Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions
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《应用生理学杂志》
Department of Kinesiology and Applied Physiology, University of Colorado, Boulder, Colorado 80309-0354
ABSTRACT
Women are capable of longer endurance times compared with men for contractions performed at low to moderate intensities. The purpose of the study was 1) to determine the relation between the absolute target force and endurance time for a submaximal isometric contraction and 2) to compare the pressor response and muscle activation patterns of men [26.3 ± 1.1 (SE) yr] and women (27.5 ± 2.3 yr) during a fatiguing contraction performed with the elbow flexor muscles. Maximal voluntary contraction (MVC) force was greater for men (393 ± 23 vs. 177 ± 7 N), which meant that the average target force (20% of MVC) was greater for men (79.7 ± 6.5 vs. 36.7 ± 2.0 N). The endurance time for the fatiguing contractions was 118% longer for women (1,806 ± 239 vs. 829 ± 94 s). The average of the rectified electromyogram (%MVC) for the elbow flexor muscles at exhaustion was similar for men (31 ± 2%) and women (30 ± 2%). In contrast, the heart rate and mean arterial pressure (MAP) were less at exhaustion for women (94 ± 6 vs. 111 ± 7 beats/min and 121 ± 5 vs. 150 ± 6 mmHg, respectively). The target force and change in MAP during the fatiguing contraction were exponentially related to endurance time (r2 = 0.68 and r2 = 0.64, respectively), whereas the change in MAP was linearly related to target force (r2 = 0.51). The difference in fatigability of men and women when performing a submaximal contraction was related to the absolute contraction intensity and was limited by mechanisms that were distal to the activation of muscle.
keywords:gender; pressor response; electromyography; elbow flexor muscles; muscle activation
INTRODUCTION
WOMEN ARE CAPABLE OF LONGER endurance times compared with men when performing isometric contractions at low to moderate intensities. This sex difference has been observed in several muscle groups, including adductor pollicis (5, 13), elbow flexors (19, 37), extrinsic finger flexors (32, 48), and knee extensors (27). The mechanism for this difference in endurance time is unknown. A common explanation has been that men, who are usually stronger, sustain greater absolute forces when the target force is based on an individual's strength (3, 28; cf. 13). Indirect evidence suggests that greater absolute forces are associated with increased intramuscular pressures, occlusion of blood flow, accumulation of metabolites, heightened metaboreflex responses, and impairment of oxygen delivery to the muscle (1, 25, 36, 41). Furthermore, activation of the metaboreflex, as measured by the rate of increase in the mean arterial pressure (MAP) and heart rate (pressor response) (29, 35), is inversely related to endurance time (9, 14, 38-40). Accordingly, women had longer endurance times when performing low-intensity contractions with the knee extensor muscles, but this difference disappeared during high-intensity contractions when both men and women would experience circulatory occlusion (27).
The endurance times of submaximal contractions that involve multiple muscles, however, could also be influenced by variation in the pattern of muscle activation (10, 24, 44, 45), perhaps including differences between men and women (42, 43). These observations raised the question of the relative contributions of the target force, circulatory limitations, and pattern of muscle activation to the observed sex difference in endurance time of the elbow flexor muscles. The purpose of this study was 1) to determine the relation between the absolute target force and endurance time for a submaximal isometric contraction and 2) to compare the pressor response and muscle activation patterns of men and women during a fatiguing contraction performed with the elbow flexor muscles. We found that the endurance time of women was greater than that for the men and that endurance time was inversely related to the absolute force sustained during the contraction. This difference in endurance time was accompanied by similar increases in electromyogram (EMG) during the fatiguing contraction for the men and women but by a reduced pressor response for the women. Preliminary accounts of these results have been presented in abstract form (11, 17).
METHODS
Subjects
Fourteen healthy adults (7 men, 26.3 ± 1.1 yr; and 7 women, 27.5 ± 2.3 yr) volunteered to participate in the study. All the subjects were right handed with no known neurological disorders. Before participation in the study, all subjects gave informed consent to a protocol approved by the Human Subjects Committee at the University of Colorado.
Mechanical Recording
Subjects were seated upright in an adjustable chair with the left (nondominant) arm abducted slightly, the elbow resting on a padded support, and the joint flexed to 90°. The hand and forearm were placed in a modified wrist-hand-thumb orthosis (Orthomerica, Newport Beach, CA), which held the forearm in a position midway between pronation and supination. The force exerted by the elbow flexor muscles in vertical and side-to-side (medial-lateral) directions was measured with a force transducer (Force-Moment Sensor, JR-3, Woodland, CA) that was mounted on a custom-designed, adjustable support. The vertical force was used to provide the target force for the fatiguing contraction, whereas the medial-lateral force provided a measure of the out-of-plane action of the involved muscles. The forces detected were recorded on digital tape (DAT Sony PC 116, Sony data Recording, Montvale, NJ). The force exerted in the vertical direction was displayed on a 14-in. computer monitor that was located 1 m in front of the subject.
Electrical Recordings
EMG signals were recorded with bipolar surface electrodes (Ag-AgCl, 8-mm diameter; 20-mm distance between electrodes) that were placed over the long head of biceps brachii, the short head of biceps brachii and brachioradialis, and the medial head of triceps brachii. Reference electrodes were placed on a bony prominence at the elbow or shoulder. The EMG of the brachialis muscle was measured with an intramuscular bipolar electrode inserted into the muscle ~3 cm proximal to the antecubital fold. The electrode comprised two stainless steel wires (100-μm diameter) that were insulated with Formvar (California Fine Wire, Grover Beach, CA). A surface electrode (8-mm diameter) placed on a bony prominence served as the reference electrode. The EMG signal was amplified (×500-2,000), band-pass filtered (20-800 Hz for the surface EMG and 20-1,000 Hz for the intramuscular EMG), recorded on digital tape, and displayed on an oscilloscope.
Cardiovascular Measurements
Heart rate and blood pressure were monitored throughout the fatiguing contraction with an automated beat-by-beat, blood pressure monitor (Finapres 2300, Ohmeda, Louisville, CO). The blood pressure cuff was placed around the middle finger of the right hand, and the arm was placed in a sling so that it was relaxed with the hand at heart level. The blood pressure signal was recorded on digital tape.
Experimental Protocol
Subjects were required to perform the protocol on three occasions, with 2 wk separating each session. Before the first experimental session, each subject visited the laboratory for an introductory session to become familiar with the equipment and the procedures, and each performed several trials of the maximal voluntary contraction (MVC) task. The experiments for each subject were performed at the same time of the morning on each occasion. The protocol comprised 1) MVCs with the elbow flexor and elbow extensor muscles, 2) an isometric contraction with the elbow flexor muscles that was sustained at 20% MVC force until exhaustion, and 3) another MVC with the elbow flexor muscles immediately after the fatiguing contraction.
MVC force. Subjects performed three MVC trials with the elbow flexor muscles and three MVC trials with the elbow extensor muscles. The MVC task consisted of a gradual increase in force from zero to maximum over 3 s, with the maximal force held for 2-3 s. Subjects were able to observe the exerted force on a monitor and were verbally encouraged to achieve maximal force. Subjects rested for 60-90 s between trials. If the peak forces from two of the three trials were not within 5% of each other, additional trials were performed until this was accomplished. The greatest force achieved by the subject was taken as the MVC force and used as the reference to calculate the target force for the fatiguing contraction. Subsequently, the MVC force for the elbow extensor muscles was determined by using the same procedures. Immediately on completion of the fatiguing contraction, a MVC was performed with the elbow flexor muscles.
Fatiguing contraction. The fatiguing contraction was performed at a target force of 20% MVC. The subject was required to match the target vertical force as displayed on the monitor and was verbally encouraged to sustain the force for as long as possible. The contraction was terminated when the subject deviated from the target force by 4% MVC force for >2 s, despite strong verbal encouragement. When this occurred, the subject was deemed to have reached exhaustion, and the duration of the contraction was recorded as the endurance time. Subjects were not informed of the endurance times until completion of the third session.
As an index of perceived effort, the rating of perceived exertion (RPE), was recorded using the modified Borg 10-point scale at regular time intervals (1-5 min between recordings) during the fatiguing contraction (2). Once the subject had attained a score of 8 on the Borg scale, the RPE was recorded every minute.
Data Analysis
The data were recorded on digital tape and then were digitized (analog-to-digital converter, 12-bit resolution) and analyzed off-line using the Spike2 data-analysis system (Cambridge Electronic Design, Cambridge, UK). The forces (vertical and medial lateral) and blood pressure were digitized at 200 samples/s, whereas the EMG signals were digitized at 2,000 samples/s.
The MVC force was quantified as the average value over a 0.5-s interval that included the peak force. Similarly, the maximal EMG for each muscle was determined as the average value over a 0.5-s interval that included the peak rectified EMG.
The amplitude of the force fluctuations was quantified as the coefficient of variation (CV = SD/mean × 100) for the first, middle, and last 60 s of the fatiguing contraction. The medial-lateral forces recorded during the fatiguing contraction were averaged over the duration of the fatiguing contraction.
