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Sex-Related Differences in Performance Fatigability Independent of Blood Flow Following a Sustained Muscle Action at a Low Perceptual Intensity

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Abstract

The purpose of this investigation was to use the RPE clamp protocol to examine sex-related differences in performance fatigability and neuromuscular responses as the result of a sustained isometric leg extension muscle action anchored to RPE = 2. Twenty adults (10 men, 10 women) performed sustained muscle actions at RPE = 2 for 5-min. Maximal voluntary isometric contractions (MVIC) were performed prior to and following the sustained muscle actions. Neuromuscular (electromyographic and mechanomyographic) parameters and force were recorded, and the values were normalized to respective MVICs and calculated every 5% across the 5-min work bout. Femoral artery blood flow (FABF) was assessed at pretest, immediately posttest, and 5-min posttest. Polynomial regression was used to define the individual and composite normalized neuromuscular and force versus time relationships during the sustained muscle action. Mixed factorial ANOVAs were used to examine differences in performance fatigability and blood flow. For performance fatigability, the men (62.4 ± 14.4 kg–43.1 ± 11.5 kg) exhibited a significantly (P < 0.05) greater decrease pretest to posttest in MVIC than the women (44.1 ± 4.8 kg vs. 38.1 ± 6.1 kg). There were different fatigue-induced neuromuscular patterns of responses between the men and women across time. For blood flow responses, however, there was no sex-related difference, but pretest (283.3 ± 70.8 mL/min) was significantly (P < 0.05) less than immediately posttest (424.5 ± 133.5 mL/min) and 5-min posttest (324.4 ± 78.3 mL/min). Thus, men demonstrated a greater degree of performance fatigability than the women, which was independent of differences in FABF. Factors such as the neuromuscular system and muscle morphology likely contributed to the difference in performance fatigability.

Introduction

Ratings of perceived exertion (RPE) are often integrated into resistance training to prescribe exercise intensity [13, 16, 21, 30, 31]. Little is known, however, regarding the specific relationships between RPE and physiological mechanisms associated with fatigue resulting from resistance exercise [13, 16, 21, 29, 37]. A limited number of previous aerobic [6, 14, 19] and resistance [21, 29] exercise studies have utilized the RPE clamp model [39] to examine fatigue-induced changes in various physiological outcome variables such as blood pressure, oxygen consumption, neuromuscular parameters, power output, and force. A common outcome of both the aerobic [6, 14, 19] and resistance exercise [21, 29] investigations is that it is necessary to reduce power output or force, respectively, to maintain a constant RPE.

Our recent investigation in women [21] utilized the RPE clamp protocol to examine the unique neuromuscular patterns of responses for muscle actions anchored to RPE. Typically, in response to fatigue resulting from a muscle action anchored to force, there are changes in motor unit activation strategies that include increases in muscle activation [electromyography (EMG) amplitude (AMP)] and motor unit recruitment [mechanomyography (MMG) AMP], as well as decreases in action potential conduction velocity [EMG mean power frequency (MPF)] and global motor unit firing rate (MMG MPF) [2, 12]. Our previous results demonstrated, however, that when force is anchored to RPE, there were increases in MMG AMP, but no simultaneous changes in EMG AMP or EMG MPF [21]. Previous studies have suggested that anchoring to both RPE [21] and force [2, 12] result in fatigue-induced decreases in maximal voluntary isometric contraction (MVIC). Despite similar decreases in MVIC, however, our previous results [21] demonstrate that there are unique fatigue-induced neuromuscular responses reliant upon anchoring strategy. These differences are likely associated with the ability to freely reduce force [21, 29] using the RPE clamp protocol [39], but not when the task was anchored to a constant force. It is unknown, however, if the men and women demonstrate the same decreases in performance and similar neuromuscular patterns of responses following a fatiguing task anchored to RPE.

