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Department of 1 Physical Therapy, 301 McKinly Laboratory, University of Delaware, Newark, DE 19716, USA
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(Received 13 March 2006;
accepted after revision 22 June 2006; first published online 14 August 2006)
Corresponding author S. Binder-Macleod: Department of Physical Therapy, 301 McKinly Laboratory, University of Delaware, Newark, DE 19716, USA. Email: sbinder{at}udel.edu
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Introduction |
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During FES, however, skeletal muscles fatigue more rapidly during repetitive stimulation than during volitional contractions (Marsolais & Edwards, 1988; Riener, 1999). Rapid fatigue during FES is thought to result from the differences in motor unit recruitment order, higher activation frequencies and imprecise control of muscle force during FES compared to volitional contractions (Peckham & Knutson, 2005). The problem of muscle fatigue is further compounded by the fact that paralysed muscles show greater fatigability than healthy muscle (Gerrits et al. 1999, 2003). Muscle fatigue is an important factor limiting the clinical use of FES (Riener, 1999). During repetitive electrical stimulation, stimulation frequency and intensity are two primary parameters that can be modulated to control skeletal muscle force. Although numerous combinations of frequency and intensity can be used to generate the required muscle force during FES, most clinical FES systems use the minimum frequency that can generate a fused tetanic contraction in the muscle being stimulated and vary the intensity to produce the desired force (Taylor et al. 1999; Weber et al. 2005). The stimulation intensity is further increased as the muscle fatigues (Taylor et al. 1999; Weber et al. 2005). The rationale for using low frequencies in FES is based on the premise that higher frequencies cause greater fatigue (Bigland-Ritchie et al. 1979; Garland et al. 1988). Although several previous studies have shown that fatigue is a function of the stimulation frequency or the number of pulses (Bigland-Ritchie et al. 1979; Marsden et al. 1983; Garland et al. 1988; Binder-Macleod et al. 1998), these studies have often ignored the effect of either the differences in initial peak force or stimulation intensities on muscle fatigue (Binder-Macleod et al. 1995; Russ et al. 2002b). Russ and colleagues (Russ et al. 2002c) recently showed that increasing the frequency or number of pulses did not affect the amount of muscle fatigue produced during repetitive isometric contractions if the initial force produced by the stimulation trains was controlled. Another study showed that intermittent high-frequency stimulation produced less fatigue than low-frequency repetitive stimulation in able-bodied and spinal cord injured subjects (Matsunaga et al. 1999). Thus, previous literature does not provide conclusive evidence about the isolated effect of stimulation frequency on muscle fatigue.
Only a few studies have investigated the relationship between stimulation intensity and muscle fatigue. Binder-Macleod et al. (1995) tested the rate and amount of fatigue during repetitive stimulation of the human quadriceps muscle with trains at stimulation amplitudes that produced 20, 50 and 80% maximum voluntary isometric contraction (MVIC) forces, and found less decline in force of the fatiguing trains during repetitive stimulation at higher compared to lower stimulation amplitudes. In contrast, Godfrey et al. (2002) recently showed greater declines in force due to fatigue at high (supramaximal) compared to low (submaximal) stimulation intensities. Thus, we also do not know which stimulation intensity levels can help to minimize fatigue when used for repetitive stimulation during FES.
Since the stimulation frequency (Bigland-Ritchie et al. 1979; Marsden et al. 1983; Garland et al. 1988; Binder-Macleod et al. 1998), intensity (Binder-Macleod et al. 1995; Godfrey et al. 2002) and force generated in response to electrical stimulation (Russ et al. 2002a,b) can affect the amount of muscle fatigue produced during repetitive stimulation, it is difficult to isolate the effects of stimulation frequency versus intensity on muscle fatigue while controlling for the force generated in response to electrical stimulation. For FES applications, however, because the targeted force is determined by the task requirements, it may not be important to isolate the effects of frequency versus intensity on muscle fatigue and performance, but to determine the combination of frequency and intensity that can generate the targeted muscle force while simultaneously minimizing muscle fatigue. It has been hypothesized, but not systematically tested, that the combination of the lowest frequency and highest intensity may minimize fatigue when used for repetitive stimulation (Binder-Macleod & Snyder-Mackler, 1993). No previous study has attempted systematically to investigate the combination of stimulation frequency and intensity that can minimize fatigue while producing a targeted force level during repetitive stimulation.
