Biceps Brachii Muscle Length Affects Force Steadiness with and Without Fatigue

Abstract

Purpose

The purpose of this study was to examine the influence of muscle length and fatigue on maximal force, submaximal force steadiness, and electromyographic (EMG) activity of the biceps brachii.

Methods

Force and EMG responses were measured before and after a fatigue protocol consisting of maximal intermittent contractions of the elbow flexors until task failure (n = 20). The protocol was performed on two separate occasions in a randomized order. During one visit, the elbow joint was at 90° (EF90) and for the other, it was extended to 120° (EF120).

Results

The results show a large effect size for greater force loss following fatigue at long muscle length (P = 0.067, \(\eta_{p}^{2}\) = 0.166). The fatigue-based decreases in force steadiness were not different between muscle lengths (P = 0.502, \(\eta_{p}^{2}\) = 0.024). Force steadiness was lower at long muscle length before and after fatigue (P < 0.01, d = 0.691). Following fatigue, muscle excitation decreased and increased during maximal and submaximal force tasks, respectively, yet there were no length-dependent EMG responses.

Conclusions

The novel findings show fatigue at long muscle length likely affects force loss to a greater degree than fatigue-based decreases in force steadiness. These data show lower elbow flexion force steadiness when the biceps brachii is in a lengthened position.

Introduction

Skeletal muscle fatigue and muscle length directly influence motor performance. Maximal muscle force weakens in the presence of fatigue and changes based on joint angle. These same factors moderate the ability to steadily control force output [9, 32]. Considerable evidence shows length-dependent fatigue responses for many skeletal muscles, yet it is unclear whether the unique responses result from differences in central nervous system control or from peripheral factors related to the muscle. Some reports show less fatigue when the agonist muscle contracts at shorter muscle lengths, yet greater fatigue at longer lengths [22, 25, 28, 38], however, the reports are conflicting and the mechanisms unclear [10]. A primary interest is discerning whether the key mechanisms responsible for length-dependent fatigue are explained by factors more related to the central nervous system’s control of muscle force or by peripheral factors related to the contractile function within the muscle itself. The simultaneous study of fatigue-based changes in force steadiness and maximal muscle force across muscle lengths should provide insight into this question given the different mechanisms supporting these two features of motor control.

Force steadiness is the ability to maintain a constant isometric voluntary force around a specified force level. The relative amplitude of force fluctuations during steady contraction reflects the degree of force steadiness, where lower force fluctuations indicate better force steadiness and thus greater force control [4, 18, 26]. Force steadiness is important not only for its relation to functional mobility but also because it provides insight into how the central nervous system controls muscle force. More specifically, force steadiness is a function of the summed neural drive from spinal, supraspinal, and proprioceptive inputs onto the active motor neurons [18, 31, 32, 36]. Different levels of force steadiness reflect variations in the descending neural drive, afferent feedback, or a combination of both [14, 39]. Surface electromyography (EMG) is a useful method linking well with examinations of force steadiness. For the biceps brachii muscle, the amplitude of the EMG signal provides an index of muscle excitation as a quasi-linear increase in EMG amplitude occurs with increases in force output, which is primarily attributed to greater motor unit recruitment and increases in motor unit firings [19, 21]. The EMG frequency content closely relates to the conduction velocity of the muscle fiber membrane and is more sensitive to peripheral disruptions within the muscle [17]. Although direct motor unit recordings from the biceps brachii show length-dependent alterations in motor unit firing behavior [8, 35], the extent to which these changes in submaximal motor unit activity influence fatigability and force control are unclear. Nevertheless, some suggest length-dependent alterations in motor unit activity explain the greater fatiguability [37, 38] and force steadiness impairments [4, 14] at long muscle lengths. Despite data showing muscle fatigue and muscle length independently alter maximal muscle force, force steadiness, and muscle excitation, the interaction between these two concepts have not been fully described.