The EMG during the fatiguing contraction was quantified in two ways: 1) for statistical analysis, as averages of the rectified EMG (AEMG) for the first, middle, and last 60 s of the fatiguing contraction; and 2) for graphic presentation, as averages of the rectified EMG for every 1% of the endurance time (100 data points). The EMG for each muscle was normalized to the maximum EMG obtained during the MVC. The normalized EMGs for the short and long heads of biceps brachii were averaged.
Heart rate and MAP during the fatiguing contraction were analyzed by comparing ~15-s averages at 10% intervals throughout the endurance time. For each interval, the blood pressure signal was analyzed for the mean peaks [systolic blood pressure (SBP)], mean troughs [diastolic blood pressure (DBP)], and the number of pulses per second (multiplied by 60 to determine heart rate). MAP was calculated for each epoch with the following equation: MAP = DBP + 1/3(SBP DBP).
As a supplement to the study on the elbow flexor muscles, we analyzed data on a hand muscle (first dorsal interosseus) that had been collected previously in our laboratory (12). Thirty-two men (n = 18) and women (n = 14) (age 20-40 yr) sustained an isometric abduction force with the index finger at either 20% (n = 6 men, 5 women), 35% (n = 7 men, 4 women), or 65% (n = 5 men, 5 women) of the MVC force for as long as possible. Each subject performed the fatiguing contraction at the same intensity on four occasions, with each session separated by 4-7 days.
Statistical Analysis
Data are reported as means ± SE unless stated otherwise. A two-factor (sex × session) repeated-measures, ANOVA (StatView, SAS Institute) was used to compare the dependent variables for endurance time, medial-lateral forces, and changes in heart rate and MAP for the fatiguing contraction. A three-factor, repeated-measures ANOVA [sex × session × time (rest, start, 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90%, 100%)] was used to compare the dependent variables for heart rate and MAP. Endurance time, MAP, and heart rate were further analyzed using analysis of covariance and varying for target force (sex × target force). A three-factor repeated-measures ANOVA [sex × session × time (before and after fatigue)] was used to compare MVC force. A three-factor [sex × session × time (first 60 s, middle 60 s, and last 60 s)] repeated-measures ANOVA was used to compare the dependent variables of AEMG and force fluctuations (CV) during the fatiguing contraction. To compare the AEMG of the elbow flexor muscles, a four-factor [muscle (biceps brachii, brachioradialis, brachialis) × sex × session × time (first 60 s, middle 60 s, and last 60 s)] repeated-measures ANOVA was utilized. A three-factor, repeated-measures ANOVA [sex × session × time (start, middle, end)] was used to compare the RPE and force fluctuations (CV). To compare the MVC force and endurance times of the men and women for the hand muscle, a two-factor (sex × session), repeated-measures ANOVA was used for the contractions performed at 20, 35, and 65% of MVC force. Post hoc analyses (Tukey-Kramer) were used to test for differences when appropriate. Regression analysis and curve fitting were performed using SigmaPlot 5.0 Scientific Graphing software (SPSS, Chicago, IL). A significance level of P < 0.05 was used to identify statistical significance.
RESULTS
The average endurance time of the women across the three sessions was longer than that for the men (1,943 ± 235 vs. 959 ± 111 s; P < 0.05). The endurance time for both the men and women increased across sessions (P < 0.05), such that session 3 was longer than sessions 1 and 2 and there was no difference between sessions 1 and 2 (P > 0.05). The adaptations in endurance time across sessions raised separate issues independent of the sex differences and so are not reported here (SK Hunter and RM Enoka, unpublished observations). Because the endurance times for men and women did not differ between sessions 1 and 2 (P > 0.05), all subsequent results are presented as the average of the first two sessions. The endurance time of the women (1,806 ± 239 s) was 118% longer than that for the men (829 ± 94 s, P < 0.05) (Table 1). However, there was no sex difference in endurance time (P = 0.35) when the difference in target force (men: 80 ± 7 N; women: 37 ± 2 N) was accounted for with a covariate analysis.
At the start of the protocol, the MVC force for the elbow flexor muscles of the women (177 ± 7 N) was 45% of the value for the men (393 ± 27 N; P < 0.05) (Table 1). The MVC force immediately after the fatiguing contraction was reduced by similar amounts for both the men (39.3 ± 6.5%) and the women (34.3 ± 6.5%; P > 0.05).
Force Fluctuations
When the effort associated with a sustained contraction becomes maximal, the exerted force exhibits low-frequency oscillations. Accordingly, we used the amplitude of the normalized force fluctuations (CV) as an index of effort during the fatiguing contraction. The CV for force increased progressively during the fatiguing contractions for both men and women (P < 0.05; Fig. 1). The recorded force fluctuations are apparent in Fig. 2 (trace at bottom). The increase in CV was similar for men and women (P > 0.05), which suggested that the relative effort was comparable. At the start of the contraction (first 60 s), the CV averaged 2.5 ± 0.2% and at the end of the contraction it was 10.0 ± 1.0%.
RPE
RPE during the fatiguing contraction began and ended at similar scores for the men and women, with no difference between sessions (P > 0.05). The RPE for the men and women was similar at 30 s into the contraction (1.5 ± 0.4 vs. 1.8 ± 0.2, respectively; P > 0.05) and at the midpoint of endurance time (7.4 ± 0.4 vs. 7.9 ± 0.6, respectively; P > 0.05). At exhaustion, all subjects had achieved a rating of 10. These results provided further evidence that the perceived effort during the fatiguing contraction was similar for men and women.
Medial-Lateral Forces
Because the elbow flexor muscles can exert a force in the transverse plane, the medial-lateral force was measured to quantify the magnitude of this action during the fatiguing contraction. The medial-lateral force was normalized to the target force. The most significant feature of the medial-lateral force was its variability, both between subjects and over the duration of the fatiguing contraction. On most occasions, the force was directed medially, which was denoted as the positive direction. The average medial-lateral force was not statistically different between men (10.0 ± 6.1%) and women (18.5 ± 8.3%; P > 0.05). The difference in endurance time between men and women, therefore, was not related to a consistent difference in the out-of-plane force exerted by the active muscles.
Adjustments in AEMG
For both men and women, the amplitude of the normalized AEMG for the elbow flexor muscles increased progressively during the fatiguing contractions (P < 0.05; Fig. 2). The increase in AEMG was similar for men and women (P > 0.05). The mean AEMG for all the elbow flexor muscles at the beginning, midpoint, and end of the fatiguing contraction was 14 ± 1, 20 ± 1, and 30 ± 2% for the men and 12 ± 1, 22 ± 1, and 31 ± 2% for the women. Because endurance time was longer for the women, this meant that the rate of increase in AEMG was greater for the men.
The increase in AEMG of the brachialis muscle, for both men and women, was different from that for biceps brachii and brachioradialis (P < 0.05; Fig. 3). At the beginning of the fatiguing contraction, the AEMG for brachialis was greater (18 ± 1%) than the average value for biceps brachii and brachioradialis (11 ± 1%). At exhaustion, however, the AEMG for brachialis (31 ± 2%) was similar to that for biceps brachii and brachioradialis (31 ± 2%). Thus the increase in AEMG for brachialis (73%) was less than that for biceps brachii and brachioradialis (192%).
AEMG for the antagonist muscle triceps brachii increased by a small but significant amount during the fatiguing contraction (Fig. 3), and this effect was similar across sessions. The triceps brachii AEMG was greater for women compared with men at the beginning (2 ± 0.2 vs. 1 ± 0.2%; P < 0.05) and the end of the fatiguing contraction (5 ± 0.4 vs. 3 ± 0.4%; P < 0.05).
MAP and Heart Rate
MAP increased during the fatiguing contraction (P < 0.05) for both men and women. The average increase in MAP during the fatiguing contraction was greater for men compared with women (P < 0.05; Fig. 4A). The MAP was not different between men and women either at rest (82.9 ± 1.6 vs. 82.1 ± 2.0 mmHg; P > 0.05) or within the first 15 s of the fatiguing contraction (108.5 ± 2.3 vs. 100.8 ± 3.0 mmHg; P = 0.06). At exhaustion, however, the increase in MAP was less for women (121.2 ± 4.8 mmHg) compared with men (149.8 ± 6.1 mmHg; P < 0.05). The increase of MAP from the beginning to the end of the fatiguing contraction was 38.3 ± 5.2% for men and 20.4 ± 3.0% for women. However, there was no main effect for sex when the MAP was covaried with target force (P > 0.05).
Heart rate increased during the fatiguing contraction (P < 0.05). As with the MAP, the increase in heart rate was greater for men compared with women (P < 0.05; Fig. 4B). Heart rate was similar for the men and women at rest (60 ± 4 vs. 66 ± 3 beats/min; P > 0.05) and at the start of the fatiguing contraction (73 ± 5 vs. 76 ± 4 beats/min; P > 0.05). At exhaustion, heart rate for women (94 ± 6 beats/min) was less than that for men (111 ± 7 beats/min; P < 0.05). The increase of heart rate from the beginning to the end of the fatiguing contraction was 53.2 ± 5.9% for men and 24.9 ± 5.8% for women. However, there was no main effect for sex when heart rate was covaried with target force (P > 0.05).
