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Abstract

BACKGROUND:

Although the common practice of verbal encouragement is scientifically supported, its effect on the maintenance of force output in fatiguing exertions is unknown.

OBJECTIVE:

To examine the effects of verbal encouragement on exercise-induced quadriceps and knee joint function during three sets of knee extension exercise.

METHODS:

Sixty-five healthy males (23.3 years, 175.8 cm, 75.3 kg) underwent testing using the administration of verbal encouragement ( $n=$ 32) or not ( $n=$ 33) during assessment of quadriceps and knee joint function. Assessments were performed at baseline and times 1, 2, and 3. The knee concentric isokinetic extension at 60 ${}^{\circ}$ /s, was performed between the time points. For quadriceps function, maximal isometric strength and activation (central activation ratio) were recorded. Absolute error values on knee flexion replications at 15 ${}^{\circ}$ or 45 ${}^{\circ}$ were recorded for knee joint function.

RESULTS:

There was no verbal encouragement effect over three sets of exercise in quadriceps strength (condition $\times$ time: $F_{3,189}=$ 1.71, $p=$ 0.17) and knee flexion replication (condition $\times$ time for 15 ${}^{\circ}$ : $F_{3,189}=$ 0.11, $p=$ 0.96; 45 ${}^{\circ}$ : $F_{3,189}=$ 0.63, $p=$ 0.6). However, subjects who had received verbal encouragement maintained quadriceps activation (condition $\times$ time: $F_{3,189}=$ 5.49, $p=$ 0.001). Specifically, quadriceps activation in the verbal condition was 3.0% higher at time 2 ( $p=$ 0.01) and 4.7% higher at time 3 ( $p=$ 0.0003) versus in the non-verbal condition.

CONCLUSIONS:

Verbal encouragement appears to be effective in maintaining central activation, but is insufficient for promoting strength. This supports the idea that peripheral contributing factors play a larger role in force production when performing multiple sets of exercises.

Keywords

Maximal voluntary isokinetic contraction central activation ratio knee joint position sense exercise-induced muscle fatigue

1. Introduction

Muscle fatigue is defined as loss of force-generating capacity or failure to maintain strength during continuous muscle contraction [1]. Depletion of energy sources (e.g., glycogen and phosphocreatine) [2] and/or accumulation of metabolic byproducts (e.g., H ${}^{+}$ and Pi) [3] associated with muscle metabolism are considered to be peripheral contributing factors to this fatigue. In contrast, central fatigue is derived from an altered central motor drive and/or neural communication associated with afferent feedback and voluntary effort [4].

Table 1
Subject demographics (mean $\pm$ 95% CIs)

	Verbal encouragement ( $n=$ 32)	Non-verbal encouragement ( $n=$ 33)	Total ( $n=$ 65)
Age (year)	22.8 (0.8)	23.7 (0.9)	23.3 (0.6)
Height (cm)	176.1 (2.1)	175.6 (1.8)	175.8 (1.4)
Mass (kg)	73.7 (3.9)	73.3 (2.6)	73.5 (2.3)
LEFS (score)	77.9 (1.2)	77.0 (1.2)	77.4 (0.9)

LEFS: lower extremity functional scale.

Providing verbal encouragement is one of the simplest and easiest ways to enhance the outcomes of muscle function. Previous data have consistently shown verbal encouragement is beneficial in regard to peak moment [5, 6] force output [7, 8], or cycling performance [9]. This phenomenon is thought to be from cognitive stimulation delivered to the central nervous system. There is sufficient data to suggest verbal encouragement has a positive outcome on aforementioned muscle [5, 8] and athletic function [7, 9]. However, the contribution of this centrally-driven factor has never been quantified with regard to maintenance of force output.

Muscle fatigue is also well-known to impair joint function, including joint position sense [10, 11, 12]. For instance, muscle fatigue in knee extensors [12] and hip abductors [11] increased the absolute errors in knee (2.5 to 3.5 ${}^{\circ}$ ) and hip (1.3 to 2.0 ${}^{\circ}$ ) joint proprioception, respectively. The proposed causes of this impaired joint proprioception include a reduction in sensitivity [13], an increase in discharge threshold of muscle spindles [11], and a decrease in $\alpha$ - $\gamma$ coactivation [14].