The purpose of this study was to determine which combination of stimulation intensity and frequency produces the least decline in force during repetitive electrical stimulation, for the same initial peak force. Both the amplitude and the duration of the stimulus pulses can be varied to modulate the stimulation intensity during electrical stimulation. For this study, we used stimulus pulse duration (PD) to vary the intensity because it was easier to control and provided a more consistent force response from the muscle compared to stimulation amplitude (Grill & Mortimer, 1996). Specifically, we compared the percentage decline in quadriceps femoris isometric muscle force produced during repetitive stimulation with trains consisting of three different combinations of stimulation frequencies and pulse durations that produced the same initial targeted peak force, as follows: protocol 1 used trains with 600 µs pulse duration (long pulse duration), and the frequency was varied for each subject to generate the targeted force (low frequency); protocol 2 used 30 Hz trains (medium frequency), and the pulse duration was varied for each subject to generate the targeted force (medium pulse duration); and protocol 3 used 60 Hz trains (high frequency) and the pulse duration was varied for each subject to generate the targeted force (short pulse duration). Please note that the terms ‘medium pulse duration’ and ‘short pulse duration’ were operational definitions for the pulse durations used to generate the targeted force using 30 and 60 Hz trains for protocols 2 and 3, respectively. In addition, the frequency and pulse duration used during protocol 2 were similar to the parameters commonly used in clinical FES systems (Taylor et al. 1999; Donaldson et al. 2000; Johnston et al. 2005).
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Methods |
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Twelve healthy individuals (6 males and 6 females) aged 22–30 years participated in the study. The subjects had no history of lower extremity orthopaedic, neurological or vascular problems. The subjects were requested to refrain from strenuous exercise for at least 48 h before the testing sessions. The subjects signed informed consent forms approved by the Human Subjects Review Board of the University of Delaware. The study was performed according to the Declaration of Helsinki.
Apparatus and set-up
The subjects were seated on an electromechanical force dynamometer (KinCom III 500-11, Chattecx Corp., Chattanooga, TN, USA) with the back supported, hips flexed approximately to 75 degrees and knees flexed at 90 deg (Fig. 1). Velcro straps were used to stabilize the subjects' upper trunk, waist and thigh. Each subject's ankle was stabilized with a strap placed approximately 5 cm proximal to the lateral malleolus. The isometric force output of the quadriceps femoris muscle was recorded via a force transducer placed against the anterior aspect of the lower leg, 5 cm proximal to the lateral malleolus. The subjects could see a representation of the force recorded by the KinCom force transducer on a display screen.
Electrical stimulation was delivered via two self-adhesive surface electrodes (Versa-Stim, 76 mm x 127 mm, CONMED Corp., New York, NY, USA). The proximal electrode was placed over the upper thigh, covering the proximal portion of the rectus femoris and vastus lateralis muscles. The distal electrode was placed over the lower aspect of the thigh, covering the vastus medialis and distal portion of the rectus femoris. The same experimenter placed electrodes across sessions, and care was taken to maintain consistency in electrode placement. A Grass S8800 stimulator (Grass Instrument Co., Quincy, MA, USA) with a SIU8T stimulus isolation unit was used to deliver the electrical stimulation. A personal computer equipped with a PCI-6024E data acquisition board and a PCI-6602 counter-timer board was used. A custom-made switch was connected in series with the stimulator to control the pulse duration. A custom-written LabVIEW program was used for data acquisition, and to control the timing and the duration of the pulses.
Experimental procedure
Each subject participated in four sessions, with a minimum of 48 h separating consecutive sessions. At the start of the first session, subjects received an overview of the testing procedures, signed the informed consent form, and were trained to perform the MVIC test (Fig. 2). They were seated on the KinCom, surface electrodes were attached to the skin of the subjects' thigh and tested for appropriate placement. Next, the MVIC force was recorded using the burst superimposition technique (Snyder-Mackler et al. 1994). During the MVIC test, the subjects attempted to produce as much knee extension force as possible. During the maximal voluntary contraction, an electrical stimulation train (amplitude, 130 V; frequency, 100 Hz; pulse duration, 600 µs) was delivered to the quadriceps femoris muscle. This stimulation train or ‘burst’ was superimposed on the volitional contraction to ensure that the subjects were truly generating maximal force. If the electrical stimulation train increased the force by 
10%, the subject's MVIC was recorded. If the electrical stimulation train increased the subject's force output by > 10%, the MVIC test was repeated after a 10 min rest. If the subject failed to elicit a true MVIC within three repetitions, they were not tested on that day. For each subject, the MVIC value measured during the first session was used to set the stimulation amplitude for all four sessions.