The present experiment addresses this issue by examining the force and surface EMG responses following a maximal fatigue protocol with the elbow flexors in two different elbow joint positions. Our approach sought to use an ‘optimal’ elbow joint position (e.g., elbow angle at 90°) as a control and compare the responses to those obtained with the elbow joint in an extended position (e.g., elbow angle at 120°) similar to previous experimental paradigms [3, 13, 25]. The rationale being that elbow joint angle may be used as a proxy for biceps brachii muscle length, thereby allowing comparisons between optimal versus long muscle lengths of the primary elbow flexor. We hypothesized that the long muscle length would exacerbate force loss and fatigue-based decreases in force steadiness.

Methods

Participants

Thirty-one participants voluntarily enrolled in the study. However, eight participants withdrew and three participants’ data were excluded because their maximal force values were greater following the fatigue protocol for both experimental visits, thereby violating the assumption of the experiment (i.e., fatigue). As a result, 20 participants data were analyzed (age = 22 ± 3 years; stature = 174.1 ± 12.3 cm; mass = 77.1 ± 15.6 kg; n = 5 females). All participants read and signed an informed consent document and completed a health history questionnaire. Limb dominance was determined based on throwing preference (n = 2, left-hand dominant). None of the participants reported any orthopedic or neurological disorders. This study was approved by the Institutional Review Board for the University of Oklahoma (IRB #6070). Participants reported to the laboratory on three occasions with approximately 48 h between each visit. The first was used as a familiarization, while the next two experimental visits were completed in a randomized order. During the familiarization visit, the participants completed an abbreviated version of the experimental protocol.

Experimental Design

This experiment sought to examine the influence of muscle length on force and EMG responses. During the experimental visits, force and EMG measurements were collected immediately before and after a fatigue intervention. During one visit, the participant performed all measurements at an optimal elbow angle of 90° (EF90). The other experimental visit was completed with an extended elbow angle of 120° (EF120). All force measurements and fatiguing contractions were performed at the respective elbow angle for each visit.

Isometric Testing

The maximal voluntary contraction (MVC) force of the dominant elbow flexors was measured in a custom-built strength testing apparatus. With the participant in a seated position, their wrist was placed within a cuff attached to a tension–compression load-cell (Model SSM-AJ-500; Interface, Scottsdale, AZ, USA) with their hand in a supinated position. The elbow joint was placed within a U-shaped pad that helped prevent extraneous movement during strength testing. The procedures for strength testing were the same for EF90 and EF120, the only difference was the elbow joint angle (Fig. 1a). A goniometer (Elite Medical Instruments) was used to determine the appropriate elbow angle (i.e., 90° and 120°) for each visit (full extension = 180°). Strength testing began following a series of submaximal isometric contractions to warm-up. Each participant performed two separate 5-s MVCs with approximately 90 s of recovery between each attempt. Specific verbal instructions to ‘flex your elbow as hard as possible’ were provided before each MVC attempt, participants also received a verbal countdown prior to each attempt “three, two, one, pull!”. Strong verbal encouragement was provided throughout the duration of each maximal attempt. Following strength testing, the participants performed a submaximal trapezoidal force matching task to evaluate force steadiness. Specifically, the participants watched their force output on a computer monitor that was at eye-level approximately 1 m from them. The Delsys software (EMGworks®) overlaid the participants force on a trapezoidal template in real-time. The participants were instructed to match their force as closely as possible to the template. A representation is shown in Fig. 1b. The participants gradually increased their force output from 0% to 50% of their MVC at a rate of 10%MVC/s, held as steadily as possible at 50% MVC for 10 s, and then gradually returned their force from 50% to 0% at a rate of 10%MVC/s. This task was performed twice after each strength measurement (i.e., pre-fatigue and post-fatigue). The amplitude of the force fluctuations during the plateau of the force-matching task was used to quantify force steadiness by calculating the coefficient of variation with the below formula. The coefficient of variation was computed for each submaximal force tracing and then averaged and retained for statistical analysis.

$$Coefficient \, of \,variation = \frac{Standard \, deviation}{{Mean }} \times 100.$$
Fig. 1
figure1

a An illustration of the experimental testing setup for the present study along with a b representative force tracing from one participant during the submaximal force-matching task. The participants force is shown in the thin black line overlaid on the trapezoid with the corresponding EMG activity directly below

Fatigue Protocol

The fatigue protocol consisted of repeated 10-s maximal contractions of the dominant elbow flexors with a 50% duty cycle (i.e., 10-s on, 10-s off). The protocol was terminated once the participant could not reach 60% of their original MVC value for 5 s. Following protocol termination, maximal force and EMG measurements were obtained within approximately 30 s to determine the fatigue response. Fatiguability was defined as the loss in maximal force following the fatigue protocol.