Endurance Time, Target Force, and MAP
The endurance times for sessions were inversely related to target force by an exponential decay, which meant that stronger individuals had briefer endurance times (r = 0.82; Fig. 5A). Similarly, the absolute change in MAP was inversely related to endurance time by an exponential decay (r = 0.80; Fig. 5B). The increase in MAP was positively associated with target force (r = 0.72), but, because of the variability in this association, the increase in MAP for some men was similar to that for women, despite these men having greater target forces (Fig. 5C).
Endurance Time and MVC Force for the Hand Muscle
We examined the relation between MVC force and endurance time for the first dorsal interosseus muscle on the basis of data that had been collected previously in our laboratory (12). There were no sex differences in endurance time for the first dorsal interosseus at any of the three intensities of contraction (20, 35, and 65% MVC) (P > 0.05), even though the men had greater MVC forces (39.5 ± 1.2 vs. 26.3 ± 1.3 N; P < 0.05) (Fig. 6A). These results were consistent across four repeat performances at each of the contraction intensities (P < 0.05). There was, however, a strong exponential relation between target force and endurance time for men and women, such that greater target forces were associated with briefer endurance times (r2 = 0.75) (Fig. 6B).
DISCUSSION
We found that women had longer endurance times than men when sustaining an isometric contraction at 20% MVC force with the elbow flexor muscles. Because the men were stronger than the women, there was no sex difference in endurance time when the data were covaried with the target force that was sustained during the contraction. Furthermore, there were no sex differences in the increase of AEMG at exhaustion, the reduction of MVC force after the contraction, the increase in force fluctuations, the average medial-lateral forces, or the change in RPE during the fatiguing contraction. However, the increase of the pressor response during the fatiguing contraction and at exhaustion was greater in the stronger individuals.
Comparable Fatigue for Men and Women
There was no evidence of a sex difference in the performance of the fatiguing contraction by the subjects. First, men and women displayed similar relative reductions in MVC force (37%) at exhaustion. Second, the increased amplitudes of force fluctuations that often characterize a fatiguing contraction (4, 6, 16, 43) were similar at exhaustion for the men and women. Third, the average medial-lateral forces were often large but were highly variable for both men and women and thus were not associated with differences in endurance time. Finally, the RPE scores were similar for the men and women at the midpoint of the fatiguing contractions and at exhaustion.
Endurance Time and Target Force Were Inversely Related
Given that the relative performance was comparable for men and women, we examined the target force, the pressor response, and muscle activation as explanations for the difference in endurance time. We observed that stronger individuals had a briefer endurance time and that this relation was exponential for both the elbow flexors and the hand muscle (Figs. 5 and 6). Furthermore, there was no sex difference in endurance time when the analysis covaried for the force that was sustained during the fatiguing contraction. Consequently, stronger individuals had shorter endurance times for actions by both a single muscle (first dorsal interosseus) and many muscles (elbow flexors), and these relations appeared to be exponential and independent of the sex of the individual. In contrast to our findings, others have reported no relation between handgrip strength and endurance times for isometric contractions performed at 30, 50, and 75% MVC, even though women had longer endurance times (48). Furthermore, women had longer endurance times for adductor pollicis when performing an intermittent isometric contraction at 50% MVC, even when men and women were matched for strength (13). Although we have found a consistent association between endurance time and absolute force, this is not a universal finding.
Women Had a Reduced Pressor Response
We examined the association between the pressor response and endurance time. The pressor response is a reflex-mediated adjustment in MAP that attempts to rectify the mismatch between perfusion and muscle metabolism during an isometric contraction (18, 34). We found that the MAP and heart rate were less in women compared with men during the contraction and at exhaustion. There are several possible explanations for the reduced pressor response of the women: 1) less muscle mass and a lower target force, resulting in greater muscle perfusion; 2) attenuated sympathetic neural outflow, resulting in greater muscle perfusion; 3) different substrate utilization and lower metabolite production; or 4) a similar metabolite production but a less responsive pressor response.
Our findings suggest that the pressor response was less in the women because of a lower absolute target force. We observed that those individuals who had the greatest increase in MAP had a shorter endurance time but sustained a greater absolute force. Furthermore, there was no sex difference in the pressor response when we statistically covaried for target force. These results, which are consistent with other observations, suggest that muscle mass is a primary determinant of the pressor response. For example, the endurance times of men are longer for low-force contractions compared with high-force contractions, but at exhaustion the pressor response was similar for the same muscle (9, 14, 39). In contrast, the pressor response is less at exhaustion for smaller muscle groups compared with larger muscle groups (30, 38, cf. 49). Consequently, the lesser increase in MAP and heart rate at exhaustion for the women may have been related to a smaller muscle mass. Because the force capacity of muscle is directly related to muscle size, stronger subjects may have experienced a greater mechanical compression of the arteries perfusing the active muscle that limited blood flow and led to an accelerated accumulation of metabolites (1, 36, 41). The heightened concentration of metabolites increases the activation of group III and IV afferents (20, 21) and contributes to the increase in MAP. Consequently, the endurance time of stronger individuals was likely limited by a greater restriction of muscle perfusion due to a greater muscle mass and target force.
Alternatively, the reduced increase in MAP in the women may have been the result of an attenuated sympathetic neural outflow (7, 31), possibly due to estrogen (8, 22, 23, 33), that reduced vasoconstriction, maintained muscle perfusion, and prolonged endurance time. Furthermore, sex differences in substrate utilization (46, 47) might reduce the rate of metabolite production and reflex-mediated change in MAP in women compared with men, which would also contribute to the prolongation of endurance time. However, when women performed an intermittent contraction at 30% MVC force with the finger flexor muscles under ischemic conditions, endurance time was similar to men even though the increase in MAP and metabolite production was less for women (7). This finding indicates that, when the circulatory adjustments were normalized in men and women, there was no sex difference in endurance time despite a lesser pressor response in women. Furthermore, it is also conceivable that the women had a similarly perfused muscle and production of glycolytic metabolites but a less responsive pressor response, although there is no evidence to support this possibility.
Sex Differences and Muscle Activation
The other factor we considered that might contribute to the sex difference in endurance time was the activation pattern of the muscle. Although the amplitude of AEMG at exhaustion did not reach the values observed during the MVC, the AEMG deficit was similar for the men and women (30% of maximum) and comparable to that reported previously (12, 48). However, the briefer endurance time for men meant that the rate of increase in AEMG was less for women. Because the progressive increase in the interference EMG during such conditions is mainly due to the recruitment of motor units (12, 15, 26), the greater rate of increase in AEMG for the men indicated an enhanced rate of motor unit recruitment. Presumably, the activated motor units fatigued more rapidly and additional units were required to achieve the target force. Nonetheless, the comparable values of AEMG at exhaustion for the men and women suggest that they eventually activated similar proportions of the motor neuron pools.
Aside from the average levels of AEMG, endurance time can also be influenced by the distribution of activation within a muscle and across a group of synergist muscles (10, 26, 42-45). There was evidence of intermittent bursts in the EMG, as our laboratory had observed in women after limb immobilization (42); however, this was common to both men and women and thus was not associated with the sex difference in endurance time. In contrast, there were differences in activation between the elbow flexor muscles. For example, the increase in AEMG during the fatiguing contraction was different for the brachialis compared with biceps brachii and brachioradialis. This pattern of activation, however, was similar for both men and women and so was not related to the longer endurance times of women. These findings suggest that coordination among the synergists did not contribute significantly to the enhanced endurance time of the women.
In summary, we found that the longer endurance time of women for a submaximal isometric contraction when performed with the elbow flexor muscles was associated with a lower absolute target force. Similarly, analysis of endurance times from a previous study (12) indicated that greater target forces for a hand muscle were associated with briefer endurance times and not the sex of the individual. The longer endurance time of the women for the elbow flexor muscles was associated with a reduced pressor response but was not related to the activation levels of the muscle at exhaustion. Consequently, the difference in endurance time between men and women for a submaximal contraction was related to the absolute contraction intensity and was limited by mechanisms that were distal to the activation of the muscle and involved the pressor response.
ACKNOWLEDGEMENTS
We thank Darren Flagg for assistance in conducting the experiments, Douglas Seals and Brian Tracy for comments on the manuscript, and Ohmeda (Louisville, CO) for loaning us the Finapres 2300.
FOOTNOTES
This research was supported by National Institute of Neurological Disorders and Stroke Grant NS-20544 (to R. M. Enoka).
Address for reprint requests and other correspondence: R. M. Enoka, Dept. of Kinesiology and Applied Physiology, Univ. of Colorado, Boulder, CO 80309-0354 (E-mail: Roger.Enoka@Colorado.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 29 May 2001; accepted in final form 15 August 2001.