Performance fatigability has been defined as the magnitude or rate of change in an objective measure of performance relative to a reference value over a discrete amount of time [23]. Recently, Enoka and Duchateau [10] suggested that investigations of performance fatigability should focus on outcome variables that characterize “real-world performance” (p. 2228) such as the duration that a task can be sustained, the perception of exertion using RPE, and changes in MVIC. Yoon et al. [40] as well as Maughan et al. [28] have shown that men had shorter times to task failure than women following sustained isometric unilateral forearm flexor and leg extension muscle actions at 20% of MVIC, respectively. These differences have primarily been observed following sustained muscle actions at low relative forces [17, 18, 28, 40] and attributed to differences in muscle blood flow [5, 33]. Hunter [17] has recently reviewed sex-related differences in performance fatigability and indicated, “…average magnitude of the sex differences across all intensities for sustained isometric muscle contractions is ~ 23%,” (p. 115) [18]. Despite Enoka and Duchateau [10] stating that there is an interaction between performance fatigability and perceived fatigability, no previous studies have examined sex-related differences following a fatiguing task anchored to a low perceptual-based intensity. Therefore, the purpose of the present study was to use the RPE clamp protocol [39], to examine possible sex-related differences in performance fatigability and neuromuscular responses as the result of a sustained isometric leg extension muscle action anchored to RPE = 2. Based on previous studies [5, 28, 40] and the low perceptual intensity of the sustained muscle action, it was hypothesized that men would exhibit a greater degree of performance fatigability, which would lead to differences in neuromuscular patterns of responses across time. In addition, the neuromuscular responses would track RPE, but not force [21]. It was also hypothesized that the men would exhibit a greater fatigue-related muscle blood flow response than the women due to differences in absolute strength.

Materials and Methods

Twenty adults (10 men: 22.9 ± 2.0 years, 180.6 ± 7.3 cm, 79.8 ± 8.5 kg and 10 women: 23.1 ± 2.3 years, 172.5 ± 10.1 cm, 77.1 ± 26.6 kg) with no known cardiovascular, metabolic, or muscular diseases volunteered to participate in this investigation. The participants were part of a large multi-independent and dependent variable study and the women were participants in our previous study [21], but there is no overlap in data presented here and our previous study except for age, height, and body weight. The participants visited the laboratory for a total of 4 visits (3 experimental visits and 1 familiarization visit) separated by at least 24 h, and all testing was scheduled at approximately the same time of day. The present investigation utilized data from 1 of the 3 experimental visits. The University Institutional Review Board for Human Participants approved the study (IRB Approval #: 20170416950EP) and during the familiarization visit all participants completed a health history questionnaire and signed a written informed consent prior to testing.

During the familiarization visit, the participant’s dominant leg (based on kicking preference), height, and body weight were recorded. The participants were oriented to their seated position on the isokinetic dynamometer (Cybex II, Cybex International Inc. Medway, MA, USA). In addition, the participants were familiarized with the 10-point Omnibus—Resistance Scale (OMNI-RES) of Robertson [31] and read the anchoring instructions, which were based on previously established recommendations and work [22].

The participants again were read the OMNI-RES anchoring instructions and performed a warm-up. After the warmup, the participants were reminded of the anchoring instructions before completing 2, pretest 6-s MVIC trials. The trial with the highest force value was used for subsequent normalization. Following the MVIC trials, the participant performed a sustained, submaximal isometric leg extension muscle action at an intensity anchored at RPE = 2. During the sustained muscle actions, the participants were blinded to the force output. In addition, the participants were not informed of the maximal time-limit (5-min) and were instructed to adjust their force to maintain a level of perceived exertion equivalent to an RPE = 2. The RPE = 2 and maximal time-limit of 5-min were selected based pilot work, which indicated that the participants would be able to sustain an RPE = 2 for the entire 5-min duration, while also exhibiting measurable fatigue-induced decreases in MVIC. Furthermore, during the sustained muscle actions, the participants were reminded to be attentive to sensations such as strain, intensity, discomfort, and fatigue felt during contractions to facilitate appropriate levels of effort. The participants were continuously assured that there were no incorrect contractions or perceptions and were reminded to always relate levels of exertion to the previously set anchors. Immediately following each sustained isometric leg extension muscle action, 2 posttest MVICs were completed. All MVIC and sustained isometric leg extension testing was completed on a calibrated Cybex II isokinetic dynamometer at a knee joint angle of 120° (180° = full extension), and force production was as measured using a low-profile pancake load cell (Honeywell Model 41, Morris Plains, NJ, USA) attached to end the dynamometer lever arm.

