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Muscle fatigue during intermittent exercise in individuals with mental retardation
Research in Developmental Disabilities 31 (2010) 388–396
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Research in Developmental Disabilities
Muscle fatigue during intermittent exercise in individuals with mental retardation Andreas Zafeiridis *, Paraskevi Giagazoglou, Konstantina Dipla, Konstantinos Salonikidis, Chrisanthi Karra, Eleftherios Kellis ** Department of Physical Education & Sport Sciences at Serres, Aristotle University of Thessaloniki, Serres, Greece
A R T I C L E I N F O
A B S T R A C T
Article history: Received 28 September 2009 Accepted 1 October 2009
This study examined fatigue profile during intermittent exercise in 10 men with mild to moderate mental retardation (MR) and 10 men without mental retardation (C). They performed 4 30 s maximal knee extensions and flexions with 1-min rest on an isokinetic dynamometer. Peak torque of flexors (PTFL) and extensors (PTEX), total work (TW), and lactate were measured. Fatigue was calculated as the magnitude of decline (%) in PTFL, PTEX, and TW and as rate of decline (linear slope) in TW from 1st to 4th set. MR had lower PTFL, PTEX, TW, and lactate throughout the protocol than C, while pre-motor time was greater in MR vs. C (p < 0.05). MR demonstrated a delayed pattern of reduction in muscular performance. Lower values were observed in MR vs. C in the magnitude of decline for PTEX and TW and the rate of decline for TW. In conclusion, MR exhibit a different fatigue profile during intermittent exercise than C. The lower magnitude and decline rate in neuromuscular performance in MR during intermittent exercise is associated with their lower peak strength, short-term anaerobic capacity, and lactate accumulation. Rehabilitation and sport professionals should consider the differences in fatigue profile when designing intermittent exercise programs for MR. ß 2009 Elsevier Ltd. All rights reserved.
Keywords: Exercise Intellectual disability Intelligence Mental retardation Fatigue Strength Rehabilitation
1. Introduction Strength and muscular fatigue are integral components of physical fitness and overall health. Fatigue originates in peripheral and central cites. Peripheral fatigue has been linked to absolute strength (Nordlund, Thorstensson, & Cresswell, 2004), substrate depletion, and/or metabolite accumulation in muscles (St Clair Gibson, Lambert, & Noakes, 2001) while the contribution of the central nervous system to fatigue depends on neural processes that govern voluntary activation of a muscle (Enoka & Stuart, 1992; Gandevia, 1998, 2001). Indeed, it has been documented that individuals with lower levels of strength, lower glycolytic capacity, lower ability of maximal voluntary activation, as well as lower voluntary activation of motor units during exercise demonstrate lower fatigue during sustained high-intensity muscular contraction (Enoka & Stuart, 1992; Hicks, Kent-Braun, & Ditor, 2001; Nordlund et al., 2004; Streckis, Skurvydas, & Ratkevicius, 2007; Yamada, Kaneko, & Masuda, 2002). Numerous studies have shown that sedentary adults and elite athletes with mental retardation demonstrate lower strength measures compared to individuals without mental retardation (Croce, Pitetti, Horvat, & Miller, 1996; Horvat, Croce, Pitetti, & Fernhall, 1999; Horvat, Pitetti, & Croce, 1997; van de Vliet et al., 2006). There is also evidence that individuals with mental retardation may have disturbed central and peripheral processing components as indicated by the longer reaction
* Corresponding author at: TEFAA at Serres, Aristotle University of Thessaloniki, Ag. Ioannis, 62110 Serres, Greece. Tel.: +30 2310 991082. ** Laboratory of Neuromechanics, TEFAA at Serres, Aristotle University of Thessaloniki, Serres, Greece. E-mail address: [email protected] (A. Zafeiridis). 0891-4222/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2009.10.003
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and motor times (Davis, Sparrow, & Ward, 1991; LeClair, Pollock, & Elliot, 1993); and the associations of intelligence and/or general mental ability with peripheral (Tan, 1996) and brain (Reed, Vernon, & Johnson, 2004) nerve conduction velocities and with neural transmission (McRorie & Cooper, 2003, 2004). Finally, individuals with mental retardation demonstrate damage in the integrity of white matter tracts that are responsible for the processing and control of sensory and motor information controlling arousal and motor function (Yu et al., 2008) that may affect motoneuronal recruitment and movement control during sustained effort. Thus, the lower strength, the impaired central nervous system, and their association with fatigue suggest that fatigue profile during exercise may be different between individuals with and without mental retardation. While several studies examined muscular fatigue during exercise in individuals with typical development (Clark, Collier, Manini, & Ploutz-Snyder, 2005; Hicks