The remaining three sessions involved fatigue testing. The order of testing of the three fatigue protocols was randomized across subjects. Only one protocol was tested on each day. Each testing session consisted of ‘fatiguing trains’ and pre- and postfatigue ‘testing trains’. The ‘fatiguing trains’, consisting of stimulation trains of three different combinations of frequency and pulse duration repetitively delivered at a rate of one train every second, were used to fatigue the muscle and to assess the muscle's performance during the fatigue test. The ‘testing trains’, consisting of stimulation trains of 60 and 20 Hz frequency at two different pulse durations, were delivered before (prefatigue) and after (postfatigue) the fatiguing trains. The testing trains measured the decline in the force-generating ability of the muscle. All fatiguing and testing trains were 300 ms long. The duty cycles used to fatigue the muscles (300 ms long trains with 700 ms rest time) were similar to the activation patterns recorded in the quadriceps muscle during normal walking (Pierrynowski & Morrison, 1985). Owing to differences in frequencies between the trains used for testing, however, the fatiguing trains for each of the three protocols contained different numbers of pulses.
The following procedures were followed during the three fatigue sessions (Fig. 2):
Set stimulation amplitude to generate 50% MVIC peak force. During each testing session, after applying the electrodes, the stimulation amplitude was set to produce 50% of the subject's MVIC force using 300 ms long, 60 Hz trains with 600 µs pulse duration. The 50% MVIC amplitude was used because it allowed a range of frequencies and pulse durations to be used to generate the target force of 20% MVIC.
Potentiation. Eleven trains (770 ms train duration, 14 Hz frequency, 600 µs pulse duration) were delivered with a 5 s rest time between trains to potentiate the muscle (Binder-Macleod et al. 2002).
Set frequency and pulse duration to generate 20% MVIC target peak force.
Either the stimulation pulse duration or frequency of a 300 ms long train was varied to generate peak force equal to 20% of the subject's MVIC. The first train of each fatigue protocol generated 
20% MVIC peak force.
Potentiation. Potentiation was repeated before the fatigue test to prevent the effects of potentiation from interacting with fatigue (Binder-Macleod et al. 2002).
Prefatigue testing trains. Sixty and 20 Hz trains were delivered at the same pulse duration as that used for the fatiguing trains for that session and also at 600 µs pulse duration. The prefatigue testing trains were delivered with a rest time of 10 s.
Fatiguing trains. After the potentiation and prefatigue testing trains had been delivered, 176 fatiguing trains were delivered at a rate of one train every second (train duration, 300 ms; rest time, 700 ms). Three different combinations of frequency and pulse duration were used during the three different fatigue protocols, as follows:
Protocol 1: Long pulse duration (600 µs) and low frequency. The pulse duration of a 300 ms long train was fixed at 600 µs, and the frequency was set to produce 20% MVIC peak force.
Protocol 2: Medium frequency (30 Hz) and medium pulse duration. The frequency of a 300 ms long train was fixed at 30 Hz, and the pulse duration was set to produce 20% MVIC peak force.
Protocol 3: High frequency (60 Hz) and short pulse duration. The frequency of a 300 ms long train was fixed at 60 Hz, and the pulse duration was set to produce 20% MVIC peak force.
Postfatigue testing trains. At the end of the fatiguing trains, postfatigue testing trains were delivered in the same order as the prefatigue testing trains at a rate of one train every second to maintain the state of muscle fatigue.