REFERENCES
1.Barnes, WS. The relationship between maximum isometric strength and intramuscular circulatory occlusion. Ergonomics 23: 352-357, 1980.
2.Borg, GA. Perceived exertion. Exerc Sport Sci Rev 2: 131-153, 1974.
3.Carlson, BR. Level of maximum isometric strength and relative load isometric endurance. Ergonomics 12: 429-435, 1969.
4.Cresswell, AG, and L?scher WN. Significance of peripheral afferent input to the alpha-motoneurone pool for enhancement of tremor during an isometric fatiguing contraction. Eur J Appl Physiol 82: 129-136, 2000.
5.Ditor, DS, and Hicks AL. The effect of age and gender on the relative fatigability of the human adductor pollicis muscle. Can J Physiol Pharmacol 78: 781-790, 2000.
6.Ebenbichler, GR, Kollmitzer J, Erim Z, Loscher WN, Kerschan K, Posch M, Nowotny T, Kranzl A, Wober C, and Bochdansky T. Load-dependence of fatigue related changes in tremor around 10 Hz. Clin Neurophysiol 111: 106-111, 2000.
7.Ettinger, SM, Silber DH, Collins BG, Gray KS, Sutliff G, Whisler SK, McClain JM, Smith MB, Yang QX, and Sinoway LI. Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol 80: 245-251, 1996.
8.Ettinger, SM, Silber DH, Gray KS, Smith MB, Yang QX, Kunselman AR, and Sinoway LI. Effects of the ovarian cycle on sympathetic neural outflow during static exercise. J Appl Physiol 85: 2075-2081, 1998.
9.Fallentin, N, and J?rgensen K. Blood pressure response to low level static contractions. Eur J Appl Physiol 64: 455-459, 1992.
10.Fallentin, N, J?rgensen K, and Simonsen EB. Motor unit recruitment during prolonged isometric contractions. Eur J Appl Physiol 67: 335-341, 1993.
11.Flagg, D, Fleshner M, Hunter SK, and Enoka RM. Circadian rhythmicity of salivary cortisol levels in men and women is reliable (Abstract). Med Sci Sports Exerc 32: S271, 2000.
12.Fuglevand, AJ, Zackowski KM, Huey KA, and Enoka RM. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol (Lond) 460: 549-572, 1993.
13.Fulco, C, Rock P, Muza S, Lammi E, Cymerman A, Butterfield G, Moore L, Braun B, and Lewis S. Slower fatigue and faster recovery of the adductor pollicis in women matched for strength with men. Acta Physiol Scand 167: 233-239, 1999.
14.Gaffney, FA, Sjogaard G, and Saltin B. Cardiovascular and metabolic responses to static contraction in man. Acta Physiol Scand 138: 249-258, 1990.
15.Garland, SJ, Enoka RM, Serrano LP, and Robinson GA. Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol 76: 2411-2419, 1994.
16.Gottlieb, S, and Lippold OC. The 4-6 Hz tremor during sustained contraction in normal human subjects. J Physiol (Lond) 336: 499-509, 1983.
17.Hunter, SK, Flagg D, Fleshner M, and Enoka RM. The endurance time of a submaximal fatiguing contraction is reliable for men and women (Abstract). Med Sci Sports Exerc 32: S184, 2000.
18.Kagaya, A, and Homma S. Brachial arterial blood flow during static handgrip exercise of short duration at varying intensities studied by a Doppler ultrasound method. Acta Physiol Scand 160: 257-265, 1997.
19.Kahn, J, Kapitaniak B, Hueart F, and Monod H. Physiological modifications of local haemodynamic conditions during bilateral isometric contractions. Eur J Appl Physiol 54: 624-631, 1986.
20.Kaufman, MP, Longhurst JC, Rybicki KJ, Wallach JH, and Mitchell JH. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55: 105-112, 1983.
21.Kaufman, MP, Rotto DM, and Rybicki KJ. Pressor reflex response to static muscular contraction: its afferent arm and possible neurotransmitters. Am J Cardiol 62: 58E-62E, 1988.
22.Kendrick, ZV, and Ellis GS. Effect of estradiol on tissue glycogen metabolism and lipid availability in exercised male rats. J Appl Physiol 71: 1694-1699, 1991.
23.Kendrick, ZV, Steffen CA, Rumsey WL, and Goldberg DI. Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J Appl Physiol 63: 492-496, 1987.
24.Kulig, K, Powers CM, Shellock FG, and Terk M. The effects of eccentric velocity on activation of elbow flexors: evaluation by magnetic resonance imaging. Med Sci Sports Exerc 33: 196-200, 2001.
25.Lind, AR, and McNicol GW. Local and central circulatory responses to sustained contractions and the effect of free or restricted arterial inflow on post-exercise hyperaemia. J Physiol (Lond) 192: 575-593, 1967.
26.Maton, B, and Gamet D. The fatigability of two agonist muscles in human isometric voluntary submaximal contraction: an EMG study. Eur J Appl Physiol 58: 369-374, 1989.
27.Maughan, R, Harmon M, Leiper J, Sale D, and Delman A. Endurance capacity of untrained males and females in isometric and dynamic muscular contractions. Eur J Appl Physiol 55: 395-400, 1986.
28.Miller, A, MacDougall J, Tarnopolsky M, and Sale D. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol 66: 254-262, 1993.
29.Mitchell, JH, Kaufman MP, and Iwamoto GA. The exercise pressor reflex: its cardiovascular effects, afferent mechanisms, and central pathways. Annu Rev Physiol 45: 229-242, 1983.
30.Nagle, FJ, Seals DR, and Hanson P. Time to fatigue during isometric exercise using different muscle masses. Int J Sports Med 9: 313-315, 1988.
31.Ng, AV, Callister R, Johnson DG, and Seals DR. Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension 21: 498-503, 1993.
32.Petrofsky, J, Burse R, and Lind A. Comparison of physiological responses of women and men to isometric exercise. J Appl Physiol 38: 863-868, 1975.
33.Rooney, TP, Kendrick ZV, Carlson J, Ellis GS, Matakevich B, Lorusso SM, and McCall JA. Effect of estradiol on the temporal pattern of exercise-induced tissue glycogen depletion in male rats. J Appl Physiol 75: 1502-1506, 1993.
34.Rowell, L. Human Cardiovascular Control. New York: Oxford Univ. Press, 1993.
35.Rowell, LB, and O'Leary DS. Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physiol 69: 407-418, 1990.
36.Sadamoto, T, Bonde-Petersen F, and Suzuki Y. Skeletal muscle tension, flow, pressure, and EMG during sustained isometric contractions in humans. Eur J Appl Physiol 51: 395-408, 1983.
37.Sato, H, and Ohashi J. Sex differences in static muscular endurance. J Hum Ergol (Tokyo) 18: 53-60, 1989.
38.Seals, DR. Influence of active muscle size on sympathetic nerve discharge during isometric contractions in humans. J Appl Physiol 75: 1426-1431, 1993.
39.Seals, DR. Influence of force on muscle and skin sympathetic nerve activity during sustained isometric contractions in humans. J Physiol (Lond) 462: 147-159, 1993.
40.Seals, DR, and Enoka RM. Sympathetic activation is associated with increases in EMG during fatiguing exercise. J Appl Physiol 66: 88-95, 1989.
41.Sejersted, O, Hargens A, Kardel K, Blom P, Jensen O, and Hermansen L. Intramuscular fluid pressure during isometric contraction of human skeletal muscle. J Appl Physiol 56: 287-295, 1984.
42.Semmler, JG, Kutzschner DV, and Enoka RM. Gender differences in the fatigability of human skeletal muscle. J Neurophysiol 82: 3590-3593, 1999.
43.Semmler, JG, Kutzscher DV, and Enoka RM. Limb immobilization alters muscle activation patterns during a fatiguing isometric contraction. Muscle Nerve 23: 1381-1392, 2000.
44.Sjogaard, G, Kiens B, Jorgensen K, and Saltin B. Intramuscular pressure, EMG and blood flow during low-level prolonged static contraction in man. Acta Physiol Scand 128: 475-484, 1986.
45.Tamaki, H, Kitada K, Akamine T, Murata F, Sakou T, and Kurata H. Alternate activity in the synergistic muscles during prolonged low-level contractions. J Appl Physiol 84: 1943-1951, 1998.
46.Tarnopolsky, LJ, MacDougall JD, Atkinson SA, Tarnopolsky MA, and Sutton JR. Gender differences in substrate for endurance exercise. J Appl Physiol 68: 302-308, 1990.
47.Tarnopolsky, MA. Gender differences in substrate metabolism during endurance exercise. Can J Appl Physiol 25: 312-327, 2000.
48.West, W, Hicks A, Clements L, and Dowling J. The relationship between voluntary electromyogram, endurance time and intensity of effort in isometric handgrip exercise. Eur J Appl Physiol 71: 301-305, 1995.