EMG Signal Acquisition and Processing

Bipolar surface EMG signals were detected from the biceps brachii of the dominant arm. The bipolar electrode (10.0 × 1.0 mm silver bars, 10.0 m interelectrode distance, DE-2.1: Delsys, Inc. Natick, MA) was secured over the belly of the biceps brachii per the recommendations from the SENIAM project [16]. A reference electrode was placed over the 7th cervical vertebrae. To faithfully replicate sensor placement across visits, the location of the electrode was outlined with indelible ink. The analog EMG signals were preamplified (gain = 1000) with a modified Bagnoli 16-channel EMG system (Delsys, Inc., Natick, MA.), high- and low-pass filtered at 10 Hz and 500 Hz, respectively, with a fourth-order Butterworth filter. A tension–compression load-cell was used for all force measurements. The force and EMG signals were digitized at a sampling rate of 20 k Hz with a 12-bit analog-to-digital converter (NI 9201, National Instruments, Austin, TX, USA). The amplitude and center frequency of the EMG signal were quantified as the root mean square (RMS) and the median frequency (MDF), respectively. The highest 3-s portion of the MVC and the mean from the 5-s window of the submaximal task plateau were used to determine the EMG amplitude and MDF values. The values were calculated for each MVC and submaximal force tracing and then averaged and retained for statistical analysis. The submaximal EMG amplitude and MDF values during the submaximal task were normalized to the maximal values obtained during MVC of the respective visit.

Statistical Analyses

Separate two-way (time [pre, post] × length [EF90, EF120]) repeated measures analysis of variance (ANOVA) tests were performed on maximal force, submaximal force steadiness, and the corresponding EMG amplitude and EMG MDF values. Estimates of effect size are reported for all ANOVA tests with the partial-eta squared (\(\eta_{p}^{2}\)) statistic, with values of 0.01, 0.06, and 0.14 corresponding to small, medium, and large effects, respectively [34]. Cohen’s d values are reported for all mean comparisons. All data are reported as means ± SD. Analyses were performed with JASP software (JASP Team 2019, Version 0.10.2.0). Alpha was set at 0.05.

Results

Maximal Isometric Force

The results from the two-way ANOVA test for MVC force showed main effects for muscle length (P = 0.014, \(\eta_{p}^{2}\) = 0.279) and time (P < 0.01, \(\eta_{p}^{2}\) = 0.717), but there was no length × time interaction (P = 0.067, \(\eta_{p}^{2}\) = 0.166). Figure 2 shows the main effects for maximal force. Collapsed across time, the MVC values for EF90 were greater than EF120 (P = 0.014, d = 0.607). Collapsed across length, the MVC values at post were lower than pre (P < 0.01, d = 1.55). The results for EMG amplitude showed a main effect for time (P < 0.01, \(\eta_{p}^{2}\) = 0.480), but no main effect for length (P = 0.722, \(\eta_{p}^{2}\) = 0.007) and no length × time interaction (P = 0.813, \(\eta_{p}^{2}\) = 0.003). Collapsed across length, the EMG amplitude values at post were less than pre (P < 0.01, d = 0.937). The results for EMG MDF showed no main effect for length (P = 0.137, \(\eta_{p}^{2}\) = 0.113) or time (P = 0.282, \(\eta_{p}^{2}\) = 0.061) and no length × time interaction (P = 0.578, \(\eta_{p}^{2}\) = 0.017). Table 1 shows the mean values for the EMG data for the maximal and submaximal force tasks before and after the fatigue protocol.