et al., 2001; Hunter, Griffith, Schlachter, & Kufahl, 2009; Kanehisa, Okuyama, Ikegawa, & Fukunaga, 1996; Pincivero, Gandaio, & Ito, 2003; Russ, Towse, Wigmore, Lanza, & Kent-Braun, 2008; Wu¨st, Morse, de Haan, Jones, & Degens, 2008), information on fatigue profile during intermittent exercise in adults with mental retardation is lacking. Muscular fatigue that occurs during intermittent exercise is a characteristic of many exercise training programs and sports. Exercise training has essential implications for individuals with mental disabilities since they demonstrate low physical fitness that has been directly related to their productivity in the work settings (Fernhall, 1993). Furthermore, in the last years individuals with mental retardation are regularly involved in intensive training to achieve a high level of physical fitness in order to participate in athletic competitions. Thus, the knowledge on the ability of the muscles to resist fatigue in individuals with mental retardation should be of great interest to rehabilitation and sport professionals because it provides a more complete profile of their neuromuscular function. In addition, understanding the ability to repeat exercise bouts during intermittent exercise (fatigue resistance) in these individuals is essential for planning and designing exercise programs for recreational and social purposes, as well as for the development of motor skills and physical fitness in rehabilitation and sport settings. Therefore, the aim of this study was to examine the fatigue profile during intermittent exercise in individuals with mental retardation vs. that in individuals without mental retardation. Furthermore, we investigated the ability of individuals with mental retardation to produce work during short-term continuous muscular effort (anaerobic capacity). 2. Methods 2.1. Participants Ten healthy men with typical development and 10 healthy individuals with mental retardation participated in the study. All volunteers engaged in recreational physical activities three times per week. The institutional review board approved the experimental protocol and the participants with typical development provided written consent; the informed consent for the individuals with mental retardation was provided by their parents or legal guardians. The IQ of participants with mental retardation was determined by a Weschler Intelligence Scale test. Participants with mental retardation had intelligence quotients (IQ) that was within a range for individuals with mild-moderate mental retardation (51 5). 2.2. Study design Each participant reported to the exercise laboratory in the morning of the testing. Following orientation and assessment of physical characteristics, they performed an intermittent exercise protocol that involved 4 sets of 30 s (18 maximal flexions and extensions of the knee joint), with a 60 s rest interval between sets. Peak torque of knee flexors (PTFL) and extensors (PTEX), and total work (TW) produced were measured at each set and fatigue was calculated. Pre-motor time was measured before the fatiguing protocol and blood lactate concentrations were measured at rest and 5 min after the completion of the exercise protocol. The participants were asked to abstain from exercise activity for 48 h before the study, to have sufficient rest the night prior the experiment, and to refrain from caffeine ingestion the day of the experiment. 2.3. Testing procedures and instrumentation Upon arrival to the laboratory height and body weight (Seca, Hamburg, Germany) were measured. Following a 10-min rest, a blood sample (5 mL) was obtained from the fingertip for the determination of baseline lactate concentration (LACTATE PRO, Akray, Japan). Next, the participants underwent a 5-min warm up on a bicycle ergometer at a heart rate of 120–130 bpm, and 5 min of stretching exercises. Following warm-up, the skin was shaved and cleaned with alcohol and bipolar surface electrodes (Model SS2, Biopac Systems, Inc., Goleta, CA, bipolar silver/silver chloride electrodes, center-to-center interelectrode distance = 2 cm) were applied to the belly of vastus medialis and on the patella for bipolar EMG recording (MP100, Biopac System, Inc.) in order to measure pre-motor time. The electrodes were interfaced to a portable amplifier/transmitter (Model TEL100M, Biopac Systems, Inc., Goleta, CA, Common mode rejection ratio > 110 db at 50/60 Hz, bandwidth = 10–500 Hz; gain = 1000). The unit was interfaced to a Biopac MP100 Data Acquisition unit (Biopac Systems, Inc., Goleta, CA) and converted into digital form at a rate of 1000 Hz. Pressing the PC mouse a lamp was turned on and at the same time a signal was given to initiate the EMG recording. The participants were asked to perform a knee extension movement as fast as possible after the visual signal to assess pre-motor time. Pre-motor time (ms) was defined as a period between the onset of a visual stimulus and the beginning of muscle activity as recorded by change in EMG (Horvat, Ramsey, Amestoy, & Croce, 2003).