Surface EMG signals were collected with pre-gelled electrodes (Ag/AgCl, AccuSensor, Lynn Medical, Wixom, MI, USA) that were placed in a bipolar arrangement (3 cm center-to-center) on the vastus lateralis of the dominant thigh according to the SENIAM recommendations. Mechanomyographic signals were recorded simultaneously with EMG using an accelerometer (Entran EGAS FT 10, bandwidth 0–200 Hz, dimensions: 1.0 × 1.0 × 0.5 cm, mass: 1.0 g, sensitivity 649.5 mV/g) placed between the proximal and distal EMG electrodes of the bipolar arrangement using double-sided adhesive tape.

The raw EMG and MMG signals were digitized at 2000 Hz with a 32-bit analog-to-digital converter (Model MP150, Biopac Systems, Inc.). The EMG signals were amplified (gain: 1000×) using differential amplifiers (EMG 100c, Biopac Systems, Inc., Santa Barbara, CA, USA). Furthermore, the EMG and MMG signals were zero-meaned and digitally bandpass filtered (fourth-order Butterworth) at 10–500 Hz and 5–100 Hz, respectively. Fast Fourier transform was used to derive the power density spectrum for both signals, and all signal analyses were performed offline with custom written programs utilizing LabView software. One second epoch lengths were utilized to calculate the AMP (root mean square) for the EMG (µVrms) and MMG (m/s2) signals as well as the MPF values for both signals (in Hz).

Femoral artery blood flow (FABF) was assessed from the common femoral artery of the dominant leg, distal to the inguinal ligament and proximal to the bifurcation with a Dopper ultrasound machine (GE Logiq e, USA) and multifrequency linear array probe (12L-Rs; 5–13 MHz; 38.4 mm field-of-view). All measurements were performed at a constant insonation angle of 60° using Pulse Wave Doppler, and the FABF values were derived from the following equation:

$$\begin{aligned} Femoral\, Artery\, Blood \,Flow \,\left( {{\text{mL}}/{\min} } \right) & = blood\, velocity \, \left( {{\text{cm}}/{\text{s}} } \right) \times \pi \\ & \quad \times \left( {\frac{{femoral \,diameter \, \left( {{\text{cm}}} \right)}}{2}} \right)^{2} \times 60. \\ \end{aligned}$$

In addition, FABF was assessed at pretest (prior MVICs and the sustained, submaximal, isometric leg extension), immediately posttest (immediately following the posttest MVICs and within 45 s of completing the sustained, submaximal, isometric leg extension), and 5-min posttest (299 ± 5 s after completing the sustained, submaximal, isometric leg extension) during the experimental visit.

The EMG AMP, EMG MPF, MMG AMP, MMG MPF, and force values were normalized to the corresponding MVIC values. Polynomial regression (linear and quadratic) analyses were used to define the individual and composite normalized EMG AMP, EMG MPF, MMG AMP, MMG MPF, and force versus normalized time (every 5% of the actual time-limit) relationships during the sustained, submaximal isometric leg extensions at RPE = 2. A 2 (sex: male and female) × 2 (test: pretest and posttest) mixed factorial ANOVA was used to examine mean differences in performance fatigability (absolute MVIC values) as well as a 2 (sex: male and female) × 3 (time: pretest, immediately posttest, and 5-min posttest) mixed model ANOVA for FABF values. Partial eta squared (\( {\eta }_{p}^{2}\)) and Cohen’s d were used to describe the effect size of each ANOVA and pairwise comparison, respectively. A P value ≤ 0.05 was considered statistically significant for all analyses, and the analyses were conducted using Statistical Package for the Social Sciences software (version 25.0. SPSS Inc. Chicago, IL, USA).

Results

All participants maintained RPE = 2 for 5-min (300.0 s), and for performance fatigability (absolute force), the 2 (sex: men and women) × 2 (time: pretest and posttest) mixed factorial ANOVA indicated there was a significant (P < 0.001; \( {\eta }_{p}^{2}\) = 0.508) interaction. The follow-up paired t tests for the pretest versus posttest MVICs were significant (P < 0.001; d = 1.48 and P = 0.001; d = 1.09) for the men (62.4 ± 14.4 kg vs. 43.1 ± 11.5 kg) and women (44.1 ± 4.8 kg vs. 38.1 ± 6.1 kg), respectively. Follow-up independent t tests indicated that the pretest MVIC of the men was significantly (P = 0.003; d = 1.68) greater than the pretest MVIC of the women, but there was no difference (P = 0.240) between the men and women for posttest MVICs (Fig. 1).