Although the common practice of verbal encouragement is scientifically supported, there is limited objective data supporting this (such as that comparing measurement values before and after fatigue). Though a series of exercises (e.g., three sets in weight-lifting) is typically performed in the athletic field, the existing literature does not guarantee the effectiveness of verbal encouragement after the second set of exercise. Therefore, in this study, we sought to observe subsequent changes in quadriceps (e.g., strength and activation) and knee joint (e.g., replications) functions during three sets of isokinetic knee extension exercises with manipulation of verbal encouragement. We expected that, compared with the non-verbal condition, quadriceps strength and activation would be maintained with verbal encouragement. We further hypothesised that subjects in both conditions would show a similar reduction pattern in knee joint function.

2. Methods

2.1 Participants

Sixty-five healthy male college students (verbal encouragement: $n=$ 32; non-verbal encouragement: $n=$ 33) took part in this study. Their personal traits appear in Table 1. Individuals were excluded if they had any orthopedic injuries in the past six months or had a history of back or lower extremity surgery. Since fatigue adaptation and management were recognised as potential confounders, individuals who exercised on a regular basis (at least twice per week) were also excluded. Prior to data collection, we obtained informed consent approved by the Kyung Hee University’s institutional revierw board (approval nmber KHSIRB 2015-010 dated 19/06/2015) which also approved the testing procedures. Participants also completed a functional outcome questionnaire to confirm normal function of the lower extremity (lower-extremity functional scale; LEFS) [15]. Individuals were included if they scored $>$ 78 of 80 points on LEFS [16].

2.2 Study design

The independent variables were condition (verbal and non-verbal) and time (baseline and times 1 through 3). The dependent variables were quadriceps strength (maximal voluntary isometric contraction; MVIC) and activation (central activation ratio; CAR), and replication of knee joint angle. Each subject experienced only one of the conditions, and the order of conditions was randomised with the random allocation function from a spreadsheet program (Excel; Microsoft Corp., Redmond, WA, USA).

2.3 Testing procedures

Upon completion of the informed consent and the LEFS, participants performed 10 minutes of warm-up cycling on a stationary bike at a self-selected pace (Fig. 1). Participants were then seated on a dynamometer (Cybex 770; Cybex Inc., Medway, MA, USA) for baseline measurements. Participant’s anterior thighs were shaved (if necessary) and cleaned with isopropyl alcohol prior to electrode placement. Two self-adhesive electrodes (Dura-Stick II; 7 $\times$ 12.7 cm; Chattanooga, Hixson, TN, USA) were attached over the proximal rectus femoris and the vastus medialis.

Figure 1.

Testing procedure. Regardless of the condition, verbal encouragement was given during baseline measurements and knee extension exercises (exercises 1 to 3). Visual feedback was not provided for either condition at any time point. Participants in the verbal encouragement condition received verbal encouragement during quadriceps strength training at times 1, 2, and 3. For knee joint function, replications of two knee joint positions (15 ${}^{\circ}$ and 45 ${}^{\circ}$ ) were randomly assessed at each time point. For quadriceps function, MVIC was recorded, and CAR was calculated based on MVIC. To avoid a potential influence from quadriceps fatigue, knee joint function was assessed prior to quadriceps function at baseline.

Baseline measurements were recorded first for the knee joint followed by quadriceps function (Fig. 1). Participants were blindfold during assessment of knee flexion replications. While participants sat on the dynamometer with their dominant hip locked at 85 ${}^{\circ}$ and knee at 90 ${}^{\circ}$ (set position), an assessor passively positioned their knees at target angles of 15 ${}^{\circ}$ and 45 ${}^{\circ}$ . Participants were allowed to sit in this position for a three-second holding time to remember the angles [17]. Three trials were randomly assessed at each angle, separated with five-second rest intervals. Absolute error values (deviation from the target angles in degrees) were then calculated and averaged to represent knee joint function alterations at each time point. Quadriceps strength and activation were tested in the same position as the knee joint replication test but with the knee locked at 90 ${}^{\circ}$ . Participants were asked to produce a quadriceps MVIC. When a subject’s quadriceps moment curve was maximised, and a plateau was seen for longer than one second, an exogenous supramaximal electrical stimulus was manually delivered to the quadriceps via the electrodes using a superimposed burst (SIB) technique. We used the S88 Grass Stimulator with the SIU8T transformer isolation unit (Grass-Telefactor, West Warwick, RI, USA) to generate the electrical stimuli (100 pps, 600 $\mu$ s pulse duration, 10 trains in 100 milliseconds in duration, and 125 volts with peak output current of 450 mA). Quadriceps activation (CAR) was calculated by dividing the MVIC value by the superimposed burst value (CAR $=$ MVIC moment/SIB moment) [18]. Three trials of quadriceps strength (activation values) were recorded, with 60-second rest intervals in between. Quadriceps strength values were normalized by body mass (N $\cdot$ m/kg). For baseline measurements of quadriceps function, all participants in both conditions received verbal encouragement (“kick as hard as you can!” and “kick! kick! harder! harder!”). Visual feedback (looking at a force trace in the computer screen) was not provided for any quadriceps strength and activation measurements at any time point.

