Systemic energy demand and pulmonary O2 uptake (V˙O2) increase almost linearly or accelerate slightly at high intensity during incremental whole-body exercise (5,11), whereas local muscle O2 metabolism is altered nonlinearly (7,14,27,28,35,40,44); muscle deoxygenation, monitored by near-infrared spectroscopy (NIRS), follows an S-shaped profile and the response displays a slowdown or plateau point (the attenuation point of muscle deoxygenation (APMD)) at high intensity despite further increase in V˙O2. The mechanisms responsible for the occurrence of APMD are still unclear. As a working muscle is capable of consuming O2 when the O2 supply is in excess, e.g., under hyperoxic conditions (43), it may not be considered that muscle O2 extraction reaches the maximum at APMD. Because muscle energy demand continuously increases after APMD, inability to further increase muscle deoxygenation would cause relative muscle O2 insufficiency compared with the O2 demand. This may lead to an increase in anaerobic energy production and the accumulation in metabolic substances, resulting in peripheral fatigue development and then alterations in neuromuscular activity.
Human skeletal muscles are composed of three main fiber types; types I, IIa, and IIx (8). Hence, the recruitment of motor units is generally in the order of smallest to largest motor units and altered by external power output and exercise duration (26). Surface EMG, which is used for noninvasive neuromuscular activity measurements, increases in proportion to the force generation during short-duration muscle activity (33). However, during continuous incremental exercise, EMG signals increase linearly up to moderate intensity and deviate up from linearity below peak V˙O2 (V˙O2peak). This breakpoint is defined as the EMG threshold (EMGT) (24,30,31,41). The reproducibility of EMGT measurements has been previously reported (30). At the EMGT, recruitment of new motor units, particularly those consisting of fast-twitch muscle fibers, occurs to compensate for the loss in contractility of fatiguing motor units (41). In addition, intracellular action potentials would change at this breakpoint because EMG signals are related to peripheral as well as central factors (4).
As mentioned above, if the inability to further increase muscle deoxygenation affects neuromuscular activity via the accumulation of metabolic substances, EMGT would occur after APMD during incremental exercise. However, to the best of our knowledge, no study has examined the relationship between APMD and EMGT. Moreover, this relationship provides no adequate evidence indicating that these breakpoints are mediated by muscle metabolites. To investigate this, the relationship between APMD and EMGT under hypoxic as well as normoxic conditions needed to be clarified. A decrease in arterial O2 content modifies the balance between power output and muscle metabolism (20) and exaggerates the development of peripheral fatigue during whole-body exercise (3,38). Therefore, if the accumulation of muscle metabolites alters neuromuscular activity patterns, it can be hypothesized that APMD precedes EMGT and that this relationship remains unaltered under both normoxic and hypoxic conditions.
The purpose of this study was to examine whether the attenuation of working muscle deoxygenation is related to alteration in neuromuscular activity patterns in different states of muscle oxygenation. To accomplish our goal, we conducted investigations into the relationship between APMD and EMGT during incremental cycling exercise under both normoxic and hypoxic conditions.
Nine active male volunteers participated in this study (age = 23 ± 2 yr, height = 174.1 ± 6.7 cm, body mass = 66.0 ± 5.7 kg (mean ± SD)). Before the experiment, all procedures and any potential risks were explained to each subject, and an informed consent document was signed. This study was approved by the local ethics committee, and all experiments were performed in accordance with the Declaration of Helsinki.
After familiarization with the experimental procedures, the subjects performed two ramp incremental cycling exercise tests in an environmentally simulated room (Espec Engineering, Osaka, Japan) under normoxic or normobaric hypoxic (FIO2 = 0.12, balanced with nitrogen) conditions in a random order. Ambient conditions (temperature = 23.0°C, relative humidity = 50%) were automatically controlled. There was a 48-h interval between each exercise session, and the exercises were performed at the same time on each day. Subjects refrained from caffeine consumption for 12 h and stressful exercise for 48 h before each test.