49.Williams, CA. Effect of muscle mass on the pressor response in man during isometric contractions. J Physiol (Lond) 435: 573-584, 1991.(Sandra K. Hunter and Roge)
ABSTRACT
Women are capable of longer endurance times compared with men for contractions performed at low to moderate intensities. The purpose of the study was 1) to determine the relation between the absolute target force and endurance time for a submaximal isometric contraction and 2) to compare the pressor response and muscle activation patterns of men [26.3 ± 1.1 (SE) yr] and women (27.5 ± 2.3 yr) during a fatiguing contraction performed with the elbow flexor muscles. Maximal voluntary contraction (MVC) force was greater for men (393 ± 23 vs. 177 ± 7 N), which meant that the average target force (20% of MVC) was greater for men (79.7 ± 6.5 vs. 36.7 ± 2.0 N). The endurance time for the fatiguing contractions was 118% longer for women (1,806 ± 239 vs. 829 ± 94 s). The average of the rectified electromyogram (%MVC) for the elbow flexor muscles at exhaustion was similar for men (31 ± 2%) and women (30 ± 2%). In contrast, the heart rate and mean arterial pressure (MAP) were less at exhaustion for women (94 ± 6 vs. 111 ± 7 beats/min and 121 ± 5 vs. 150 ± 6 mmHg, respectively). The target force and change in MAP during the fatiguing contraction were exponentially related to endurance time (r2 = 0.68 and r2 = 0.64, respectively), whereas the change in MAP was linearly related to target force (r2 = 0.51). The difference in fatigability of men and women when performing a submaximal contraction was related to the absolute contraction intensity and was limited by mechanisms that were distal to the activation of muscle.
keywords:gender; pressor response; electromyography; elbow flexor muscles; muscle activation
INTRODUCTION
WOMEN ARE CAPABLE OF LONGER endurance times compared with men when performing isometric contractions at low to moderate intensities. This sex difference has been observed in several muscle groups, including adductor pollicis (5, 13), elbow flexors (19, 37), extrinsic finger flexors (32, 48), and knee extensors (27). The mechanism for this difference in endurance time is unknown. A common explanation has been that men, who are usually stronger, sustain greater absolute forces when the target force is based on an individual's strength (3, 28; cf. 13). Indirect evidence suggests that greater absolute forces are associated with increased intramuscular pressures, occlusion of blood flow, accumulation of metabolites, heightened metaboreflex responses, and impairment of oxygen delivery to the muscle (1, 25, 36, 41). Furthermore, activation of the metaboreflex, as measured by the rate of increase in the mean arterial pressure (MAP) and heart rate (pressor response) (29, 35), is inversely related to endurance time (9, 14, 38-40). Accordingly, women had longer endurance times when performing low-intensity contractions with the knee extensor muscles, but this difference disappeared during high-intensity contractions when both men and women would experience circulatory occlusion (27).
The endurance times of submaximal contractions that involve multiple muscles, however, could also be influenced by variation in the pattern of muscle activation (10, 24, 44, 45), perhaps including differences between men and women (42, 43). These observations raised the question of the relative contributions of the target force, circulatory limitations, and pattern of muscle activation to the observed sex difference in endurance time of the elbow flexor muscles. The purpose of this study was 1) to determine the relation between the absolute target force and endurance time for a submaximal isometric contraction and 2) to compare the pressor response and muscle activation patterns of men and women during a fatiguing contraction performed with the elbow flexor muscles. We found that the endurance time of women was greater than that for the men and that endurance time was inversely related to the absolute force sustained during the contraction. This difference in endurance time was accompanied by similar increases in electromyogram (EMG) during the fatiguing contraction for the men and women but by a reduced pressor response for the women. Preliminary accounts of these results have been presented in abstract form (11, 17).
METHODS
Subjects
Fourteen healthy adults (7 men, 26.3 ± 1.1 yr; and 7 women, 27.5 ± 2.3 yr) volunteered to participate in the study. All the subjects were right handed with no known neurological disorders. Before participation in the study, all subjects gave informed consent to a protocol approved by the Human Subjects Committee at the University of Colorado.
Mechanical Recording
Subjects were seated upright in an adjustable chair with the left (nondominant) arm abducted slightly, the elbow resting on a padded support, and the joint flexed to 90°. The hand and forearm were placed in a modified wrist-hand-thumb orthosis (Orthomerica, Newport Beach, CA), which held the forearm in a position midway between pronation and supination. The force exerted by the elbow flexor muscles in vertical and side-to-side (medial-lateral) directions was measured with a force transducer (Force-Moment Sensor, JR-3, Woodland, CA) that was mounted on a custom-designed, adjustable support. The vertical force was used to provide the target force for the fatiguing contraction, whereas the medial-lateral force provided a measure of the out-of-plane action of the involved muscles. The forces detected were recorded on digital tape (DAT Sony PC 116, Sony data Recording, Montvale, NJ). The force exerted in the vertical direction was displayed on a 14-in. computer monitor that was located 1 m in front of the subject.
Electrical Recordings
EMG signals were recorded with bipolar surface electrodes (Ag-AgCl, 8-mm diameter; 20-mm distance between electrodes) that were placed over the long head of biceps brachii, the short head of biceps brachii and brachioradialis, and the medial head of triceps brachii. Reference electrodes were placed on a bony prominence at the elbow or shoulder. The EMG of the brachialis muscle was measured with an intramuscular bipolar electrode inserted into the muscle ~3 cm proximal to the antecubital fold. The electrode comprised two stainless steel wires (100-μm diameter) that were insulated with Formvar (California Fine Wire, Grover Beach, CA). A surface electrode (8-mm diameter) placed on a bony prominence served as the reference electrode. The EMG signal was amplified (×500-2,000), band-pass filtered (20-800 Hz for the surface EMG and 20-1,000 Hz for the intramuscular EMG), recorded on digital tape, and displayed on an oscilloscope.
Cardiovascular Measurements
Heart rate and blood pressure were monitored throughout the fatiguing contraction with an automated beat-by-beat, blood pressure monitor (Finapres 2300, Ohmeda, Louisville, CO). The blood pressure cuff was placed around the middle finger of the right hand, and the arm was placed in a sling so that it was relaxed with the hand at heart level. The blood pressure signal was recorded on digital tape.
Experimental Protocol
Subjects were required to perform the protocol on three occasions, with 2 wk separating each session. Before the first experimental session, each subject visited the laboratory for an introductory session to become familiar with the equipment and the procedures, and each performed several trials of the maximal voluntary contraction (MVC) task. The experiments for each subject were performed at the same time of the morning on each occasion. The protocol comprised 1) MVCs with the elbow flexor and elbow extensor muscles, 2) an isometric contraction with the elbow flexor muscles that was sustained at 20% MVC force until exhaustion, and 3) another MVC with the elbow flexor muscles immediately after the fatiguing contraction.
MVC force. Subjects performed three MVC trials with the elbow flexor muscles and three MVC trials with the elbow extensor muscles. The MVC task consisted of a gradual increase in force from zero to maximum over 3 s, with the maximal force held for 2-3 s. Subjects were able to observe the exerted force on a monitor and were verbally encouraged to achieve maximal force. Subjects rested for 60-90 s between trials. If the peak forces from two of the three trials were not within 5% of each other, additional trials were performed until this was accomplished. The greatest force achieved by the subject was taken as the MVC force and used as the reference to calculate the target force for the fatiguing contraction. Subsequently, the MVC force for the elbow extensor muscles was determined by using the same procedures. Immediately on completion of the fatiguing contraction, a MVC was performed with the elbow flexor muscles.
Fatiguing contraction. The fatiguing contraction was performed at a target force of 20% MVC. The subject was required to match the target vertical force as displayed on the monitor and was verbally encouraged to sustain the force for as long as possible. The contraction was terminated when the subject deviated from the target force by 4% MVC force for >2 s, despite strong verbal encouragement. When this occurred, the subject was deemed to have reached exhaustion, and the duration of the contraction was recorded as the endurance time. Subjects were not informed of the endurance times until completion of the third session.
As an index of perceived effort, the rating of perceived exertion (RPE), was recorded using the modified Borg 10-point scale at regular time intervals (1-5 min between recordings) during the fatiguing contraction (2). Once the subject had attained a score of 8 on the Borg scale, the RPE was recorded every minute.
Data Analysis
The data were recorded on digital tape and then were digitized (analog-to-digital converter, 12-bit resolution) and analyzed off-line using the Spike2 data-analysis system (Cambridge Electronic Design, Cambridge, UK). The forces (vertical and medial lateral) and blood pressure were digitized at 200 samples/s, whereas the EMG signals were digitized at 2,000 samples/s.
The MVC force was quantified as the average value over a 0.5-s interval that included the peak force. Similarly, the maximal EMG for each muscle was determined as the average value over a 0.5-s interval that included the peak rectified EMG.
The amplitude of the force fluctuations was quantified as the coefficient of variation (CV = SD/mean × 100) for the first, middle, and last 60 s of the fatiguing contraction. The medial-lateral forces recorded during the fatiguing contraction were averaged over the duration of the fatiguing contraction.