To induce quadriceps fatigue, participants were asked to perform continuous isokinetic knee extensions (60 ${}^{\circ}$ /s) on the same isokinetic dynamometer. When three consecutive moment values were $<$ 50% of the peak moment recorded at baseline [19], participants stopped the contractions (and therefore finished the exercise set). Three sets of knee extension exercises were performed, with rest intervals of 30 seconds between them. Participants in both conditions received verbal encouragement.

While participants were performing the first set of exercises, an opaque sealed envelope was opened to determine the condition. After each set of knee extension exercises, the same measurements as at baseline were recorded at times 1, 2, and 3. Quadriceps function was evaluated first, followed by knee joint function. Each dependent measurement was recorded only once during each 30-second rest interval between sets (Fig. 1). When assessing quadriceps strength and activation, verbal encouragement was provided for the verbal condition group. Verbal encouragement was provided by the two researchers (HL: $>$ 90% of participants; JS: $<$ 10% of the time) with a consistent loudness level (97.1 $\pm$ 2.0 dB). This verbal encouragement included the same words that were said at baseline and during the quadriceps exercise. Regardless of the condition, no verbal encouragement was provided during the knee replication tests.

Table 2

Changes in quadriceps function (mean $\pm$ 95% CIs)

	Strength (N $\cdot$ m/kg)		Activation (central activation ratio)
	Verbal encouragement	Non-verbal encouragement	Verbal encouragement		Non-verbal encouragement
Baseline	2.96 (0.66)	3.00 (0.63)	0.941	(0.014)	0.933	(0.012)
Time 1	2.24 (0.57) ${}^{*}$	2.17 (0.52) ${}^{*}$	0.934	(0.018)	0.909	(0.022) ${}^{**}$
Time 2	2.14 (0.53) ${}^{*}$	2.06 (0.46) ${}^{*}$	0.915	(0.019) ${}^{\dagger}$	0.879	(0.021) ${}^{{\#}\S}$
Time 3	2.11 (0.53) ${}^{*}$	1.98 (0.48) ${}^{*}$	0.906	(0.019) ${}^{{\dagger}{\ddagger}}$	0.855	(0.026) ${}^{{\#}\S}$

There was no condition $\times$ time interaction for strength ( $F_{3,189}=$ 1.71, $p=$ 0.17). ${}^{*}$ Regardless of condition, quadriceps strength was reduced at time 1 (time main effect: $F_{3,189}=$ 280.79, $p<$ 0.0001). There was a condition $\times$ time interaction for activation ( $F_{3,189}=$ 5.15, $p=$ 0.002). ${}^{{\dagger}}$ Different from the baseline values in the verbal encouragement condition ( $p<$ 0.04). ${}^{{\ddagger}}$ Different from the time 1 values in the verbal encouragement condition ( $p=$ 0.02). ${}^{**}$ Different from the values at time 2 ( $p=$ 0.006) and 3 ( $p<$ 0.0001) in the non-verbal encouragement condition. ${}^{\#}$ Different from the time 1 values in the non-verbal encouragement condition ( $p<$ 0.006). ${}^{\S}$ Different from the baseline values in the non-verbal encouragement condition ( $p<$ 0.0001).