After calibrating the NIRS signals (see below) and breathing in each gas mixture at rest for at least 15 min to equilibrate body gas stores of O2 and CO2, the subject performed the ramp incremental cycling exercise tests. The protocol followed a warm-up (WU) exercise at 10 W for 4 min and increased at a ramp rate of 20 W·min−1 to exhaustion. An electromagnetically braked cycle ergometer (75XL2; Combi, Tokyo, Japan) was used; the seat and handlebar height remained constant for each subject, and the pedal frequency was maintained at 60 rpm.
Breath-by-breath measurements of pulmonary gas exchange and minute ventilation (V˙ E) were obtained by using a computerized metabolic cart (model Vmax29c; SensorMedics, Homestead, FL). Expiratory flow measurements were performed by using a mass flow sensor that was calibrated before each experiment with a 3-L syringe at three different flow rates. The O2 and CO2 analyzers were calibrated before each experiment. Pulmonary V˙O2 and CO2 output (V˙CO2) were expressed in STPD, and V˙ E was expressed in BTPS. HR was determined from an ECG signal. Arterial blood O2 saturation (Spo2) was continuously monitored noninvasively by a pulse oximeter (OLV-3100; Nihon Kohden, Tokyo, Japan) on the first or second finger. To ensure accuracy of the data, the pulse data were simultaneously measured and confirmed to nearly match HR. Blood lactate concentration (BLa) was measured at the fingertip before exercise, at WU, every 40 W, and after exhaustion, using a blood lactate test meter (Lactate-Pro; Arkray, Kyoto, Japan).
Ventilatory threshold (VT) and respiratory compensation point (RCP) were mathematically determined from the plot of V˙O2 versus V˙CO2 and V˙CO2 versus V˙ E (a V-slope method), respectively (6). The criteria for V˙O2peak were at least three of five as follows: no increase in V˙O2 despite an increase in power output, HR within ±10 bpm of the age-predicted maximum, RER >1.10, BLa >8 mM, and pedal cadence dropping below 55 rpm despite strong verbal encouragement.
Changes in oxygenated (O2Hb) and deoxygenated (HHb) hemoglobin (Hb) and myoglobin (Mb) concentrations, calculated using the modified Beer-Lambert law, were measured with continuous-wave NIRS (NIRO-200; Hamamatsu Photonics, Shizuoka, Japan). The principle, validity, and limitation of the measurements in humans have been previously reported (13,16). The baseline values were obtained while the subject lay on a bed in a temperature- and relative humidity-controlled room under normoxic conditions for at least 10 min. The changes in total Hb (THb) were calculated by adding the changes in O2Hb and HHb. The value of HHb was expressed relative to arterial occlusion (13,16) under normoxic conditions before exposure to each condition; 0% HHb was taken as the baseline value and 100% HHb was taken as the maximum value during arterial occlusion.
Two fiber-optic bundles transmitted the NIR light produced by the laser diodes to the tissue of interest. Three laser diodes of different wavelengths (775, 810, and 850 nm) were used as the light source. The intensity of the transmitted light was measured at 6 Hz. The optodes were housed in a plastic holder, and the position of the optodes relative to each other was fixed. The optodes were placed on the lower third of the vastus lateralis muscle (VL), at a distance of 4 cm from each other. The depth of the measured area was approximately half of the distance between the emitter and receiver, i.e., ∼2 cm (16). The skin overlying the probe was carefully shaved, and the optode assembly secured to the skin was covered with a black cloth to minimize the intrusion of stray light and loss of NIR-transmitted light.
EMG signals were continuously recorded from the lower third of the VL. The skin surface was cleaned with alcohol and abraded with sandpaper. Surface bipolar electrodes (Ag-AgCl, 5 mm contact diameter, 2.0 cm spacing) were aligned in the direction of the muscle fibers. The wires connected to the electrodes were secured with tape to avoid movement-induced artifacts. The surface EMG signals were amplified, and band-pass filtering was set at both low- (100 Hz) and high- (1 kHz) cutoff filters (AG-621G; Nihon Kohden). To evaluate the difference between subjects, the root mean square value of the EMG signal (EMGRMS) was normalized by the value obtained during WU.