The EMG during the fatiguing contraction was quantified in two ways: 1) for statistical analysis, as averages of the rectified EMG (AEMG) for the first, middle, and last 60 s of the fatiguing contraction; and 2) for graphic presentation, as averages of the rectified EMG for every 1% of the endurance time (100 data points). The EMG for each muscle was normalized to the maximum EMG obtained during the MVC. The normalized EMGs for the short and long heads of biceps brachii were averaged.
Heart rate and MAP during the fatiguing contraction were analyzed by comparing ~15-s averages at 10% intervals throughout the endurance time. For each interval, the blood pressure signal was analyzed for the mean peaks [systolic blood pressure (SBP)], mean troughs [diastolic blood pressure (DBP)], and the number of pulses per second (multiplied by 60 to determine heart rate). MAP was calculated for each epoch with the following equation: MAP = DBP + 1/3(SBP DBP).
As a supplement to the study on the elbow flexor muscles, we analyzed data on a hand muscle (first dorsal interosseus) that had been collected previously in our laboratory (12). Thirty-two men (n = 18) and women (n = 14) (age 20-40 yr) sustained an isometric abduction force with the index finger at either 20% (n = 6 men, 5 women), 35% (n = 7 men, 4 women), or 65% (n = 5 men, 5 women) of the MVC force for as long as possible. Each subject performed the fatiguing contraction at the same intensity on four occasions, with each session separated by 4-7 days.
Statistical Analysis
Data are reported as means ± SE unless stated otherwise. A two-factor (sex × session) repeated-measures, ANOVA (StatView, SAS Institute) was used to compare the dependent variables for endurance time, medial-lateral forces, and changes in heart rate and MAP for the fatiguing contraction. A three-factor, repeated-measures ANOVA [sex × session × time (rest, start, 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90%, 100%)] was used to compare the dependent variables for heart rate and MAP. Endurance time, MAP, and heart rate were further analyzed using analysis of covariance and varying for target force (sex × target force). A three-factor repeated-measures ANOVA [sex × session × time (before and after fatigue)] was used to compare MVC force. A three-factor [sex × session × time (first 60 s, middle 60 s, and last 60 s)] repeated-measures ANOVA was used to compare the dependent variables of AEMG and force fluctuations (CV) during the fatiguing contraction. To compare the AEMG of the elbow flexor muscles, a four-factor [muscle (biceps brachii, brachioradialis, brachialis) × sex × session × time (first 60 s, middle 60 s, and last 60 s)] repeated-measures ANOVA was utilized. A three-factor, repeated-measures ANOVA [sex × session × time (start, middle, end)] was used to compare the RPE and force fluctuations (CV). To compare the MVC force and endurance times of the men and women for the hand muscle, a two-factor (sex × session), repeated-measures ANOVA was used for the contractions performed at 20, 35, and 65% of MVC force. Post hoc analyses (Tukey-Kramer) were used to test for differences when appropriate. Regression analysis and curve fitting were performed using SigmaPlot 5.0 Scientific Graphing software (SPSS, Chicago, IL). A significance level of P < 0.05 was used to identify statistical significance.
RESULTS
The average endurance time of the women across the three sessions was longer than that for the men (1,943 ± 235 vs. 959 ± 111 s; P < 0.05). The endurance time for both the men and women increased across sessions (P < 0.05), such that session 3 was longer than sessions 1 and 2 and there was no difference between sessions 1 and 2 (P > 0.05). The adaptations in endurance time across sessions raised separate issues independent of the sex differences and so are not reported here (SK Hunter and RM Enoka, unpublished observations). Because the endurance times for men and women did not differ between sessions 1 and 2 (P > 0.05), all subsequent results are presented as the average of the first two sessions. The endurance time of the women (1,806 ± 239 s) was 118% longer than that for the men (829 ± 94 s, P < 0.05) (Table 1). However, there was no sex difference in endurance time (P = 0.35) when the difference in target force (men: 80 ± 7 N; women: 37 ± 2 N) was accounted for with a covariate analysis.
At the start of the protocol, the MVC force for the elbow flexor muscles of the women (177 ± 7 N) was 45% of the value for the men (393 ± 27 N; P < 0.05) (Table 1). The MVC force immediately after the fatiguing contraction was reduced by similar amounts for both the men (39.3 ± 6.5%) and the women (34.3 ± 6.5%; P > 0.05).
Force Fluctuations
When the effort associated with a sustained contraction becomes maximal, the exerted force exhibits low-frequency oscillations. Accordingly, we used the amplitude of the normalized force fluctuations (CV) as an index of effort during the fatiguing contraction. The CV for force increased progressively during the fatiguing contractions for both men and women (P < 0.05; Fig. 1). The recorded force fluctuations are apparent in Fig. 2 (trace at bottom). The increase in CV was similar for men and women (P > 0.05), which suggested that the relative effort was comparable. At the start of the contraction (first 60 s), the CV averaged 2.5 ± 0.2% and at the end of the contraction it was 10.0 ± 1.0%.
RPE
RPE during the fatiguing contraction began and ended at similar scores for the men and women, with no difference between sessions (P > 0.05). The RPE for the men and women was similar at 30 s into the contraction (1.5 ± 0.4 vs. 1.8 ± 0.2, respectively; P > 0.05) and at the midpoint of endurance time (7.4 ± 0.4 vs. 7.9 ± 0.6, respectively; P > 0.05). At exhaustion, all subjects had achieved a rating of 10. These results provided further evidence that the perceived effort during the fatiguing contraction was similar for men and women.
Medial-Lateral Forces
Because the elbow flexor muscles can exert a force in the transverse plane, the medial-lateral force was measured to quantify the magnitude of this action during the fatiguing contraction. The medial-lateral force was normalized to the target force. The most significant feature of the medial-lateral force was its variability, both between subjects and over the duration of the fatiguing contraction. On most occasions, the force was directed medially, which was denoted as the positive direction. The average medial-lateral force was not statistically different between men (10.0 ± 6.1%) and women (18.5 ± 8.3%; P > 0.05). The difference in endurance time between men and women, therefore, was not related to a consistent difference in the out-of-plane force exerted by the active muscles.
Adjustments in AEMG
For both men and women, the amplitude of the normalized AEMG for the elbow flexor muscles increased progressively during the fatiguing contractions (P < 0.05; Fig. 2). The increase in AEMG was similar for men and women (P > 0.05). The mean AEMG for all the elbow flexor muscles at the beginning, midpoint, and end of the fatiguing contraction was 14 ± 1, 20 ± 1, and 30 ± 2% for the men and 12 ± 1, 22 ± 1, and 31 ± 2% for the women. Because endurance time was longer for the women, this meant that the rate of increase in AEMG was greater for the men.
The increase in AEMG of the brachialis muscle, for both men and women, was different from that for biceps brachii and brachioradialis (P < 0.05; Fig. 3). At the beginning of the fatiguing contraction, the AEMG for brachialis was greater (18 ± 1%) than the average value for biceps brachii and brachioradialis (11 ± 1%). At exhaustion, however, the AEMG for brachialis (31 ± 2%) was similar to that for biceps brachii and brachioradialis (31 ± 2%). Thus the increase in AEMG for brachialis (73%) was less than that for biceps brachii and brachioradialis (192%).
AEMG for the antagonist muscle triceps brachii increased by a small but significant amount during the fatiguing contraction (Fig. 3), and this effect was similar across sessions. The triceps brachii AEMG was greater for women compared with men at the beginning (2 ± 0.2 vs. 1 ± 0.2%; P < 0.05) and the end of the fatiguing contraction (5 ± 0.4 vs. 3 ± 0.4%; P < 0.05).
MAP and Heart Rate
MAP increased during the fatiguing contraction (P < 0.05) for both men and women. The average increase in MAP during the fatiguing contraction was greater for men compared with women (P < 0.05; Fig. 4A). The MAP was not different between men and women either at rest (82.9 ± 1.6 vs. 82.1 ± 2.0 mmHg; P > 0.05) or within the first 15 s of the fatiguing contraction (108.5 ± 2.3 vs. 100.8 ± 3.0 mmHg; P = 0.06). At exhaustion, however, the increase in MAP was less for women (121.2 ± 4.8 mmHg) compared with men (149.8 ± 6.1 mmHg; P < 0.05). The increase of MAP from the beginning to the end of the fatiguing contraction was 38.3 ± 5.2% for men and 20.4 ± 3.0% for women. However, there was no main effect for sex when the MAP was covaried with target force (P > 0.05).
Heart rate increased during the fatiguing contraction (P < 0.05). As with the MAP, the increase in heart rate was greater for men compared with women (P < 0.05; Fig. 4B). Heart rate was similar for the men and women at rest (60 ± 4 vs. 66 ± 3 beats/min; P > 0.05) and at the start of the fatiguing contraction (73 ± 5 vs. 76 ± 4 beats/min; P > 0.05). At exhaustion, heart rate for women (94 ± 6 beats/min) was less than that for men (111 ± 7 beats/min; P < 0.05). The increase of heart rate from the beginning to the end of the fatiguing contraction was 53.2 ± 5.9% for men and 24.9 ± 5.8% for women. However, there was no main effect for sex when heart rate was covaried with target force (P > 0.05).