Fig. 1
figure1

Mean (± SD) force values resulting from the MVIC pretest and posttest trials for the men (a) and women (b) with individual observations represented with numbers corresponding to participant numbers on Tables 1 and 2, respectively. * demarcates a significant mean decrease pretest to posttest MVIC; † demarcates that the pretest MVIC for the men was significantly greater than the pretest of the women

Individual and composite responses for the normalized EMG AMP, EMG MPF, MMG AMP, MMG MPF, and force values versus time relationships for the men and women during the sustained muscle actions are presented in Tables 1 and 2 (Fig. 2).

Table 1 Polynomial regression model, r, and P values (if significant) for normalized EMG AMP, EMG MPF, MMG AMP, MMG MPF, and force vs. time relationships for the men during the sustained, submaximal isometric leg extension anchored to RPE = 2
Table 2 Polynomial regression model, r, and P values (if significant) for normalized EMG AMP, EMG MPF, MMG AMP, MMG MPF, and force vs. time relationships for the women during the sustained, submaximal isometric leg extension anchored to RPE = 2
Fig. 2
figure2

Mean (± SD) normalized force (diamonds), EMG AMP (circles), EMG MPF (squares), MMG AMP (upward triangles), and MMG MPF (downward triangle) values and corresponding trendlines resulting from polynomial regression analysis (quadratic or linear) for the sustained isometric leg extension muscle action at RPE = 2 for the men (a) and women (b)

For the men, the normalized individual and composite EMG AMP responses indicated that there were significant, negative, quadratic relationships (r = − 0.738 and − 0.977) for 2 of the 10 participants as well as the composite, significant, positive, quadratic relationships (0.761–0.891) for 3 participants, and no significant relationship for 5 participants. For the normalized individual and composite EMG MPF responses, there were significant, negative, quadratic relationships (r = − 0.721 to − 0.771) for 3 participants as well as for the composite, a significant, positive, quadratic relation for 1 participant, a linear, negative relationship (r = − 0.513) for 1 participant, and no significant relationships for 5 participants. For the normalized individual and composite MMG AMP responses, there were significant, positive, quadratic relationships (r = 0.741–0.855) for 7 of the 10 participants as well as for the composite, a significant, negative, quadratic relationship (r = − 0.588) for 1 participant, and no significant relationship for 2 participants. For the normalized individual and composite MMG MPF responses, there were significant, negative, quadratic relationships (r = − 0.664 and − 0.767) for 2 of the 10 participants as well as for the composite, and no significant relationships for the remaining 8 participants. For force, all 10 participants and composite exhibited significant, negative, quadratic relationships (r = − 0.739 to − 0.987).

For the women, the normalized individual and composite EMG AMP responses indicated that there were significant, negative, quadratic relationships (r = − 0.782 to − 0.899) for 4 of the 10 participants as well as for the composite, significant, positive, quadratic relationships (0.884 and 0.936) for 2 participants, and no significant relationships for 4 participants. For the normalized individual and composite EMG MPF responses, there were significant, negative, quadratic relationships (r = − 0.626 and − 0.894) for 2 participants, a significant linear, positive relationship (r = 0.481) for 1 participant, no significant relationships for 7 participants, and a significant, negative, linear relationship (r = − 0.462) for the composite response. For the normalized individual and composite MMG AMP responses, there were significant, negative, quadratic relationships (r = − 0.601 and − 0.751) for 2 of the 10 participants, significant, positive, quadratic relationships (r = 0.605–0.906) for 5 participants, and no significant relationships for 3 participants or for the composite. For the normalized MMG MPF the were no significant relationships for any of the ten individuals or the composite responses. For force, all ten participants and composite exhibited significant, negative, quadratic relationships (r = − 0.783 to − 0.989).

For FABF, the 2 (sex: men and women) × 3 (time: pretest, immediately posttest, and 5-min posttest) mixed factorial ANOVA indicated there was no significant interaction (P = 0.223). There was, however, a significant (P < 0.001; \({\eta }_{p}^{2}\) = 0.463) main effect for time, but not sex (P = 0.780). As seen in Fig. 3c, the pairwise comparisons for time (collapsed across sex) indicated that the Pretest FABF (283.3 ± 70.8 mL/min) was significantly (P < 0.001; d = 1.32 and P = 0.008; d = 0.551) less than immediately posttest (424.5 ± 133.5 mL/min) and 5-min posttest (324.4 ± 78.3 mL/min).