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Fig. 1. The course of absolute torque of knee extensors and flexors over 18 repetitions during the first set in individuals with mental retardation.
The fatiguing protocol was performed on the Kin Com isokinetic dynamometer (Chatanooga Group Inc., USA). The subjects assumed a seated position and their body was adjusted and secured to minimize extraneous movements. The axis of rotation of the dynamometer was carefully aligned with the approximate knee joint axis of rotation (lateral femoral epicondyle), the gravity correction was performed, and the angular velocity was set at 1208 s 1. Only the leg of preference was tested. Next, the participants performed three submaximal and three maximal efforts of the knee extensors and flexors to determine PTEX and PTFL. After a 5-min rest, the participants performed the main testing protocol that consisted of 4 30 s maximum knee extensions and flexions at angular velocity 1208 s 1 (18-reps for each movement). The selection of 30 s for each set was based on the facts that in several published studies, individuals with moderate mental retardation have been engaged in maximal efforts for at least 30 s (i.e. Wingate test, last stage of VO2max test, sit-up and other endurance tests) (Chia, Lee, & Teo-Koh, 2002; Fernhall et al., 1998; MacDonncha, Watson, McSweeney, & O’Donovan, 1999; Pommering et al., 1994; van de Vliet et al., 2006) and because a longer duration may result in a drop of subjects’ motivation. Isokinetic dynamometry was chosen as several studies have assessed fatigue using 30–50 maximal reps (Kanehisa et al., 1996; Laforest, St-Pierre, Cyr, & Gayton, 1990; Pincivero et al., 2003; Pincivero, Gear, & Sterner, 2001), and because isokinetic dynamometry has been consistently used in individuals with mental retardation to measure peak torque (Angelopoulou, Tsimaras, Christoulas, Kokaridas, & Mandroukas, 1999; Croce et al., 1996; Horvat et al., 1997, 1999; Pitetti, Climstein, Mays, & Barrett, 1992). This protocol has been previously used to assess muscle fatigue (Dipla et al., 2009). In this study, every attempt was made to have the participants to perform their maximum. These included practice sessions for the movement before testing, continuous verbal motivation to the participants to work as hard as possible in both directions of the movement. Also, the coach of individuals with mental retardation was present during all practice and testing sessions to supervise the procedures. The course of peak torques of extensors and flexors values over the 18 repetitions in individuals with mental retardation (Fig. 1) was typical to that observed during fatiguing isokinetic protocol using maximal contractions (slight increase in the second-third repetition and then gradual decline). Five minutes after the completion of the exercise, a blood sample (5 mL) was obtained from the fingertip and analyzed for lactate concentration (mmol L 1). 2.4. Measurements and calculations The absolute PTEX (Nm) and PTFL (Nm), and TW (J) of each set were directly computed and recorded by the Kin Com software. TW in each set was calculated by the summation of work produced during each movement. Fatigue was calculated using the magnitude and the rate of decline. The fatigue resistance was calculated as the % of the PTEX, PTFL, and TW value achieved in the 4th set relative to the 1st set [i.e. fatigue resistance = (4th set value/1st set value) 100]; where higher (%) values indicate greater fatigue resistance. The rate of decline was calculated for TW by using the slope of linear regression from the 1st to the 4th set for each participant. The presentation of muscle fatigue by linear slope has been previously used (Halin, Germain, Bercier, Kapitaniak, & Buttelli, 2003; Pincivero et al., 2001, 2003) and has been suggested to quantify muscle fatigue during high-intensity, short-term exercise more reliably compared to the % decline (Pincivero et al., 2001). 