Endurance Time, Target Force, and MAP
The endurance times for sessions were inversely related to target force by an exponential decay, which meant that stronger individuals had briefer endurance times (r = 0.82; Fig. 5A). Similarly, the absolute change in MAP was inversely related to endurance time by an exponential decay (r = 0.80; Fig. 5B). The increase in MAP was positively associated with target force (r = 0.72), but, because of the variability in this association, the increase in MAP for some men was similar to that for women, despite these men having greater target forces (Fig. 5C).
Endurance Time and MVC Force for the Hand Muscle
We examined the relation between MVC force and endurance time for the first dorsal interosseus muscle on the basis of data that had been collected previously in our laboratory (12). There were no sex differences in endurance time for the first dorsal interosseus at any of the three intensities of contraction (20, 35, and 65% MVC) (P > 0.05), even though the men had greater MVC forces (39.5 ± 1.2 vs. 26.3 ± 1.3 N; P < 0.05) (Fig. 6A). These results were consistent across four repeat performances at each of the contraction intensities (P < 0.05). There was, however, a strong exponential relation between target force and endurance time for men and women, such that greater target forces were associated with briefer endurance times (r2 = 0.75) (Fig. 6B).
DISCUSSION
We found that women had longer endurance times than men when sustaining an isometric contraction at 20% MVC force with the elbow flexor muscles. Because the men were stronger than the women, there was no sex difference in endurance time when the data were covaried with the target force that was sustained during the contraction. Furthermore, there were no sex differences in the increase of AEMG at exhaustion, the reduction of MVC force after the contraction, the increase in force fluctuations, the average medial-lateral forces, or the change in RPE during the fatiguing contraction. However, the increase of the pressor response during the fatiguing contraction and at exhaustion was greater in the stronger individuals.
Comparable Fatigue for Men and Women
There was no evidence of a sex difference in the performance of the fatiguing contraction by the subjects. First, men and women displayed similar relative reductions in MVC force (37%) at exhaustion. Second, the increased amplitudes of force fluctuations that often characterize a fatiguing contraction (4, 6, 16, 43) were similar at exhaustion for the men and women. Third, the average medial-lateral forces were often large but were highly variable for both men and women and thus were not associated with differences in endurance time. Finally, the RPE scores were similar for the men and women at the midpoint of the fatiguing contractions and at exhaustion.
Endurance Time and Target Force Were Inversely Related
Given that the relative performance was comparable for men and women, we examined the target force, the pressor response, and muscle activation as explanations for the difference in endurance time. We observed that stronger individuals had a briefer endurance time and that this relation was exponential for both the elbow flexors and the hand muscle (Figs. 5 and 6). Furthermore, there was no sex difference in endurance time when the analysis covaried for the force that was sustained during the fatiguing contraction. Consequently, stronger individuals had shorter endurance times for actions by both a single muscle (first dorsal interosseus) and many muscles (elbow flexors), and these relations appeared to be exponential and independent of the sex of the individual. In contrast to our findings, others have reported no relation between handgrip strength and endurance times for isometric contractions performed at 30, 50, and 75% MVC, even though women had longer endurance times (48). Furthermore, women had longer endurance times for adductor pollicis when performing an intermittent isometric contraction at 50% MVC, even when men and women were matched for strength (13). Although we have found a consistent association between endurance time and absolute force, this is not a universal finding.
Women Had a Reduced Pressor Response
We examined the association between the pressor response and endurance time. The pressor response is a reflex-mediated adjustment in MAP that attempts to rectify the mismatch between perfusion and muscle metabolism during an isometric contraction (18, 34). We found that the MAP and heart rate were less in women compared with men during the contraction and at exhaustion. There are several possible explanations for the reduced pressor response of the women: 1) less muscle mass and a lower target force, resulting in greater muscle perfusion; 2) attenuated sympathetic neural outflow, resulting in greater muscle perfusion; 3) different substrate utilization and lower metabolite production; or 4) a similar metabolite production but a less responsive pressor response.
Our findings suggest that the pressor response was less in the women because of a lower absolute target force. We observed that those individuals who had the greatest increase in MAP had a shorter endurance time but sustained a greater absolute force. Furthermore, there was no sex difference in the pressor response when we statistically covaried for target force. These results, which are consistent with other observations, suggest that muscle mass is a primary determinant of the pressor response. For example, the endurance times of men are longer for low-force contractions compared with high-force contractions, but at exhaustion the pressor response was similar for the same muscle (9, 14, 39). In contrast, the pressor response is less at exhaustion for smaller muscle groups compared with larger muscle groups (30, 38, cf. 49). Consequently, the lesser increase in MAP and heart rate at exhaustion for the women may have been related to a smaller muscle mass. Because the force capacity of muscle is directly related to muscle size, stronger subjects may have experienced a greater mechanical compression of the arteries perfusing the active muscle that limited blood flow and led to an accelerated accumulation of metabolites (1, 36, 41). The heightened concentration of metabolites increases the activation of group III and IV afferents (20, 21) and contributes to the increase in MAP. Consequently, the endurance time of stronger individuals was likely limited by a greater restriction of muscle perfusion due to a greater muscle mass and target force.
Alternatively, the reduced increase in MAP in the women may have been the result of an attenuated sympathetic neural outflow (7, 31), possibly due to estrogen (8, 22, 23, 33), that reduced vasoconstriction, maintained muscle perfusion, and prolonged endurance time. Furthermore, sex differences in substrate utilization (46, 47) might reduce the rate of metabolite production and reflex-mediated change in MAP in women compared with men, which would also contribute to the prolongation of endurance time. However, when women performed an intermittent contraction at 30% MVC force with the finger flexor muscles under ischemic conditions, endurance time was similar to men even though the increase in MAP and metabolite production was less for women (7). This finding indicates that, when the circulatory adjustments were normalized in men and women, there was no sex difference in endurance time despite a lesser pressor response in women. Furthermore, it is also conceivable that the women had a similarly perfused muscle and production of glycolytic metabolites but a less responsive pressor response, although there is no evidence to support this possibility.
Sex Differences and Muscle Activation
The other factor we considered that might contribute to the sex difference in endurance time was the activation pattern of the muscle. Although the amplitude of AEMG at exhaustion did not reach the values observed during the MVC, the AEMG deficit was similar for the men and women (30% of maximum) and comparable to that reported previously (12, 48). However, the briefer endurance time for men meant that the rate of increase in AEMG was less for women. Because the progressive increase in the interference EMG during such conditions is mainly due to the recruitment of motor units (12, 15, 26), the greater rate of increase in AEMG for the men indicated an enhanced rate of motor unit recruitment. Presumably, the activated motor units fatigued more rapidly and additional units were required to achieve the target force. Nonetheless, the comparable values of AEMG at exhaustion for the men and women suggest that they eventually activated similar proportions of the motor neuron pools.
Aside from the average levels of AEMG, endurance time can also be influenced by the distribution of activation within a muscle and across a group of synergist muscles (10, 26, 42-45). There was evidence of intermittent bursts in the EMG, as our laboratory had observed in women after limb immobilization (42); however, this was common to both men and women and thus was not associated with the sex difference in endurance time. In contrast, there were differences in activation between the elbow flexor muscles. For example, the increase in AEMG during the fatiguing contraction was different for the brachialis compared with biceps brachii and brachioradialis. This pattern of activation, however, was similar for both men and women and so was not related to the longer endurance times of women. These findings suggest that coordination among the synergists did not contribute significantly to the enhanced endurance time of the women.
In summary, we found that the longer endurance time of women for a submaximal isometric contraction when performed with the elbow flexor muscles was associated with a lower absolute target force. Similarly, analysis of endurance times from a previous study (12) indicated that greater target forces for a hand muscle were associated with briefer endurance times and not the sex of the individual. The longer endurance time of the women for the elbow flexor muscles was associated with a reduced pressor response but was not related to the activation levels of the muscle at exhaustion. Consequently, the difference in endurance time between men and women for a submaximal contraction was related to the absolute contraction intensity and was limited by mechanisms that were distal to the activation of the muscle and involved the pressor response.
ACKNOWLEDGEMENTS
We thank Darren Flagg for assistance in conducting the experiments, Douglas Seals and Brian Tracy for comments on the manuscript, and Ohmeda (Louisville, CO) for loaning us the Finapres 2300.
FOOTNOTES
This research was supported by National Institute of Neurological Disorders and Stroke Grant NS-20544 (to R. M. Enoka).
Address for reprint requests and other correspondence: R. M. Enoka, Dept. of Kinesiology and Applied Physiology, Univ. of Colorado, Boulder, CO 80309-0354 (E-mail: Roger.Enoka@Colorado.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 29 May 2001; accepted in final form 15 August 2001.