2.4 Statistical analyses

We performed an a priori power analysis based on previous research to calculate the sample size. We determined an expected mean difference in the MVIC of 0.44 N $\cdot$ m/kg with a standard deviation of 0.6 N $\cdot$ m/kg. These values yielded an effect size of 0.73 [20]. We used an alpha of 0.05 and a beta of 0.2. These calculations estimated that 16 participants would be necessary in each condition.

Mean and SD values were calculated from each measurement at each time point. To test the effects of verbal encouragement over time, we performed a 2 $\times$ 4 mixed model analysis of variance (ANOVAs) for quadriceps and knee joint function. Tukey-Kramer post-hoc tests were used for pairwise comparisons (R 3.4.3; R development core team, $p<$ 0.05 for all tests). We also calculated Cohen’s d effect size (ES $=$ $[\bar{X}_{1}-\bar{X}_{2}]/\sigma_{\text{pooled}}$ ) [21].

3. Results

3.1 Quadriceps function

There was no verbal encouragement effect over three sets of exercise (condition $\times$ time: $F_{3,189}=$ 1.71, $p=$ 0.17; condition effect: $F_{1,189}=$ 0.22, $p=$ 0.64; Table 2). Regardless of condition (time main effect: $F_{3,189}=$ 280.79, $p<$ 0.0001), quadriceps strength was reduced at time 1 (26%, $p<$ 0.0001, ES $=$ 1.31) and reduced again at time 2 (5%, $p=$ 0.03, ES $=$ 0.2). The total amount of quadriceps strength loss (from baseline to time 3) was 29% (ES $=$ 1.42) in the verbal condition and 31% (ES $=$ 1.82) in the non-verbal condition (Fig. 2).

Figure 2.

Change in quadriceps strength (N $\cdot$ m/kg) displayed as percentage change from baseline (upper and lower limits of the 95% CIs).

There was verbal encouragement effect on quadriceps activation (condition $\times$ time: $F_{3,189}=$ 5.15, $p=$ 0.02). Participants who received verbal encouragement maintained quadriceps activation at time 1 (0.7% reduction from baseline, $p=$ 0.99), and then showed a 2.8% reduction at time 2 ( $p=$ 0.04, ES $=$ 0.44) and a 3.7% reduction at time 3 ( $p=$ 0.001, ES $=$ 0.59). In contrast, in the non-verbal condition, a 2.6% ( $p=$ 0.6, ES $=$ 0.39), a 5.8% ( $p<$ 0.0001, ES $=$ 0.98), and a 8.4% ( $p<$ 0.0001, ES $=$ 1.11) reduction was observed at times 1, 2, and 3, respectively (Fig. 3).

Figure 3.

Change in quadriceps activation (CAR) displayed as percentage change from baseline (upper and lower limits of the 95% CIs).

Table 3

Changes in knee joint function (mean $\pm$ 95% CIs)

	Replications at 15 ${}^{\circ}$		Replications at 45 ${}^{\circ}$
	Verbal encouragement	Non-verbal encouragement	Verbal encouragement	Non-verbal encouragement
Baseline	8.84 (5.62)	6.66 (4.60)	5.97 (3.64)	6.15 (3.52)
Time 1	11.19 (8.20) ${}^{*}$	9.12 (6.69) ${}^{*}$	7.34 (6.07) ${}^{*}$	9.18 (6.60) ${}^{*}$
Time 2	10.97 (7.61)	9.39 (7.20)	10.97 (7.61)	9.39 (7.20)
Time 3	12.41 (8.40)	10.82 (7.21)	12.41 (8.40)	10.82 (7.21)

There was no condition $\times$ time interaction (15 ${}^{\circ}$ : $F_{3,189}=$ 0.11, $p=$ 0.96; 45 ${}^{\circ}$ : $F_{3,189}=$ 0.63, $p=$ 0.60). ${}^{*}$ Regardless of condition, absolute errors in knee joint angle replications at 15 ${}^{\circ}$ ( $F_{3,189}=$ 10.66, $p<$ 0.0001) and 45 ${}^{\circ}$ ( $F_{3,189}=$ 5.78, $p=$ 0.0008) increased after the first set of exercise (15 ${}^{\circ}$ : $p=$ 0.004; 45 ${}^{\circ}$ : $p=$ 0.004).