Fig. 2
figure2

Individual and mean (bars) values for maximal isometric force of the elbow flexors before and after fatigue for the long (EF120) and optimal (EF90) muscle length fatigue tasks. The mean relative force loss was − 20.6% and − 12.8% for EF120 and EF90, respectively. *Significantly lower force following fatigue. ǂSignificantly lower force compared to EF90

Table 1 The EMG data (mean ± SD) during the maximal and submaximal tasks for both elbow positions before and after the fatigue protocol

Submaximal Force Task

The results from the two-way ANOVA test for the coefficient of variation during the submaximal force task showed main effects for muscle length (P < 0.01, \(\eta_{p}^{2}\) = 0.334) and time (P < 0.01, \(\eta_{p}^{2}\) = 0.350), but there was no length × time interaction (P = 0.502, \(\eta_{p}^{2}\) = 0.024). Figure 3 shows the main effects for force steadiness. Collapsed across time, the coefficient of variation values for EF120 were greater than EF90 (P < 0.01, d = 0.691). Collapsed across length, the coefficient of variation values were greater at post compared to pre (P < 0.01, d = 0.716). The results for normalized EMG amplitude showed a main effect for time (P < 0.01, \(\eta_{p}^{2}\) = 0.361), but no main effect for length (P = 0.280, \(\eta_{p}^{2}\) = 0.061) and no length × time interaction (P = 0.780, \(\eta_{p}^{2}\) < 0.01). Collapsed across length, the normalized EMG amplitude values at post were greater than pre (60.23% vs. 53.53%, P < 0.01, d = 0.712). The results for normalized EMG MDF showed no main effect for length (P = 0.959, \(\eta_{p}^{2}\) < 0.01) or time (P = 0.414, \(\eta_{p}^{2}\) = 0.035) and no length × time interaction (P = 0.978, \(\eta_{p}^{2}\) < 0.01).

Fig. 3
figure3

Individual and mean (bars) force steadiness values of the elbow flexors before and after fatigue for the long (EF120) and optimal (EF90) muscle length tasks. The mean relative increases in force variability were + 22.6% and + 21.1% for EF120 and EF90, respectively. *Significantly greater force variability following fatigue. ǂSignificantly greater force variability compared to EF90

Discussion

This study examined the force and EMG responses before and after a fatigue protocol with the elbow flexors at two different elbow joint angles. The main finding shows a non-significant trend for greater force loss following fatigue at long versus optimal muscle length. In addition, there were similar fatigue-based increases in force fluctuations between muscle length conditions. Following fatigue, relative force loss was generally greater at long (− 20.6%) versus optimal (− 12.8%) muscle lengths yet increases in force variability were similar (+ 22.6% vs. + 21.1%, respectively). Force steadiness was more variable before and after fatigue when the biceps brachii was in a lengthened versus optimal position. There were no significant length-dependent EMG responses, maximal and submaximal muscle excitation decreased and increased, respectively, following the fatigue protocol irrespective of muscle length.

Maximal Force Task

Muscle length is known to modulate maximal force [20]. In vivo experiments examining this topic typically manipulate joint angles to shorten or lengthen the prime movers. Here, an optimal elbow joint angle for maximal force served as a control against an extended elbow angle and thus longer biceps brachii muscle length, similar to other in vivo muscle length-tension experimental paradigms [3, 13, 25]. Although many define the optimal elbow angle for maximal force production at 90° during supinated elbow flexion, it should be noted the optimal position can vary between individuals, which likely results from inter-individual differences in optimal fascicle length and moment arms [20, 27]. We observed a significant difference in maximal elbow flexion strength with and without fatigue. Before the fatigue protocol, the average maximal force at long muscle length was ~ 4% lower than optimal. Following the fatigue protocol, this difference widened to ~ 13%. Lower maximal force at long muscle lengths has been shown for single-joint and multiarticular movements [10, 11, 20, 23]. The primary mechanisms to explain this effect are mainly peripheral in origin and revolve around differing muscle moment arms and the length-tension relationship [20]. It is challenging to reconcile the precise mechanisms contributing to the differences in maximal strength before and after fatigue in this study given the modest difference in elbow joint angle (i.e., 30°). For elbow flexion, ascending-descending strength curves are seen as elbow joint angle increases from a flexed to extended position (i.e., the inverted-U) [11, 20, 23]. Although Murray et al. [27] show in a sample of cadavers that sarcomere lengths are longer for the elbow flexors when the elbow is extended versus at ~ 90°, they report the large moment arm of the biceps brachii muscle allows it to operate over a broad range of fascicle lengths (and thus elbow joint angles). Therefore, a smaller moment arm in the extended elbow position is likely the primary mechanism for the lower maximal strength values with less influence from the length-tension properties of the elbow flexor muscles [20]. It is important to note that decreases in pennation angles and fascicle insertion angles have been shown for the elbow flexors with the elbow joint in an extended versus flexed position during low intensity flexion contraction [2, 15], therefore mechanisms related to muscle architecture between elbow joint positions in the current study may also have a role for the lower strength values in the extended elbow position.