REFERENCES
1.Barnes, WS. The relationship between maximum isometric strength and intramuscular circulatory occlusion. Ergonomics 23: 352-357, 1980.
2.Borg, GA. Perceived exertion. Exerc Sport Sci Rev 2: 131-153, 1974.
3.Carlson, BR. Level of maximum isometric strength and relative load isometric endurance. Ergonomics 12: 429-435, 1969.
4.Cresswell, AG, and L?scher WN. Significance of peripheral afferent input to the alpha-motoneurone pool for enhancement of tremor during an isometric fatiguing contraction. Eur J Appl Physiol 82: 129-136, 2000.
5.Ditor, DS, and Hicks AL. The effect of age and gender on the relative fatigability of the human adductor pollicis muscle. Can J Physiol Pharmacol 78: 781-790, 2000.
6.Ebenbichler, GR, Kollmitzer J, Erim Z, Loscher WN, Kerschan K, Posch M, Nowotny T, Kranzl A, Wober C, and Bochdansky T. Load-dependence of fatigue related changes in tremor around 10 Hz. Clin Neurophysiol 111: 106-111, 2000.
7.Ettinger, SM, Silber DH, Collins BG, Gray KS, Sutliff G, Whisler SK, McClain JM, Smith MB, Yang QX, and Sinoway LI. Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol 80: 245-251, 1996.
8.Ettinger, SM, Silber DH, Gray KS, Smith MB, Yang QX, Kunselman AR, and Sinoway LI. Effects of the ovarian cycle on sympathetic neural outflow during static exercise. J Appl Physiol 85: 2075-2081, 1998.
9.Fallentin, N, and J?rgensen K. Blood pressure response to low level static contractions. Eur J Appl Physiol 64: 455-459, 1992.
10.Fallentin, N, J?rgensen K, and Simonsen EB. Motor unit recruitment during prolonged isometric contractions. Eur J Appl Physiol 67: 335-341, 1993.
11.Flagg, D, Fleshner M, Hunter SK, and Enoka RM. Circadian rhythmicity of salivary cortisol levels in men and women is reliable (Abstract). Med Sci Sports Exerc 32: S271, 2000.
12.Fuglevand, AJ, Zackowski KM, Huey KA, and Enoka RM. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol (Lond) 460: 549-572, 1993.
13.Fulco, C, Rock P, Muza S, Lammi E, Cymerman A, Butterfield G, Moore L, Braun B, and Lewis S. Slower fatigue and faster recovery of the adductor pollicis in women matched for strength with men. Acta Physiol Scand 167: 233-239, 1999.
14.Gaffney, FA, Sjogaard G, and Saltin B. Cardiovascular and metabolic responses to static contraction in man. Acta Physiol Scand 138: 249-258, 1990.
15.Garland, SJ, Enoka RM, Serrano LP, and Robinson GA. Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol 76: 2411-2419, 1994.
16.Gottlieb, S, and Lippold OC. The 4-6 Hz tremor during sustained contraction in normal human subjects. J Physiol (Lond) 336: 499-509, 1983.
17.Hunter, SK, Flagg D, Fleshner M, and Enoka RM. The endurance time of a submaximal fatiguing contraction is reliable for men and women (Abstract). Med Sci Sports Exerc 32: S184, 2000.
18.Kagaya, A, and Homma S. Brachial arterial blood flow during static handgrip exercise of short duration at varying intensities studied by a Doppler ultrasound method. Acta Physiol Scand 160: 257-265, 1997.
19.Kahn, J, Kapitaniak B, Hueart F, and Monod H. Physiological modifications of local haemodynamic conditions during bilateral isometric contractions. Eur J Appl Physiol 54: 624-631, 1986.
20.Kaufman, MP, Longhurst JC, Rybicki KJ, Wallach JH, and Mitchell JH. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55: 105-112, 1983.
21.Kaufman, MP, Rotto DM, and Rybicki KJ. Pressor reflex response to static muscular contraction: its afferent arm and possible neurotransmitters. Am J Cardiol 62: 58E-62E, 1988.
22.Kendrick, ZV, and Ellis GS. Effect of estradiol on tissue glycogen metabolism and lipid availability in exercised male rats. J Appl Physiol 71: 1694-1699, 1991.
23.Kendrick, ZV, Steffen CA, Rumsey WL, and Goldberg DI. Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J Appl Physiol 63: 492-496, 1987.
24.Kulig, K, Powers CM, Shellock FG, and Terk M. The effects of eccentric velocity on activation of elbow flexors: evaluation by magnetic resonance imaging. Med Sci Sports Exerc 33: 196-200, 2001.
25.Lind, AR, and McNicol GW. Local and central circulatory responses to sustained contractions and the effect of free or restricted arterial inflow on post-exercise hyperaemia. J Physiol (Lond) 192: 575-593, 1967.
26.Maton, B, and Gamet D. The fatigability of two agonist muscles in human isometric voluntary submaximal contraction: an EMG study. Eur J Appl Physiol 58: 369-374, 1989.
27.Maughan, R, Harmon M, Leiper J, Sale D, and Delman A. Endurance capacity of untrained males and females in isometric and dynamic muscular contractions. Eur J Appl Physiol 55: 395-400, 1986.
28.Miller, A, MacDougall J, Tarnopolsky M, and Sale D. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol 66: 254-262, 1993.
29.Mitchell, JH, Kaufman MP, and Iwamoto GA. The exercise pressor reflex: its cardiovascular effects, afferent mechanisms, and central pathways. Annu Rev Physiol 45: 229-242, 1983.
30.Nagle, FJ, Seals DR, and Hanson P. Time to fatigue during isometric exercise using different muscle masses. Int J Sports Med 9: 313-315, 1988.
31.Ng, AV, Callister R, Johnson DG, and Seals DR. Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension 21: 498-503, 1993.
32.Petrofsky, J, Burse R, and Lind A. Comparison of physiological responses of women and men to isometric exercise. J Appl Physiol 38: 863-868, 1975.
33.Rooney, TP, Kendrick ZV, Carlson J, Ellis GS, Matakevich B, Lorusso SM, and McCall JA. Effect of estradiol on the temporal pattern of exercise-induced tissue glycogen depletion in male rats. J Appl Physiol 75: 1502-1506, 1993.
34.Rowell, L. Human Cardiovascular Control. New York: Oxford Univ. Press, 1993.
35.Rowell, LB, and O'Leary DS. Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physiol 69: 407-418, 1990.
36.Sadamoto, T, Bonde-Petersen F, and Suzuki Y. Skeletal muscle tension, flow, pressure, and EMG during sustained isometric contractions in humans. Eur J Appl Physiol 51: 395-408, 1983.
37.Sato, H, and Ohashi J. Sex differences in static muscular endurance. J Hum Ergol (Tokyo) 18: 53-60, 1989.
38.Seals, DR. Influence of active muscle size on sympathetic nerve discharge during isometric contractions in humans. J Appl Physiol 75: 1426-1431, 1993.
39.Seals, DR. Influence of force on muscle and skin sympathetic nerve activity during sustained isometric contractions in humans. J Physiol (Lond) 462: 147-159, 1993.
40.Seals, DR, and Enoka RM. Sympathetic activation is associated with increases in EMG during fatiguing exercise. J Appl Physiol 66: 88-95, 1989.
41.Sejersted, O, Hargens A, Kardel K, Blom P, Jensen O, and Hermansen L. Intramuscular fluid pressure during isometric contraction of human skeletal muscle. J Appl Physiol 56: 287-295, 1984.
42.Semmler, JG, Kutzschner DV, and Enoka RM. Gender differences in the fatigability of human skeletal muscle. J Neurophysiol 82: 3590-3593, 1999.
43.Semmler, JG, Kutzscher DV, and Enoka RM. Limb immobilization alters muscle activation patterns during a fatiguing isometric contraction. Muscle Nerve 23: 1381-1392, 2000.
44.Sjogaard, G, Kiens B, Jorgensen K, and Saltin B. Intramuscular pressure, EMG and blood flow during low-level prolonged static contraction in man. Acta Physiol Scand 128: 475-484, 1986.
45.Tamaki, H, Kitada K, Akamine T, Murata F, Sakou T, and Kurata H. Alternate activity in the synergistic muscles during prolonged low-level contractions. J Appl Physiol 84: 1943-1951, 1998.
46.Tarnopolsky, LJ, MacDougall JD, Atkinson SA, Tarnopolsky MA, and Sutton JR. Gender differences in substrate for endurance exercise. J Appl Physiol 68: 302-308, 1990.
47.Tarnopolsky, MA. Gender differences in substrate metabolism during endurance exercise. Can J Appl Physiol 25: 312-327, 2000.
48.West, W, Hicks A, Clements L, and Dowling J. The relationship between voluntary electromyogram, endurance time and intensity of effort in isometric handgrip exercise. Eur J Appl Physiol 71: 301-305, 1995.
49.Williams, CA. Effect of muscle mass on the pressor response in man during isometric contractions. J Physiol (Lond) 435: 573-584, 1991.(Sandra K. Hunter and Roge)