during sleep. No significant differences were observed in the LF/HF ratios across the three trials (P > 0.05). Figure 3A–3D shows the mean SDNN, RMSSD, NN50, and pNN50 during sleep. Although SDNN, RMSSD, and NN50 did not differ significantly across the three trials (P > 0.05), pNN50 was significantly lower in the HYP and NOR trials than in the REST trial (P < 0.05).
Averages of SDNN (A), RMSSD (B), NN50 (C), and pNN50 (D) during sleep.
Values are means ± SD. †; P < 0.05 vs. HYP, §; P < 0.05 vs. NOR.
Table 2 shows the mean RR interval, HR, and frequency-domain HRV parameters (LF, HF, and total power) during sleep. No significant differences were observed among these variables across the three trials (P > 0.05).
DISCUSSION
Our findings revealed that most frequency-domain (LF, HF, LF/HF, and total power) and time-domain (SDNN, RMSSD, and NN50) HRV parameters did not exhibit significant differences among the three trials. However, the mean pNN50 was significantly lower in the NOR and HYP trials than in the REST trial. These findings indicate that evening endurance exercise under hypoxic conditions did not impair all parameters of parasympathetic nervous activity during sleep compared with the same endurance exercise under normoxic conditions. However, evening endurance exercise, regardless of oxygen concentration, may partially influence autonomic nerve activity during sleep.
Previous studies have demonstrated increased sympathetic nerve activity under hypoxic conditions [20]. However, our findings indicate that evening endurance exercise under hypoxic conditions had minimal impact on sympathetic nerve activity during sleep. With a 6-h recovery period between exercise completion and sleep onset, our study revealed no significant alterations in most HRV parameters, indicating that autonomic nerve activity during sleep was not significantly affected by evening endurance exercise under hypoxic conditions. We were unable to control the activities on the testing days except for identical bedtime among the three trials. Thus, we cannot present detailed time course changes in HRV parameters from the end of the exercise to the onset of sleep. A significant reduction in pNN50, a marker of parasympathetic nerve activity, was observed during the NOR and HYP trials compared with the REST trial. This decrease in parasympathetic activity during sleep was specific to pNN50, as the other time-domain (SDNN, RMSSD, and NN50) and frequency-domain (LF, HF, LF/HF ratio, and total power) HRV parameters did not exhibit significant differences among the three trials. Consistent with our findings, Seo et al. [21] demonstrated significant alterations in NN50 and pNN50 following high-intensity interval training (HIIT) and sprint interval training under normoxic conditions. However, they evaluated HRV parameters immediately after the exercise, and the exercise protocol utilized was different from that of the present study. In our results, only pNN50 showed a significantly lower value after both exercise trials (NOR and HYP trials) compared to the REST trial. These findings suggest that parasympathetic nerve activity during sleep was diminished after exercise in both normoxic and hypoxic conditions. However, caution is required because the significant difference was limited to pNN50, and other parameters (e.g., RMSSD and NN50) did not differ significantly among the three trials. Furthermore, the subjective sleep quality scores did not differ significantly among the three trials. In a previous study [22], reduced HF during sleep was associated with impaired sleep quality, as evaluated using the Multiple Sleep Latency Test and Stanford Sleepiness Scale. In the present study, the significant reduction in pNN50 during sleep in the HYP and NOR trials did not adversely affect the subjective sleep quality. However, further measurements may be necessary because of the lack of objective sleep assessments (e.g., polysomnography).
Our study has several limitations. First, the sample size was relatively small (n = 10), and significant interindividual variability was observed. Further studies with larger sample sizes are required to validate these findings. Second, although the workload was matched between the HYP and NOR trials, the lower V̇O2max in hypoxic conditions resulted in a higher relative exercise intensity in the HYP trial [23]. Because V̇O2max decreases [24] under hypoxic conditions, physical strain is expected to be greater under hypoxic conditions. In future studies, similar comparisons under relatively matched workloads should be performed. Third, the study included only young, healthy males, limiting the applicability of these findings to other populations, such as females and the older individuals. Finally, the experiments were conducted in the evening. Although exercise timing may influence biological responses during sleep, its effects have been inconsistent across studies [25]. Burgness et al. [26] found no effect of exercise timing or modality on sleep quality, whereas Goldberg et al. [27] reported varying effects. Future studies investigating the effects of exercise at different times of day are required.
In conclusion, evening endurance exercise under hypoxic conditions did not exacerbate autonomic nerve activity during sleep compared to the same endurance exercise under normoxic conditions. However, despite different inspiratory oxygen levels during exercise (FiO2: 20.9% or 14.5%), evening endurance exercise may partially suppress parasympathetic nerve activity during sleep. These findings would apply to people who are involved in endurance exercise under hypoxic conditions.
Acknowledgements
This study was supported by a research grant from the Ritsumeikan University. We thank all the participants of the study.