Data analyses
The decline in force generated in response to the fatiguing trains for each protocol was used as a measure of the ‘muscle's performance’ or the muscle's ability to maintain force output in response to the fatiguing trains. The percentage declines in peak force between the first and last fatiguing train were calculated for each fatigue protocol. Since muscle fatigue was the primary focus of our study, it was important to define muscle fatigue in the context of this study. Muscle fatigue is a decline in the force-generating ability of the muscle as a result of recent activity (Edwards, 1981; Vollestad, 1997). We used the percentage decline in peak force between pre- and postfatigue 60 Hz testing trains as a measure of the decline in the force-generating ability (Vollestad, 1997). The decline in peak force of the 60 Hz testing trains at the same pulse duration as the fatiguing trains provided a measure of the amount of muscle fatigue produced in the population of motor units recruited by the fatiguing trains during each fatiguing protocol. The decline in peak force of the 60 Hz testing trains at the 600 µs pulse duration provided a measure of the muscle fatigue produced within a comparable number of motor units as were recruited during the protocol that used the longest pulse duration (i.e. protocol 1). In addition, the ratio of peak forces produced in response to 20 versus 60 Hz testing trains (20 Hz:60 Hz peak force ratio) was used as a measure of low-frequency fatigue (Vollestad, 1997; Russ & Binder-Macleod, 1999). The 20 Hz:60 Hz peak force ratios were calculated at the beginning (prefatigue) and end (postfatigue) of the fatigue protocols both for testing trains at the pulse duration of the fatiguing trains and at the 600 µs pulse duration.
Statistical analyses
The percentage decline in peak forces from the first to last fatiguing trains, percentage decline in peak force between pre- and postfatigue 60 Hz testing trains at the pulse duration of the fatiguing trains, and the percentage decline in 60 Hz testing trains at 600 µs pulse duration were compared using one-way repeated measures ANOVAs. Pairwise post hoc comparisons using the least squared difference (LSD) were performed only if the ANOVA showed significant differences. The pre- and postfatigue 20 Hz:60 Hz peak force ratios for the three fatigue protocols were compared using two-way (protocol x fatigue) repeated measures ANOVAs. In addition, peak forces produced in response to the first fatiguing train of each protocol were compared using a repeated-measures one-way ANOVA to determine whether the fatigue protocols produced similar initial peak forces. The significance level was set at P = 0.05.
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Results |
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Force responses to the fatiguing trains
There were significant differences in percentage decline in peak force (F = 30.08; P < 0.01) between the first and last fatiguing trains among the three protocols (Fig. 4). Protocol 1, consisting of fatiguing trains with long (600 µs) pulse duration and low frequency, produced the smallest percentage decline in peak force (31.3 ± 9.4%), and protocol 3, consisting of fatiguing trains with high frequency (60 Hz) and short pulse duration, produced the largest percentage decline in peak force (51.3 ± 7.5%; Fig. 4).
Force responses of testing trains
Average peak forces produced in response to the 60 Hz testing trains at the same pulse duration as the fatiguing trains for protocols 1, 2 and 3, respectively, were 481.5 ± 164.2, 238.7 ± 69.2 and 221.1 ± 78.6 N (prefatigue) and 367.5 ± 102.8, 170.4 ± 44.3 and 117.1 ± 36.8 N (postfatigue). Protocol 1 produced the smallest decline in peak force (21.5 ± 9.5%), protocol 2 produced an intermediate decline (27.4 ± 8.2%), and protocol 3 produced the largest decline (46.1 ± 6.7%) in peak force in response to the 60 Hz testing train at the same pulse duration as the fatiguing trains (F = 77.23; P < 0.01; Fig. 5). Average peak forces produced in response to the 60 Hz testing trains at the 600 µs pulse duration for protocols 1, 2 and 3, respectively, were 486.6 ± 160.9, 491.7 ± 142.4 and 489.2 ± 151.8 N (prefatigue) and 362.6 ± 101.4, 416.4 ± 112.0 and 376.3 ± 114.1 N (postfatigue). Interestingly, for the 60 Hz testing trains at 600 µs pulse duration, protocol 2, consisting of medium frequency and medium pulse duration fatiguing trains, produced significantly smaller declines in peak force (14.7 ± 7%) than protocol 1 (23.6 ± 8.3%) or protocol 3 (22.4 ± 10.3%; F = 6.40; P = 0.01; Fig. 5).