2.5. Statistical analysis All data are presented as means SD and were analyzed by Statistica (version 7.0, StatSoft Inc., Tulsa, OK). The physical characteristics, pre-motor time, and fatigue were analyzed using t-tests for independent groups. Two-way ANOVA with repeated measures were used to analyze data for absolute PTFL, PTEX, TW, and lactate. Tukey post hoc tests were used to locate the significantly different means. The relationships between: (a) fatigue resistance for TW and peak TW values and (b) fatigue
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resistance for TW and peak lactate concentration were examined using Pearson’s correlation analysis. The level of significance for all statistical analyses was set at p < 0.05. 3. Results 3.1. Physical and physiological characteristics There were no differences between individuals with and without mental retardation in age (24.0 3.3 yrs vs. 23.5 4.2 yrs) and body mass (78.4 8.4 kg vs. 73.2 12.9 kg; BMI 24.7 1.9 vs. 24.6 4.8). However, individuals with mental retardation (MR) were significantly shorter compared to their counterparts without mental retardation (173 6 cm vs. 178 5 cm; p < 0.05). Individuals without mental retardation (C) exhibited significantly greater absolute and relative peak torques of flexors and extensors, and total work than MR (p < 0.05), while pre-motor time was significantly greater in MR vs. C (p < 0.05). The peak torque and total work parameters, as well as, pre-motor times in the two groups are presented in Table 1. Table 1 Physiological characteristics. Variable
MR (n = 10)
Control (n = 10)
PTFL Absolute (Nm) Relative (Nm/kg)
92 23 1.3 0.3
133 36** 1.7 0.5*
PTEX Absolute (Nm) Relative (Nm/kg)
126 29 1.7 0.4
165 30** 2.1 0.4*
2893 388 40.1 5.6 276 60
4324 710** 55.3 8.6** 215 52*
TW (FL + EX) Absolute (J) Relative (J/kg) Pre-motor time (ms) * **
p < 0.05 vs. MR. p < 0.01 vs. MR.
Fig. 2. Absolute values (means SD) of peak torque of flexors (PTFL) and extensors (PTEX), and total work (TW) for individuals with mental retardation (MR) and those with typical intelligence (control) in 4 sets. *Significantly different (p < 0.001–0.05) from the respective value of the 1st set. #Significantly different (p < 0.01) between MR and control for the respective set.
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Fig. 3. Magnitude of decline (%) = [(1st set value 4th set value)/1st set value) 100] of peak torque (PT) and total work (TW) of flexors (FL) and extensors (EX) for individuals with mental retardation (MR) and those with typical intelligence (control). *Significant difference between MR and control at p < 0.01–0.05.
3.2. Fatigue parameters The two-way ANOVA indicated a significant ‘‘group set’’ interaction for absolute PTFL (Nm) (p < 0.05), PTEX (Nm) (p < 0.001), and TW (J) (p < 0.001) (Fig. 2). During the fatiguing protocol, peak torques of flexors and extensors and total work demonstrated a significant decline in both groups (p < 0.001). PTEX and PTFL started to decline from the 2nd and 3rd set, respectively, in C group, and from 3rd and 4th set in MR (p < 0.001). In both groups TW started to declined from the 2nd set; the decline was continuous in C group throughout the protocol (p < 0.05), whereas it was stabilized after the 3rd set in the
Fig. 4. The relationships between fatigue resistance and fatigue slopes (rate of decline) of TW with the peak values of TW and peak lactate concentration at the end of protocol.
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Fig. 5. *p < 0.001 rest vs. mid-point and vs. 5 min recovery within both groups; #p < 0.01–0.001 between MR and control.