Fig. 3
figure3

Mean (± SD) femoral artery blood flow (FABF) response values at pretest, immediately posttest, and 5-min posttest are shown for the men (a) and women (b) with individual observations represented with numbers corresponding to participant numbers on Tables 1 and 2, respectively. * demarcates a significant increase in FABF compared to pretest from the mean values (collapsed across sex) in c

Discussion

The results of the present study indicated that all subjects were able to sustain the fatiguing muscle action anchored to RPE = 2 for the maximal time-limit (300 s) and reduced force to maintain RPE = 2. The men, however, were stronger and exhibited greater performance fatigability than the women following the sustain muscle action. From the pretest to posttest MVIC, the men demonstrated a 30.9% decrease in force, while the women showed a 13.6% decrease (Fig. 1). Furthermore, during the sustained muscle action at RPE = 2, the men decreased force nearly twofold more than the women (61.0% vs. 34.7%). These findings were typical of fatigue-related differences between men and women [17, 28, 33, 35, 36], but this is the first study to report a sex-related difference in performance fatigability following a muscle action anchored to a perception of exertion as opposed to a relative force value. Typically, sex-related differences are more pronounced following low-intensity than high-intensity sustained isometric muscle actions due to differences in the amount of muscle mass activated, which, in theory, leads to differences in muscle blood flow and neuromuscular responses between men and women [5, 17, 18, 28, 36]. For example, Clark et al. [5] examined men and women who performed sustained isometric leg extension muscle actions at 25% of MVIC and reported that the women exhibited a 21.3% longer time to exhaustion and greater (39.8%) relative muscle activation (EMG AMP) at task failure than the men. Both sex-related differences (time to exhaustion and muscle activation) disappeared when repeated under an ischemic condition [5], which suggested that the differences were blood flow dependent [33]. Furthermore, Sars et al. [35] recently hypothesized that sex-related differences in performance fatigability may be more influenced by peripheral factors such as fiber type distribution and intramuscular pressure than central factors such as neural drive and corticospinal excitability. Hunter [18] has previously described “…the magnitude of the sex-differences is specific to the task performed…” (p. 114). Thus, in conjunction with previous studies of low-intensity muscle actions [5, 28, 40], the present investigation provided evidence to support that there are observable sex-related differences in performance fatigability following fatiguing muscle actions anchored to a low constant perception of exertion as well as low relative force values. It was postulated that factors such as neuromuscular activation patterns and muscle blood flow contribute to the sex-related differences in performance fatigability at low relative forces [5, 17, 18, 28, 33, 36, 40] as well as low perceptions of exertion.

Neuromuscular responses have been used to make inferences regarding the motor unit activation strategies utilized to complete fatiguing tasks [11, 24]. Typically, the neuromuscular patterns of responses during a sustained, fatiguing, submaximal, isometric muscle action anchored to force are characterized by increases in the amplitude and decreases in the frequency contents of EMG and MMG signals [2, 12], which reflect increases in muscle activation (EMG AMP) and motor unit recruitment (MMG AMP), as well as decreases in the global motor unit firing rate (MMG MPF) and muscle fiber action potential conduction velocity (EMG MPF) [2, 12, 25]. Neuromuscular responses during fatiguing tasks anchored to RPE [6], however, are typically different from those anchored to force [21]. For example, the current study found that the composite (data averaged across subjects) responses for the men and women exhibited decreases in muscle activation (EMG AMP) (Fig. 2). Previously, we [21] reported that women demonstrated a mean increase in MMG AMP, but no change in EMG AMP, EMG MPF, or MMG MPF during a sustained isometric muscle action anchored to RPE = 5. Thus, EMG AMP, EMG MPF, and MMG MPF tracked RPE, but not force [21]. In addition, it was hypothesized [21] that the increase in MMG AMP was likely related to changes in muscle compliance (increase compliance due to decreased force) and not a reflection of motor unit recruitment. The results of the current study, however, were not consistent with our previous findings at RPE = 5 [21] and indicated that the decrease in the composite EMG AMP response at RPE = 2 tracked force across time for the men and women. Previously, EMG AMP has been reported to be influenced by motor unit recruitment, rate coding, and synchronization [1] and, despite conflicting opinion [8], EMG AMP has been used to quantify the neural drive to activated skeletal muscle [9, 27]. The current findings at RPE = 2, in conjunction with our previous results at RPE = 5 [21], indicated that there was an intensity-related difference in the EMG AMP and MMG AMP responses during fatiguing isometric muscle actions anchored to a perception of exertion. Furthermore, in contrast to our previous findings at RPE = 5 [21], all subjects in the current study were able to complete the maximal time-limit (5-min), which was likely due to less activated muscle mass and reduced muscle activation (perhaps reduced neural drive) necessary to maintain RPE = 2. The resulting response was that EMG AMP tracked force, not RPE.