During three sets of exercise, (condition effect: $F_{1,189}=$ 6.00, $p=$ 0.02), participants who received verbal encouragement performed with a 33% higher quadriceps activation (0.92 vs. 0.89 in CAR: ES $=$ 1.12). Regardless of condition (time effect: $F_{3,189}=$ 38.51, $p<$ 0.0001), there was a decrease in central activation after the first set of knee extension exercises. Specifically, there was a 1.7% ( $p=$ 0.04, ES $=$ 0.31), 4.3% ( $p<$ 0.0001, ES $=$ 0.79), and 6.0% ( $p<$ 0.0001, ES $=$ 0.99) decrease at times 1, 2, and 3, respectively.

3.2 Knee joint function

The ability to perform knee joint replication did not change for either 15 ${}^{\circ}$ (condition $\times$ time: $F_{3,189}=$ 0.11, $p=$ 0.96; Fig. 3) or 45 ${}^{\circ}$ (condition $\times$ time: $F_{3,189}=$ 0.63, $p=$ 0.60; Table 3). Regardless of condition (time effect), joint angle replications of 15 ${}^{\circ}$ ( $F_{3,189}=$ 10.66, $p<$ 0.0001) and 45 ${}^{\circ}$ ( $F_{3,189}=$ 5.78, $p=$ 0.0008) were altered after the first set of exercise (15 ${}^{\circ}$ : $p=$ 0.004, ES $=$ 0.38; 45 ${}^{\circ}$ : $p=$ 0.004, ES $=$ 0.43; Table 3). However, there were no further alterations thereafter ( $p>$ 0.16 for all tests; Table 3).

4. Discussion

The two main objectives of the present study were (1) to explore the effects of verbal encouragement on fatigued quadriceps strength and activation during three sets of quadriceps exercises and (2) to evaluate the relationship between magnitude of quadriceps dysfunction and kinesthetic function at the knee joint. We observed that the patterns of reduction in strength and joint proprioception in the two conditions were very similar, indicating that our verbal encouragement did not appear to be effective on quadriceps force output during the three sets of exercise. Interestingly, however, quadriceps central activation was maintained in participants who received verbal encouragement. In contrast, quadriceps central activation gradually decreased in participants in the nonverbal condition. The difference between the two conditions after the third set (at time 3) was 0.051 in CAR (ES $=$ 0.76). These results suggest that, although verbal encouragement had little effect on force production, it was effective in delaying centrally mediated fatigue.

While the changes in force output were almost identical for the two conditions, the reduction rate for central activation was more than twofold greater in participants in the non-verbal condition (e.g., 8.4% vs. 3.7% in the verbal condition at time 3). This could in part be explained by monoamine neurotransmitter activity and afferent feedback. In particular, there may have been an accumulation of serotonin and/or a decrease in dopamine concentration [22] in the non-verbal condition participants. In addition facilitation of groups III and IV afferents from the quadriceps may have suppressed the neural commands [22]. Regardless we assume that accumulation of metabolic byproducts [23] depletion of substrates [24] insufficiency in oxygen delivery [25] and deviation in muscle contractile properties [26] were similar in the verbal and non-verbal conditions. According to the previously discussed neurophysiological mechanisms, we speculate that verbal encouragement was effective at preventing central fatigue, maintaining subject willingness to perform and focus, and at enhancing the neural drive for maximal force. However, the preserved central activation (due to verbal encouragement) did not linearly influence the last stage of force production. A previous report [27] suggested central activation failure and intramuscular disturbance were responsible for approximately 20% and 80% of the total amount of muscle fatigue, respectively. This may explain why force output was not influenced by verbal encouragement despite its effects on central activation. Therefore, we suspect peripheral mechanisms (e.g. increased H ${}^{+}$ and accumulation of metabolic byproducts) play a larger role than central mechanisms with accumulated muscle fatigue. In addition, verbal encouragement may not be effective (especially after the second set of exercise). Therefore an intervention at the peripheral level may be required to sustain performance when one is completing multiple sets of exercise.