MR group. Pair-wise comparisons between groups within each set, revealed that the absolute values for all variables were significantly higher in C than in MR in all 4 sets (p < 0.01). The magnitude (%) of decline in the 4th set was significantly greater (p < 0.05) in participants with typical development vs. MR for PTEX (28.2 9.8% vs. 19.4 8.7%; p < 0.05) and for TW (41.4 5.5% vs. 32.3 8.2%; p < 0.01). No differences were detected in the magnitude of decline for PTFL (21.8 5.7% vs. 18.8 13.6%) (Fig. 3). When the rate of decline was examined, the regression coefficients (R2) of the linear fit for TW values ranged from 0.88 to 1.00 in participants with typical development (0.94 0.05; p < 0.05) and from 0.80 to 0.99 in MR (0.90 0.06; p < 0.05). The results revealed significantly steeper slope (greater rate of fatigue) in participants with typical development compared to MR for TW ( 600 142 J/set vs. 312 84 J/set; p < 0.001). Pearson’s correlation analysis documented significant associations between the fatigue resistance and fatigue slopes of TW with the peak values of TW (r = 53 and r = 90 for fatigue resistance and fatigue slope, respectively; p < 0.05 and 0.001; Fig. 4) and peak lactate concentration (r = 56 and r = 67 for fatigue resistance and fatigue slope, respectively; p < 0.01 and 0.001; Fig. 4). There was a significant (p < 0.01) ‘‘group time’’ interaction for lactate (Fig. 5). Lactate increased with time in both groups (p < 0.001). MR demonstrated lower lactate values vs. C at mid- (5.44 1.74 vs. 7.99 1.47; p < 0.01) and end-protocol (7.66 3.04 vs. 10.59 2.06; p < 0.001). 4. Discussion The major finding of this study was that although individuals with mental retardation demonstrate lower peak muscular performance, neuromuscular fatigue develops at a slower rate during high-intensity intermittent exercise compared to adults with typical development. The rate and the magnitude of decline in neuromuscular performance were associated with peak strength, short-term anaerobic capacity (total work), and the accumulation of by-products of metabolism. Furthermore, we observed a delayed period between the onset of a visual stimulus and the beginning of muscular activity in individuals with mental retardation. In this study, adults with mental retardation attained 70% and 77% of the peak torque of extensors and flexors, respectively, of those observed in typically developing adults. Previous studies have reported slightly larger differences in peak torque generating capacity when individuals with typical development were compared with untrained mentally retarded individuals (Angelopoulou et al., 1999; Croce et al., 1996; Horvat et al., 1997, 1999; Pitetti et al., 1992), but smaller differences when typically developing individuals were compared to elite athletes with mental retardation (van de Vliet et al., 2006). Thus, the differences in the effect size between this and other studies may be the result of the lifestyle of our mentally retarded participants who were regularly involved in athletic training (3–4 times/week for at least 3 yrs), although they were not elite athletes. A noteworthy finding of this study is that adults with mental retardation clearly demonstrate a lower short-term anaerobic capacity that approximates 65% of that observed in their typically developing counterparts. To the best of our knowledge, previous studies that examined muscular function in individuals with mental retardation have focused on their ability to generate maximal force or torque. Our results are in line with Chia et al. (2002) who reported a 56% lower mean anaerobic power (as assessed by the Wingate test) in children with mental retardation compared to those without mental retardation. The lower peak strength/power and anaerobic power of mentally retarded individuals may be attributed to possible differences in neural drive and neuromuscular coordination (Chia et al., 2002). However, it should be pointed out, that these physical and physiological qualities manifest part of their intrinsic characteristic and are evident when they perform exercise training or even during their daily tasks. In support of that, Yu et al. (2008) observed damage of the corticospinal tract in mentally retarded individuals and proposed that there is a possible neural basis for the impaired motor function.
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Muscular fatigue has been extensively studied in individuals with typical development (Clark et al., 2005; Hicks et al., 2001; Hunter et al., 2009; Kanehisa et al., 1996; Pincivero et al., 2003; Russ et al., 2008; Wu¨st et al., 2008); however, this is the first study to examine neuromuscular fatigue in adults with mental retardation. Individuals with mental retardation maintain better their maximal performances during intermittent exercise compared to those with typical development. The differences in the fatigue profile between individuals with and without mental retardation was expressed by: (i) the significant ‘‘group set’’ interaction and the delayed onset of reduction in peak muscular performance parameters in MR (Fig. 2), (ii) the lower magnitude of reduction in neuromuscular performance at the completion of the entire protocol in MR (Fig. 3), and (iii) an approximately two-fold reduced rate in the decrease of total work in MR. Our findings are not in agreement with those of Auxter (1966) who examined muscular fatigue in children 9–11 yrs of age with moderate mental retardation. The author reported that the ability of children with mental retardation to sustain 4–5-s maximal isometric contractions on handgrip dynamometer was significantly lower compared to their typically developing counterparts. At that time, the author