The present study also indicated that the men and women exhibited different EMG MPF patterns of responses (quadratic vs. linear, respectively), yet the same overall direction of response for the composite values. It has previously been reported [15, 20] that reductions in muscle fiber action potential conduction velocity (EMG MPF) are associated with decreases in intracellular pH and increases in extracellular potassium, which result in a loss of membrane excitability (i.e. slowing conduction velocity). Thus, it is likely that the fatigue-induced decreases in EMG MPF can be attributed to the accumulation of metabolic byproducts (i.e. [K+] and [H+]), which affected both the men and women. The men, however, exhibited an exponential decrease, whereas the women demonstrated a linear decline. It is possible that the precipitous decrease in EMG MPF for the men, but not the women, may be explained by differences in relative proportions of muscle fiber types within the quadriceps [17, 32]. It has previously been suggested [17, 32] that women have a greater proportional area of type I fibers and smaller muscle fibers in the vastus lateralis, so it is possible the women exhibited a slower accumulation of metabolic byproducts than the men. The individual responses, however, indicated that the majority of the neuromuscular patterns of responses for men and women demonstrated non-significant changes across time. Therefore, despite the potential differences in fiber type distribution, both the men and women exhibited similar EMG MPF responses including the same composite directional response (decrease in EMG MPF), which tracked force, not RPE.

In the current study, the MMG-related neuromuscular patterns of responses differed between the men and women. The men exhibited an increase in MMG AMP and decrease in MMG MPF, which was consistent with previous fatigue-induced results of a sustained isometric forearm flexion muscle action anchored to 10% of MVIC [4]. That is, to sustain the muscle action at RPE = 2, the men likely exhibited an increase in motor unit recruitment (MMG AMP) and a decrease in global motor unit firing rate (MMG MPF), whereas the women did not. Thus, for the men, the decrease across time in EMG AMP was likely more influenced by a decrease in global motor unit firing rate (MMG MPF) than an increase in motor unit recruitment (MMG AMP). These overall patterns of neuromuscular responses and changes in motor unit activation strategies (increase in motor unit recruitment, decrease in firing rate) were consistent with the “Onion Skin” scheme [7] and the Muscle Wisdom theory [26]. The Onion Skin scheme proposes that fatigue is characterized by the recruitment of additional higher threshold motor units and an increase in the firing rates of the already activated motor units. The later recruited motor units, however, have lower firing rates than those initially recruited. The lower firing rates of the later recruited motor units are more influential and, therefore, there is a net decrease in the global motor unit firing rate (MMG MPF) as a result of fatigue [7]. According to the Muscle Wisdom theory [26] there is an economical activation of the fatiguing muscle by the central nervous system, which is characterized by decreases in force, increases in motor unit recruitment (MMG AMP), progressive prolongation of relaxation time, and decrease in the firing rate of the active motor units (MMG MPF) to optimize force production. An alternative hypothesis, however, is that even though the task was fatiguing (decrease in MVIC and EMG MPF), the decreases in EMG AMP and increase in MMG AMP were due to the decrease in force across time, which required less muscle activation (EMG AMP) and resulted in a decrease in muscle stiffness (fewer attached actin-myosin cross-bridges) [4]. This decrease in muscle stiffness would have allowed greater freedom for muscle fibers to oscillate, and, therefore, increased MMG AMP.