Alterations in joint position sense are a common consequence of exercise-induced strength reduction [12, 28, 29]. No prior study evaluated changes in knee joint proprioception during multiple sets of exercise. Therefore, we were interested in studying the ability to perform joint replications during multiple sets of fatiguing exercise. The acuity of joint replications at both angles was reduced after the first set, but there were no further alterations in joint function thereafter. Verbal encouragement provided during quadriceps contractions did not seem to affect our results. These results suggest joint function is more related to rate of strength changes than it is to central activation. Following strength reduction, altered afferent sensory input from mechanoreceptors [30], nociceptors [31] and proprioceptors [12] is thought to cause a reduction in conscious knee joint awareness. Since central activation indicates the ratio in the amount of neural drive from the cerebral cortex and the force output [32], it is possible central activation also plays a role in acuity of joint replications. There was no further decrease in quadriceps strength or knee joint function after the first set of exercise. We do not know if these two variables are directly related to one another, especially when muscle fatigue accumulated. Since an improvement of joint position sense with strength development was previously observed [33], future studies are needed to investigate the correlation between the two factors.

Several issues deserve further elaboration regarding the testing procedures and measurements. Muscle fatigue was induced by concentric quadriceps isokinetic contractions at 60 ${}^{\circ}$ /s. This exercise was continued until three consecutive moment values $<$ 50% of the baseline value were observed. This method to define muscle fatigue (including half of the maximal moment as a cutoff value) was used in previous studies [19, 34, 35]. This protocol allowed each participant to perform different numbers of repetitions to reach their maximal quadriceps fatigue. During typical weight-lifting, resistance is mostly loaded on the agonist muscle group. Therefore, we implemented isokinetic resistance on knee extension instead of on flexion (hamstring-antagonist) so that the present results regarding joint function are particularly applicable to resistance exercises that produce quadriceps fatigue. In one previous report [12], the increased error rates in knee joint position sense between agonist (quadriceps) and antagonist (hamstring) muscle fatigue were similar. Thus, we assume that similar joint dysfunction may occur when hamstring muscle groups are fatigued.

This study has several limitations. First, it consisted of men only in order to eliminate a potential confounder that might arise from sex difference. Thus, generalizing the conclusions to women cannot be made at this moment. Second, we acknowledge that our participants were not blinded. The document explaning the testing procedures provided information of random group allocations. After the first isokinetic exercise, participants were obviously aware of what group they were in, which could have affected participants’ maximal effort and motivation. Third, verbal encouragement was provided by two investigators (HL and JS) which may have not guaranteed the consistent stimulus. However, more than 90% of the verbal encouragement was provided by one researcher (HL). Additionally, the loudness was consistent with a small variation (97.1 $\pm$ 2.0 dB). Therefore, we believe that the effect of this variable was minimal. Lastly, we did not compare the number of repetitions performed at each set in each condition. That said, this may have not been a major limitation since we used a between-subject design in which the same number of contractions may have yielded different magnitudes of muscle fatigue in each condition.

5. Conclusions

Receiving verbal encouragement during three sets of knee extension exercise appears to be effective in maintaining the quadriceps central activation, but not for enhancing quadriceps strength and knee joint replication. This observation supports the idea that peripheral contributing factors such as energy delpletion or metabolic byproducts accumulation play a larger role than central factors in force production against exercise-induced muscle fatigue. Since centrally-driven fatigue could potentially affect muscle and joint function in subsequent exercises, we still recommend practicing verbal encouragement during multiple sets of exercise.

Author contributions

CONCEPTION: Hyunwook Lee, Jaeyoon Shin, Daeho Kim and Jihong Park.

PERFORMANCE OF WORK: Hyunwook Lee, Jaeyoon Shin and Daeho Kim.

INTERPRETATION OR ANALYSIS OF DATA: Hyunwook Lee, Jaeyoon Shin, Daeho Kim and Jihong Park.

PREPARATION OF THE MANUSCRIPT: Hyunwook Lee and Jihong Park.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Hyunwook Lee, Jaeyoon Shin, Daeho Kim and Jihong Park.

SUPERVISION: Jihong Park.

Ethical considerations

This study was approved by the Kyung Hee University’s institutional review board (approval number KHSIRB 2015-010 dated 19/06/2015). All participants provided signed inform consent.

Funding

The authors report no funding.

Footnotes

Acknowledgments

The data of this study are part of Hyunwook Lee and Jaeyoon Shin’s undergraduate thesis project.

Conflict of interest

The authors declare that they have no competing interests.

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