Average peak forces produced in response to the 20 Hz testing trains at the pulse duration of the fatiguing trains for protocols 1, 2 and 3, respectively, were 363.2 ± 117.7, 175.0 ± 55.1 and 162.6 ± 53.9 N (prefatigue) and 224.7 ± 68.4, 73.6 ± 24.7 and 41.9 ± 17.1 N (postfatigue). Average peak forces produced in response to the 20 Hz testing trains at the 600 µs pulse duration for protocols 1, 2 and 3, respectively, were 366.2 ± 116.5, 375.7 ± 111.5 and 362.6 ± 110.1 N (prefatigue) and 221.4 ± 68.9, 253.0 ± 72.6 and 230.9 ± 70.3 N (postfatigue). For testing trains at the pulse duration of the fatiguing trains, the two-way repeated measures ANOVA (protocol x fatigue) showed significant effects of protocol (F = 32.00; P < 0.01) and fatigue (F = 308.93; P < 0.01) on the 20 Hz:60 Hz peak force ratios (Fig. 6A). There was a significant interaction between protocol and fatigue (F = 35.32; P < 0.01). There were no significant differences in the prefatigue 20 Hz:60 Hz peak force ratios among the three protocols. The postfatigue 20 Hz:60 Hz peak force ratios showed significant differences among protocols (F = 50.7; P < 0.01). For testing trains at the pulse duration of the fatiguing trains, protocol 1 showed the largest postfatigue 20 Hz:60 Hz ratio (0.61 ± 0.07), and protocol 3 showed the smallest ratio (0.37 ± 0.11; Fig. 6A). For testing trains at 600 µs pulse duration, the two-way ANOVA showed a significant effect of fatigue (F = 66.95; P < 0.01), no significant effect of protocol (F = 0.03; n.s.), and no significant interaction between the effects of protocol and fatigue (F = 2.62; n.s.; Fig. 6B).
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Discussion |
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Recently, Godfrey et al. (2002) studied the effects of stimulation intensity on force production of thenar hand muscles in patients with spinal cord injury. In contrast to our present findings, Godfrey et al. (2002) found greater fatigue during stimulation at supra- compared to submaximal intensities. We believe that the differences in the findings of Godfrey et al. (2002) versus our present study resulted from methodological differences. Since Godfrey et al. (2002) delivered both supra- and submaximal stimulation intensities at the same frequency (40 Hz), different force levels were generated at the two intensities. The higher forces generated at supra- versus submaximal intensities probably contributed to the greater muscle fatigue observed by Godfrey et al. (2002) at the supramaximal intensities (Russ et al. 2002b,c). However, the differences between the results of our present study and those of Godfrey et al. (2002) may also result from differences in the subject populations and the muscle tested.
Protocol 1 also produced the least low-frequency fatigue in the motor units recruited by the fatiguing trains (Fig. 6A). Low-frequency fatigue is the result of impairment in excitation–contraction coupling that is thought to result from increased levels of intracellular Ca2+ during muscle activation (Westerblad et al. 1993; Chin & Allen, 1996; Chin et al. 1997). Intracellular Ca2+ concentrations have been shown to be directly related to the stimulation frequency (Chin & Allen, 1996). The low frequency used during protocol 1 would therefore result in the lowest levels of intracellular Ca2+ and the least low-frequency fatigue among the three protocols (Westerblad et al. 1993; Chin & Allen, 1996; Chin et al. 1997).
In contrast to our present findings, Matsunaga et al. (1999) showed smaller declines in force during repetitive stimulation at high- (100 Hz) versus low-frequency (20 Hz) activation. Compared to our study, the fatigue protocols tested by Matsunaga et al. (1999) were of much longer durations (60 min versus 180 s in our study), used much shorter duty cycles (1:15, 1:30 and 1:60 versus 1:2.3 in our study), and produced smaller percentage declines in peak force (22.3 ± 15.1% at 100 Hz versus 51.3 ± 7.5% at 60 Hz in our study). Since muscle performance is a function of the extent of force fatigue and low-frequency fatigue produced by the fatiguing trains in the motor unit population recruited by the fatiguing trains, we believe that the results of Matsunaga et al. (1999) can be explained by greater low-frequency fatigue and less muscle fatigue than presently observed. That is, even if greater muscle fatigue was produced by the 100 Hz trains than the 20 Hz trains in their study (Matsunaga et al. 1999), low-frequency fatigue may have markedly reduced the muscles' responses to the 20 Hz trains and therefore resulted in poorer performance in response to the 20 Hz trains.