Unlike the men, the women did not exhibit changes in the neuromuscular responses across time except for EMG MPF, despite the sustained muscle action eliciting fatigue (decrease in MVIC and EMG MPF). Thus, the unique neuromuscular responses of the women may have been reflective of a sex-related difference in muscle fiber distribution [3] or an ability to sustained an RPE = 2 for 5-min without observable changes to motor unit activation strategies. For example, perhaps the greater proportional area of type I fibers [32] in women compared to men provided a fatigue-resistant mechanism for the women as evidenced by only reducing force by 34.7% to maintain an RPE = 2, whereas the men reduced force by 61.0%. Thus, it is possible that the 5-min time-limit was not long enough to induce observable fatigue-related neuromuscular changes in the women for the MMG AMP or MMG MPF. In addition, perhaps a sex-related difference in amount of activated muscle mass contributed to the discrepancy in MMG responses between the men and women. Recently, it has been hypothesized that the amount of activated muscle mass is directly related to the magnitude of performance fatigability [38]. The current results supported this hypothesis given the men exhibited greater overall strength and, thus, likely more muscle mass than the women, as well as a greater degree of performance fatigability (30.9% decrease) compared to the women (13.6%). Therefore, it is likely that although the task was fatiguing, it did not induce a great enough degree of performance fatigability in the women to induce changes in the MMG parameters.

Despite the men in the current study likely having greater muscle mass than the women, the current study reported no sex-related difference in FABF. The men and women exhibited similar increases in FABF immediately following the sustained muscle action at RPE = 2, which remained elevated (compared to pretest) 5-min posttest. Previously, following sustained low intensity muscle actions, it has been hypothesized [17, 28, 33, 40] that the most likely explanation of sex-related difference in performance fatigability is a difference in muscle blood flow. For example, a difference in muscle mass contributes to the ability of men to generate more intramuscular pressure than women at the same relative intensity [17, 18]. Specifically, at low intensities (10–40% of MVIC), men typically generate sufficient intramuscular pressure to attenuate blood flow to the active muscle, which contributes to fatigue earlier than women during sustained isometric muscle action anchored to a force [17, 34]. Furthermore, due to men demonstrating arterial occlusion at a lower relative intensity than women, men likely experience a faster rate of buildup of metabolic byproducts and/or a greater reduction in muscle perfusion compared to women at the same relative intensity [17, 18, 33]. The present results, however, failed to extend this hypothesis to muscle actions anchored to a low perceptual intensity. Perhaps, when force is free to vary during a sustained muscle action at RPE = 2, men and women self-select an intensity that accommodates sufficient blood flow and perfusion to active skeletal muscle. Therefore, the current FABF findings do not explain the greater performance fatigability exhibited by the men compared to the women.

A limitation of the current study included utilizing a maximal time-limit of 5-min. Perhaps, a longer sustained muscle action anchored to RPE = 2 would elicit different sex-specific responses or eliminate the sex-related difference in performance fatigability and MMG responses. In addition, the current study only utilized 10 men and 10 women to perform a sustained muscle action anchored to RPE = 2. It is possible that an increased sample size and an experimental trial anchored to a force corresponding to RPE = 2 would provide additional findings.

In summary, the men demonstrated a greater degree of performance fatigability than the women following a sustained muscle action anchored to RPE = 2, which was independent of sex-related differences in FABF. In addition, the current study identified two possible sex-related differences, which were related to the MMG neuromuscular responses and, potentially, amount of muscle mass. Therefore, we hypothesize that due to the men exhibiting greater absolute muscular strength than the women, the men experienced a greater magnitude of performance fatigability, which promoted a change in motor unit activation strategies (i.e. Onion Skin Scheme or Muscle Wisdom) as indicated by the MMG parameters. Also, it was demonstrated that the RPE clamp protocol elicits similar magnitudes performance fatigability as traditional anchoring by constant force schemes. Thus, future fatigue-related studies should consider utilizing the RPE clamp protocol to investigate potential sex-related differences in performance fatigability following a fatiguing muscle actions anchored to a constant perception of exertion of control for changes in perceived fatigability. Furthermore, these future studies should use an extended or indefinite maximal time-limit as well as quantify the amount of relevant muscle mass.

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Acknowledgements

We would like to thank all the participants for their compliance and willingness to participate. In addition, there are no conflicts of interest to report.

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Correspondence to Joshua L. Keller.

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Keller, J.L., Housh, T.J., Hill, E.C. et al. Sex-Related Differences in Performance Fatigability Independent of Blood Flow Following a Sustained Muscle Action at a Low Perceptual Intensity. J. of SCI. IN SPORT AND EXERCISE (2020). https://doi.org/10.1007/s42978-020-00052-7

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Keywords

  • Perception
  • Resistance training
  • Electromyography
  • Fatigue
  • Mechanomyography
  • RPE clamp