The NIRS and EMG signals were simultaneously recorded by a computer (Chart 4.1.2; AD Instruments, Bella Vista, Australia) via an A/D converter (Power Lab 16sp; AD Instruments) at a sampling rate of 4 kHz. The location of the NIRS probe and EMG electrodes was marked on the skin using a pen to ensure the electrodes were placed at the same location in both the tests.
To establish an objective criterion, APMD and EMGT were mathematically calculated using a computer. Piecewise linear regression analysis was applied to the plots of HHb versus power output between VT and V˙O2peak: 1) the first regression line was applied between VT and an arbitrary point, whereas the second regression line was applied between the next point of the arbitrary point of the first line and V˙O2peak; 2) always, the error sum of squares of each regression line was calculated; and 3) when the sum of the error sum of squares of the two lines was minimal, the intersection between the two lines was determined as APMD (28,35) (Fig. 1A). Similarly, EMGT was assessed by the plots of EMGRMS versus power output (24,30,31,41) (Fig. 1B).
All data are represented as mean ± SE. Statistical analyses were performed using the statistical package SPSS for Windows (version 12.0; SPSS, Chicago, IL). Exercise-induced changes in the parameters were compared by two-way ANOVA, with FIO2 and power output as the main effects. On finding significant main effects, the Bonferroni post hoc test was performed. Pearson product-moment correlations were determined between the V˙O2 at RCP, APMD, and EMGT. Values of P < 0.05 were considered significant.
Power output and averaged cardiopulmonary responses at WU, VT, RCP, and V˙O2peak are shown in Table 1. Peak power output and V˙O2peak under hypoxic conditions were significantly reduced by 19.5% ± 2.2% and 22.7% ± 2.7%, respectively. In comparison with the absolute exercise intensity, BLa was significantly higher from 90 to 210 W under hypoxic conditions than under normoxic conditions. However, BLa at V˙O2peak was similar between the two conditions (normoxia = 12.6 ± 0.6 mM, hypoxia = 12.9 ± 0.4 mM).
The responses of V˙O2, THb, HHb, and EMGRMS in a representative subject and the average responses are shown in Figure 2. In addition, THb, HHb, and EMGRMS at WU, VT, RCP, and V˙O2peak are shown in Table 2. The change in THb increased from the start of exercise but reached a plateau after RCP. At the absolute exercise intensity and at V˙O2peak, no significant difference in THb was found between the two conditions. The response of HHb increased as the exercise intensity increased but leveled off at high intensity under both conditions. There was a significant difference in HHb between the two conditions at the absolute exercise intensity and at V˙O2peak. The response of EMGRMS increased nonlinearly under both conditions. The value of EMGRMS at VT and RCP, but not at V˙O2peak, was significantly lower under hypoxic conditions than under normoxic conditions.