stated that in the absence of known physiological differences between children with and without mental retardation, psychological factors should be considered as explanations to these differences. However, since then several physiological differences have been reported between individuals with and without mental retardation, such as disturbed central and peripheral processing components and deformities in the integrity of brain white mater (Davis et al., 1991; LeClair et al., 1993; McRorie & Cooper, 2003; Tan, 1996; Yu et al., 2008). The explanations behind the differences in the ability to resist fatigue between individuals with and without mental retardation are not readily available. However, three of the most prudent hypotheses to explain fatigue differences in individuals with mental retardation might be: (i) the lower ability of individuals with mental retardation to achieve maximal voluntary activation, (ii) the lower absolute forces developed during the fatiguing protocol (Table 1) in individuals with mental retardation, and (iii) the lower reliance on glycolytic metabolism for energy production in individuals with mental retardation as suggested by their lower lactate concentration (Fig. 5). Although, there is scientific evidence that each of the above factors alone may influence the ability of an individual to resist fatigue, the interrelation/interdependence among them is apparent. It has been demonstrated that individuals with poor ability to achieve full activation during a maximal voluntary contraction develop less peripheral fatigue (Nordlund et al., 2004) and longer endurance time during a fatiguing protocol (Yamada et al., 2002). In fact, Nordlund et al. (2004) reported that the level of activation in the first bout of intermittent isometric fatiguing protocol could explain 39% of the peripheral fatigue. The logic behind the above idea is that individuals with a lower ability to achieve full activation will recruit less fast-twitch motor units at the beginning of exercise and therefore have greater ability to sustain the initially generated force and experience less fatigue (Nordlund et al., 2004). Pincivero et al. (2001) also suggested that higher motor unit activation at the beginning of exercise may result in a faster rate of fatigue during an isokinetic protocol. Despite the fact that neither we nor others have assessed the ability of maximal voluntary activation in individuals with mental retardation, there is ample evidence to suggest that they may be classified as a low voluntary activation population. This is supported by several facts collectively. First, individuals with mental retardation demonstrate a low maximal muscular force that is independent of their body dimensions (this study; Horvat et al., 1999). Second, maximal voluntary force depends on the extent of motor unit activation (Gandevia, 2001) and movement coordination (Van Praagh & Dore´, 2002) that are influenced by the development of the CNS and its integration with periphery. Third, in individuals with mental retardation there is damage in the integrity of corpus callosum and corticospinal tract (Yu et al., 2008)—important structures for communication of sensorimotor information and major motor pathway in CNS that transmits the neural drive to motoneurons. Fourth, corticospinal lesions in several pathological conditions impair the voluntary drive (Gandevia, 2001). Further evidence for the disturbed central and peripheral processing components in individuals with mental retardation may be provided by their longer pre-motor and/or motor times (this study; Davis et al., 1991; Horvat et al., 2003) and the associations of intelligence with neural transmission (McRorie & Cooper, 2003) and nerve conduction velocities (Reed et al., 2004; Tan, 1996). In the present study, individuals with mental retardation produced significantly lower absolute forces and total work (Fig. 2) throughout the fatiguing protocol. Furthermore, the rate of decline and fatigue resistance were correlated with total work production in the first set ( 0.90 and 0.53, respectively). These results support the general view that the greater the force exerted, work done or rate of work during a task the more the muscle will fatigue (Enoka & Stuart, 1992). Nordlund et al., 2004 reported that the maximal voluntary torque in the first bout of intermittent fatiguing protocol explained as much as 55% of the peripheral fatigue. The explanation for the inverse relationship between the ability to generate greater absolute forces and fatigue resistance may be linked to muscle fibre composition, muscle metabolism, and the ability of an individual to achieve full activation (activate type II muscle fibres). Lactate concentration was significantly lower in participants with mental retardation; this provides indirect evidence that they relied less on the glycolytic system for energy production. This is in line with Chia et al. (2002) who found lower blood lactate levels in children with mental retardation vs. typically developing children after a Wingate test. It has been discussed that the increased accumulation of by-products of anaerobic metabolism may impair the excitation-contraction coupling and cross-bridges formation (peripheral fatigue), as well as decrease the motoneuron excitability by an increase input of metabolically sensitive group III and IV muscle afferents (central fatigue). However, it should be pointed out that the effect of metabolites on the involvement of group III and IV muscle afferents on decreased motoneuron excitability is still uncertain and controversial effects have been reported for different muscle groups (Martin, Smith, Butler, Gandevia, & Taylor, 2006; Taylor & Gandevia, 2008).