The neural contributions to the length-dependent changes in muscle force, however, are not as clear. Despite lower maximal force at the long muscle length, our observation that elbow joint angle did not influence maximal muscle excitation agrees with previous reports on the EMG–force relationship of the biceps brachii [11, 23]. Therefore, even with different muscle moment arms and force–length properties during elbow flexion, it is reasoned the level of muscle excitation for the biceps brachii is predicated upon the total available force output [11, 23]. The present data show no significant effect of muscle length on EMG center frequency, although there was a large effect (\(\eta_{p}^{2}\) = 0.113) for lower values at the long muscle length. It is possible the modest change in elbow angle in this study did not provide sufficient muscle length change to detect length-dependent EMG MNF responses, as there are reports of lower EMG MDF values at long muscle lengths for a variety of skeletal muscles [1, 11, 24]. Whether the length-dependent response is physiological or an artifact of sensor placement is not fully clear. Some [1, 24] suggest that lower muscle fiber conduction velocities at longer muscle lengths may explain this effect, whereas others [11] speculate geometrical differences in muscle fiber diameter, skin tissue thickness, and/or differences in electrode pick-up area likely account for the length-dependent response for EMG MDF.

Muscle fatigue is a task-dependent process that lowers the maximal force capacity of the neuromuscular system. In the present study, significantly lower levels of maximal muscle excitation were observed for both muscle lengths following fatigue. The depression in EMG amplitude is attributable to lower motor unit activity. There were no significant changes in maximal EMG MDF following the protocol at either length. Although the frequency content of the EMG signal shows intensity-dependent decreases during sustained isometric contractions to task failure [6], the intermittent nature of the present fatigue protocol likely attenuated the intramuscular metabolic disruption with the restoration of blood flow between maximal contractions [5]. Several reports show an inverse relationship between fatigability and muscle length [22, 28]. This observation is not entirely uniform and consideration of the fatigue protocol and the muscle groups involved is important. The present data builds upon previous experiments for the length-dependent properties of muscle fatigue for the elbow flexors. Our observations show force loss was generally greater following fatigue at long versus optimal muscle lengths, approximately 70% of the participants lost more of their relative force in the lengthened position. In a similar experimental design, McKenzie and Gandevia [25] show the elbow flexors lost less force at a shortened elbow angle (e.g., 45°) compared to optimal (e.g., 90°) during a series of 18 maximal, 10 s contractions. When linked with these [25] previous findings, there appears to be a direct relationship between fatigability (force loss) and muscle length for the elbow flexors. However, it is important to recognize that McKenzie and Gandevia [25] used a fatigue protocol with a standardized volume, not a task failure approach as the present study. Despite the large effect size for force loss between muscle lengths, there were no length-dependent EMG responses in the present study. This observation differs from those of Doud and Walsh [12] who reported greater changes in the EMG frequency content of the biceps brachii for the smaller angles of flexion at task failure following fatiguing submaximal (~ 50% concentric 1RM) elbow flexions in a smaller sample of participants (n = 5). The different EMG responses between the present and previous [12] data are not clear, but it is likely that task demands (i.e., submaximal versus maximal, dynamic versus isometric) account for the discrepancies. For instance, it is not clear if the greater frequency content compression at the short versus long muscle position of the concentric contraction was due to muscle length itself or the greater concentration of metabolic byproducts within the muscle at the end of the 3 s contraction (i.e., short) versus the start (i.e., long) [12].