Exposure to hypoxic conditions decreased the power outputs at APMD (normoxia = 228 ± 11 W, hypoxia = 190 ± 6 W, P < 0.01) and at EMGT (normoxia = 250 ± 13 W, hypoxia = 210 ± 10 W, P < 0.01). The V˙O2 at APMD significantly differed between the two conditions (P < 0.01); the percent decrease with hypoxia was 17.9% ± 2.7%. Similarly, there was a significant difference in the V˙O2 at EMGT between both conditions (P < 0.01); the percent decrement with hypoxia was 17.7% ± 2.1% (Fig. 3). Pulmonary V˙O2 was significantly higher at EMGT than at APMD (P < 0.01) under both conditions. However, the relationship between APMD and EMGT was significant under both normoxic (r = 0.95, P < 0.01) and hypoxic (r = 0.89, P < 0.01) conditions (Fig. 4). Hence, the V˙O2 at APMD was not significantly different from and was significantly related to that at RCP under normoxic (r = 0.88, P < 0.01) and hypoxic (r = 0.85, P < 0.01) conditions. The %V˙O2peak at APMD was not significantly different between either sets of conditions (normoxia = 74.8% ± 2.2%, hypoxia = 79.4% ± 1.8%, P = 0.14). The %V˙O2peak at EMGT tended to be higher under hypoxic conditions but not significantly different from that under normoxic conditions (normoxia = 82.0% ± 2.5%, hypoxia = 87.3% ± 1.5%, P = 0.08). In addition, HHb at APMD was significantly higher under hypoxic conditions (normoxia = 72.2% ± 5.0%, hypoxia = 91.6% ± 5.4%, P < 0.01), and HHb at EMGT was statistically different between the two conditions (normoxia = 79.6% ± 5.6%, hypoxia = 100.3% ± 6.6%, P < 0.01).
We examined the relationship between the breakpoints of muscle deoxygenation and neuromuscular activity and the effects of acute hypoxia on this relationship during incremental exercise. The main findings of this study are that V˙O2 at APMD was significantly lower than but related to V˙O2 at EMGT and that the significant relationship between APMD and EMGT existed under hypoxic conditions despite decreased V˙O2 at both APMD and EMGT. These findings suggest that the inability to further increase muscle deoxygenation is related to alterations in neuromuscular activity during incremental exercise, regardless of the oxygenation status. Although numerous studies have reported the occurrence of APMD and EMGT, their relationship had not been clarified. Our study may aid in clarifying the unique physiological changes that occur in locomotor muscles before exhaustion and the effects of hypoxia on aerobic performance during whole-body exercise.
The balance between muscle O2 delivery and consumption differs between muscles composed of slow- and fast-twitch muscle fibers (32). Hence, the recruitment patterns of motor units change to match power output and peripheral fatigue development during incremental exercise (26). Thus, it was possible that V˙O2 was similar at APMD and EMGT. However, our results showed that V˙O2 was significantly lower at APMD than at EMGT. In addition, the relationship between APMD and EMGT under hypoxic conditions was similar to that under normoxic conditions although hypoxia modified the muscle anaerobic energy system (20) and decreased V˙O2 at both APMD and EMGT. These findings suggest that an attenuation of muscle deoxygenation might indicate relative muscle O2 insufficiency. This would subsequently increase anaerobic energy production, which would affect group III and IV afferents and central motor output (29), and alter the patterns of neuromuscular activity, probably not only the recruitment and firing rates of motor units but also the intracellular action potentials (4). Moreover, as found in a previous study (28), the V˙O2 at RCP, defined as the breakpoint at which metabolic acidosis is relatively compensated with hyperventilation, was similar to that at APMD. These findings suggest that metabolic acidosis and the accumulation of metabolic substances might accelerate more rapidly after APMD, and the progression of physiological changes could be the trigger for the alteration in neuromuscular activity.
In this study, APMD was defined as the slowdown or plateau point of muscle deoxygenation at high intensity during incremental exercise. Although NIRS cannot measure Hb and Mb separately, it is thought that Hb is predominantly reflected in human muscle studies (13,16). Therefore, APMD might indicate a leveling off of microvascular deoxygenation. Consistent with previous studies (35,40), HHb during incremental exercise was significantly higher under hypoxic conditions; this was mainly attributed to decreased muscle O2 delivery (27). Indeed, Spo2 gradually reduced from VT under hypoxic conditions but not under normoxic conditions. On the other hand, some studies have reported similar muscle deoxygenation at a given exercise intensity between normoxic and hypoxic conditions (1,12,36,39). The differences among studies were predominantly due to working muscle mass, exercise protocol, and FIO2. Further research is needed to elucidate the effects of hypoxia on changes in muscle deoxygenation.