The frequencies used during protocols 1, 2 and 3 in our study were on the low, middle and high ranges of the force–frequency curves, respectively. Surprisingly, however, the average pulse durations used during protocols 2 (150 ± 22 µs) and 3 (131 ± 24 µs), although significantly different, only varied by 19 µs. A possible reason could be that the pulse durations used for protocols 2 and 3 were in the steep rising part of the force versus pulse durations curves. Thus, our results showed that although the difference in frequencies between protocols 2 and 3 was relatively large (30 versus 60 Hz), a relatively small difference in pulse duration between protocol 3 and protocol 2 enabled the targeted 20% MVIC force to be reached for both the protocols.
The present findings could have implications for the development of strategies for optimal activation of skeletal muscle during FES. Functional electrical stimulation is used to generate functional movements in patients with upper motor neurone lesions, such as spinal cord injury, hemiplegia following stroke, and cerebral palsy. This study represents the first step in a project whose long-term aim is to develop electrical stimulation strategies that can maximize FES performance. Initial testing on healthy individuals has helped us to identify hypotheses that can then be tested on paralysed muscles using fewer experimental sessions. Interestingly, consistent with out present findings, recent studies showed that for healthy subjects and for subjects with spinal cord injury, starting at low frequencies and later switching to high frequencies produced better performance during repetitive non-isometric contractions than stimulation using either a low or high frequency alone (Kebaetse & Binder-Macleod, 2004; Kebaetse et al. 2005). Starting repetitive stimulation with low frequencies produced less muscle fatigue, and switching to a higher stimulation frequency allowed the stimulation to overcome the effects of low-frequency fatigue (Kebaetse & Binder-Macleod, 2004; Kebaetse et al. 2005). Future studies will need to identify the best frequency and intensity of the initial trains, as well as the strategies for modulation of frequency and intensity of the subsequent trains, to maximize muscle performance during FES.
An interesting finding of this study was the difference in the responses to the testing trains when the pulse duration was maintained at the levels used to fatigue the muscle versus when a 600 µs pulse duration was used (see Figs 5 and 6). During protocols 2 and 3, the postfatigue testing trains at 600 µs pulse duration activated previously unrecruited motor units. The responses to the testing trains at 600 µs pulse duration were therefore the sum of the forces produced by the recruited and previously unrecruited motor units. Protocol 3 showed the most and protocol 1 the least muscle fatigue and low-frequency fatigue when the pulse duration was maintained at the level used to fatigue the muscle (Fig. 5). Thus, during FES applications, if the frequency and pulse duration are held constant during repetitive stimulation, using the lowest frequency and longest pulse duration may maximize performance. However, Protocols 3 and 1 showed comparable amounts of muscle fatigue and protocol 2 showed the least muscle fatigue when tested at the 600 µs pulse duration (Fig. 5). In addition, in response to testing trains at 600 µs pulse duration, there were no differences in the overall levels of low-frequency fatigue among the three protocols (Fig. 6B). This is an important finding because most FES systems used at present deliver a constant frequency and increase the intensity to increase muscle force output as the muscle fatigues (Weingarden et al. 1997; Taylor et al. 1999; Weber et al. 2005). Thus, for FES applications where intensity is increased as the muscle fatigues, a ‘medium’ frequency, similar to the frequency used in protocol 2 of our study, may minimize muscle fatigue. The combination of frequency and pulse duration that minimizes muscle fatigue and/or maximizes performance during FES may depend on whether or not modulation of frequency or intensity will be used as strategies during repetitive stimulation.
Conclusion
The present findings support the hypothesis that when the same initial peak force is generated using different combinations of frequency and pulse duration, and when the frequency and pulse duration are kept constant throughout repetitive stimulation, repetitive stimulation with a long pulse duration (600 µs) and low frequency (11.5 ± 1.2 Hz; protocol 1) would maximize isometric performance by minimizing muscle fatigue. Interestingly, repetitive stimulation with a medium frequency (30 Hz) and medium pulse duration (150 ± 22 µs; protocol 2) produced the least muscle fatigue when comparable motor unit populations were tested across protocols (i.e. at the 600 µs pulse duration). These findings may have important implications for the design of optimal stimulation strategies to use during FES. Specifically, the present results should help in the design of future studies involving patient populations where complex stimulation strategies that modulate both the frequency and pulse durations will be tested.
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