Additional insight regarding potential mechanisms to account for the length-dependent fatigability responses may be drawn from the comparatively greater number of investigations in the lower limbs. For the lower limbs, there are data showing length-dependent alterations in patterns of motor unit activity during fatigue [1, 10, 22, 37]. Weir et al. [37] show greater rates of change in the EMG amplitude of the tibialis anterior at long versus short muscle lengths despite no differences in relative force loss between lengths. Some reports [1] show longer muscle lengths result in lower muscle fiber conduction velocity, shorter times to task failure, and greater rates of electrophysiological fatigue. These data [1, 37] show there may be time-dependent EMG fatigue processes related to muscle length that were not captured by the present experimental design. Desbrosses et al. [10] provide a thorough examination of the mechanisms accounting for length-dependent differences in fatigability. With their unique design, the authors show similar force loss following a maximal knee extensor fatigue protocol at long and short muscle lengths, yet they report different manifestations of fatigue between conditions. Specifically, fatigue at short muscle lengths brought about greater deficits in voluntary activation and EMG amplitude, whereas the relative decrements in the amplitude of the potentiated twitch were greater following fatigue at long muscle lengths. The latter finding supports the notion that greater fatigability at long muscle lengths is due to larger contractile dysfunction. Whether the increased contractile perturbations at long muscle lengths are accounted for by greater rates of metabolism and/or impairments in excitation–contraction coupling is not clear [10, 22].

Submaximal Force Task

Data showing the influence of muscle length on force steadiness primarily focuses on the lower limb [18, 29, 33], while less is known on this topic for the upper limb [4]. The present results are in line with the majority of the published literature on this topic. Specifically, we show lower force steadiness when the elbow joint was extended, and thus the biceps brachii in a lengthened position. Impairments in force control at long muscle lengths have been shown for the quadriceps muscles. Krishnan et al. [18] observed greater force fluctuations for the knee extensors during a submaximal force-matching task at 50% MVC when the knee was in a more flexed joint position. It has been shown that even with a constant elbow joint angle, variations in forearm posture (i.e., neutral, supinated, pronated) influence elbow flexor force steadiness. Specifically, Brown et al. [4] show that across a range of submaximal intensities, force output was less steady when the forearm was in a pronated position compared to a neutral or supinated position. This finding merges well with the current data as it shows length-dependent changes in force steadiness for the elbow flexors. Explanations for lower force steadiness at long muscle lengths are not entirely clear. Krishnan et al. [18] provide data showing higher levels of agonist muscle excitation at long muscle lengths contributes to lower force steadiness, with antagonist muscle excitation having an inconsequential role [18]. The authors [18] also speculate lower EMG MDF at long muscle lengths reflects greater motor unit synchronization and thus explains the lower force steadiness. However, the limitations imposed when interpreting motor unit firing properties from bipolar surface EMG, the absence of length-dependent EMG responses for the current study, and the controversial role on motor unit synchronization on force steadiness [9, 36] challenge this speculation. Additional explanations for length-dependent force steadiness relate to the influence of muscle afferent input, most notably group Ia, on the motor neuron pool as there are data showing changes in muscle length modulate motor unit firing properties [8, 14, 30]. For instance, Christova et al. [8] show the mean motor unit interspike intervals for the biceps brachii were lower when the elbow was at 90° versus 120° for the majority of motor units detected. Harwood et al. [14] report higher motor unit recruitment thresholds and lower motor unit firing rates for the short head of the biceps brachii with the forearm in a pronated versus supinated position. Recent data also shows lower spinal excitability for the biceps brachii when in a pronated versus supinated forearm position [39]. Collectively, subtle changes in the length of the biceps brachii cause functional consequences in elbow flexion force control, the mechanisms of which likely relate to a combination of muscle afferent mediated alterations in motor unit firing properties, spinal excitability, and descending neural drive [4, 14, 39].