Why muscle deoxygenation is attenuated both at submaximal intensity and at a muscle deoxygenation level below the value during cuff ischemia is unclear (27,44). One of the putative theories is that a decline in the transit time of red blood cells in muscle capillaries along with an increase in microvascular blood velocity may inhibit further deoxygenation (21). This theory was partially supported by our finding of lower V˙O2 at APMD under hypoxic conditions than under normoxic conditions presumably due to the increased muscle blood velocity during submaximal exercise under hypoxic conditions (9). This might reasonably explain the fact that HHb at APMD was lower than that during occlusion (i.e., 100% HHb) because of the theoretically minimal blood flow during occlusion. Another uncertainty concerning APMD is that systemic V˙O2 and O2 extraction continuously increase until V˙O2peak (34) despite an attenuation of muscle deoxygenation. During incremental cycling exercise, cardiac output response assessed by direct methods was reported to level off (34) or increase slightly (10) at high intensity, and the increased rate of cardiac output does not seem to accelerate. Thus, some of the possible explanations concerning further increasing V˙O2 after APMD include a rise in respiratory muscle O2 consumption (17) and a shift in the contribution rates of different muscles against power output and V˙O2 (15,19,23).
We noted that, unlike the other subjects, HHb continuously increased in one subject and APMD was not determined under either conditions. Previous studies (7,14,40) have reported that a few subjects did not exhibit APMD. Their data were excluded in this study because our purpose was to assess the relationship between APMD and EMGT. Further studies are needed to clarify the factors that influence the presence or the absence of APMD.
EMG signals are influenced by central and peripheral factors, and it was recently reported that muscle properties such as prolongation of intracellular action potentials are more related to the signals (4). In this study, contrary to a previous report (31), V˙O2 at EMGT was decreased under hypoxic conditions. This discrepancy in results was mainly attributed to the difference in FIO2, suggesting that moderate hypoxia used in that study minimally affected the occurrence of EMGT. In addition, %V˙O2peak at EMGT was not significantly different between the two conditions, but tended to be increased under hypoxic conditions, indicating that the relative time to exhaustion from EMGT was shorter under hypoxic conditions. This might partly be related to the delay in phosphocreatine resynthesis (18) and the higher fatigability of fast-twitch muscle fibers in hypoxia (22).
In comparison with the absolute exercise intensity until 200 W, hypoxia did not significantly affect EMGRMS. These results, which were consistent with those of a previous study (42), imply that, at the intensity below EMGT, neuromuscular activity was predominantly altered by an external power output because of less activation of metaboreceptors or chemoreceptors. Moreover, EMGRMS at V˙O2peak did not differ statistically between the two conditions. These results were similar to those obtained in some studies (31) but at odds with other studies (2,25,37). It is unclear why different results were obtained, but it might be partly attributed to differences of subjects and exercise protocol. A study by Amann et al. (3) has demonstrated that, during constant-load exercise, EMG at exhaustion was similar between 0.21 and 0.15, but not 0.10 of FIO2 conditions, despite different exercise durations among three FIO2 conditions. These findings imply that EMG at exhaustion during cycling exercise is determined not only by exercise intensity and duration but also by hypoxic level.
In conclusion, we observed that an attenuation of muscle deoxygenation is related to and precedes alterations in neuromuscular activity during incremental cycling exercise. The physiological mechanisms underlying the relationship are still not fully understood, but it is likely that muscle metabolic changes partly play a role. The results of this study contribute to the understanding of the relationship between locomotor muscle O2 metabolism and neuromuscular activity before exhaustion during whole-body aerobic exercise under both normoxic and hypoxic conditions.
The authors received no funding for this work.
The authors thank the subjects in this study.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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Keywords:©2011The American College of Sports Medicine
NEAR-INFRARED SPECTROSCOPY; EMG; MUSCLE METABOLISM; BREAKPOINT; INCREMENTAL EXERCISE