The present data show fatigue impairs force steadiness regardless of muscle length. In agreement with others, significant increases in force variability and muscle excitation are shown following fatigue. Interestingly, these responses were unaffected by muscle length as the relative changes were similar between conditions with negligible effect sizes for the EMG amplitude and force data. These results are in line with others [9, 26] showing elevations in submaximal EMG amplitude at the same absolute submaximal force level following fatigue. The higher EMG amplitude values following fatigue indicate higher threshold motor units were recruited to compensate for the contractile dysfunction brought about by the fatigue protocol. The greater twitch forces, lower firing rates, and longer interspike intervals in the firing properties of higher-threshold motor units are likely mechanisms contributing to greater force variability following fatigue [9, 26]. In a thorough experimental design, Missenard et al. [26] provide data showing greater muscle excitation following fatigue is the primary factor contributing to fatigue-based decreases in force steadiness. The support for this hypothesis stems from the observation that when participants matched the same absolute submaximal force following fatigue, greater force variability occurred across a range of intensities, yet when the participants matched their level of muscle excitation there was no change in force variability at moderate forces (~ 30%–50% MVC). Since fatigue and long muscle lengths independently decrease force steadiness, the obvious question raised from our findings is how was there no additive effect of these two variables on force control? In consideration with others [26], it is likely that similar elevations in neural drive were necessary to accomplish the force task following fatigue despite differences in muscle length.

Limitations

Several limitations must be considered when interpreting the present results. Perhaps the greatest limitation when interpreting the present experiment is the absence of the time to task failure data for the two tasks. Although our approach provides direct comparisons of force and EMG changes following the same degree of fatigue (i.e., task failure), useful information related to length-dependent fatigue resistance would have been provided with the time to task failure. Importantly, the maximal EMG values were not normalized to the compound muscle action potential and we were unable to measure voluntary activation. In addition, our EMG measurements captured the global activity of the biceps brachii as we did not differentiate between the long and short heads of the muscle, this is important because changes in muscle length may differentially affect the activity of the two heads of the biceps brachii [14]. We did not capture antagonist or synergist muscle activity, both of which are influenced by changes in joint position [11] and fatigue [7]. More robust interpretations would have been afforded by examining the excitation properties of agonist–antagonist muscle pairs, unfortunately our experimental setup did not permit appropriate EMG recordings from the triceps brachii. We were also unable to measure muscle fascicle length and pennation angle and thus relied solely on elbow joint configuration as a proxy for muscle length. Indeed, muscle length is a function of joint angle, but a deeper view of muscle architecture would have provided richer information. Finally, comparing these responses between sexes would have been a worthwhile pursuit given the paucity of data in this area [4]. Future studies addressing the knowledge gap regarding sex-based differences in force control will benefit our understanding of human motor control.

Conclusions

In conclusion, the present data show length-dependent force steadiness responses for the elbow flexors. We also show a large effect size for greater force loss following fatigue at long muscle lengths compared to optimal. Importantly, there were similar fatigue-based increases in submaximal force variability between muscle lengths. Force variability is greater at long muscle lengths with and without the presence of fatigue during elbow flexion. This novel finding should be examined in other muscle groups with different muscle spindle densities. Overall, the EMG data for the biceps brachii do not explain the differences in fatigue or force steadiness between long and optimal muscle lengths. The depression and elevation of muscle excitation for the maximal and submaximal force tasks, respectively, were similar between elbow joint positions following fatigue. We speculate the large effect for greater force loss at long muscle lengths is due to greater impairments in contractile function [10], yet the similar changes in force variability suggests fatigue-based changes in the mechanisms impairing force control are not length-dependent. The present findings may be useful to practitioners when prescribing isometric strength training at long muscle lengths. These findings offer additional insight into the length-dependent properties of motor control.

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The authors thank Evan Murta, Designer for the customized illustrations.

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Carr, J.C., Ye, X. & Tharp, H.M. Biceps Brachii Muscle Length Affects Force Steadiness with and Without Fatigue. J. of SCI. IN SPORT AND EXERCISE (2021). https://doi.org/10.1007/s42978-020-00102-0

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Keywords

  • Neuromuscular fatigue
  • EMG
  • Elbow flexors
  • Force control