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5. Conclusion In conclusion, the results of this study confirm previous findings that individuals with mental retardation have inferior strength compared to those with typical development. The present study extends the knowledge on neuromuscular function of individuals with mental retardation reporting that they also have limited ability to produce work at high rates during short continuous muscular effort (anaerobic capacity). Thus, exercise training is imperative for individuals with mental retardation since physical fitness (in particular muscular strength) has been related to their productivity in the work settings (Fernhall, 1993) and overall health. This study also provides evidence that albeit individuals with mental retardation have lower maximal performances, they maintain better their maximal strength and anaerobic capacity during an intermittent exercise, suggesting greater recovery potentials after maximal efforts. This supports the general view that the lower the force exerted, work done or rate of work during a task the less the muscle will fatigue (Enoka & Stuart, 1992). However, it should be kept in mind that this ability may not be evident when individuals with mental retardation perform daily tasks that require a specific amount of absolute work because they will be working at higher relative intensities. Insights into the ability of individuals with mental retardation to repeat exercise bouts during intermittent training is important in rehabilitation and sport settings in order to design exercise programs to optimize improvements in physical fitness and in skill acquisition; and to reduce the risk of musculoskeletal injury due to fatigue during training. Yet, the perspective that individuals with mental retardation may be less capable of maximally activate their motoneuron pool appears as an appealing view to explain their different fatigue profile during intermittent exercise. 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Contents lists available at ScienceDirect
Research in Developmental Disabilities
Muscle fatigue during intermittent exercise in individuals with mental retardation Andreas Zafeiridis *, Paraskevi Giagazoglou, Konstantina Dipla, Konstantinos Salonikidis, Chrisanthi Karra, Eleftherios Kellis ** Department of Physical Education & Sport Sciences at Serres, Aristotle University of Thessaloniki, Serres, Greece
A R T I C L E I N F O
A B S T R A C T
Article history: Received 28 September 2009 Accepted 1 October 2009
This study examined fatigue profile during intermittent exercise in 10 men with mild to moderate mental retardation (MR) and 10 men without mental retardation (C). They performed 4 30 s maximal knee extensions and flexions with 1-min rest on an isokinetic dynamometer. Peak torque of flexors (PTFL) and extensors (PTEX), total work (TW), and lactate were measured. Fatigue was calculated as the magnitude of decline (%) in PTFL, PTEX, and TW and as rate of decline (linear slope) in TW from 1st to 4th set. MR had lower PTFL, PTEX, TW, and lactate throughout the protocol than C, while pre-motor time was greater in MR vs. C (p < 0.05). MR demonstrated a delayed pattern of reduction in muscular performance. Lower values were observed in MR vs. C in the magnitude of decline for PTEX and TW and the rate of decline for TW. In conclusion, MR exhibit a different fatigue profile during intermittent exercise than C. The lower magnitude and decline rate in neuromuscular performance in MR during intermittent exercise is associated with their lower peak strength, short-term anaerobic capacity, and lactate accumulation. Rehabilitation and sport professionals should consider the differences in fatigue profile when designing intermittent exercise programs for MR. ß 2009 Elsevier Ltd. All rights reserved.
Keywords: Exercise Intellectual disability Intelligence Mental retardation Fatigue Strength Rehabilitation
1. Introduction Strength and muscular fatigue are integral components of physical fitness and overall health. Fatigue originates in peripheral and central cites. Peripheral fatigue has been linked to absolute strength (Nordlund, Thorstensson, & Cresswell, 2004), substrate depletion, and/or metabolite accumulation in muscles (St Clair Gibson, Lambert, & Noakes, 2001) while the contribution of the central nervous system to fatigue depends on neural processes that govern voluntary activation of a muscle (Enoka & Stuart, 1992; Gandevia, 1998, 2001). Indeed, it has been documented that individuals with lower levels of strength, lower glycolytic capacity, lower ability of maximal voluntary activation, as well as lower voluntary activation of motor units during exercise demonstrate lower fatigue during sustained high-intensity muscular contraction (Enoka & Stuart, 1992; Hicks, Kent-Braun, & Ditor, 2001; Nordlund et al., 2004; Streckis, Skurvydas, & Ratkevicius, 2007; Yamada, Kaneko, & Masuda, 2002). Numerous studies have shown that sedentary adults and elite athletes with mental retardation demonstrate lower strength measures compared to individuals without mental retardation (Croce, Pitetti, Horvat, & Miller, 1996; Horvat, Croce, Pitetti, & Fernhall, 1999; Horvat, Pitetti, & Croce, 1997; van de Vliet et al., 2006). There is also evidence that individuals with mental retardation may have disturbed central and peripheral processing components as indicated by the longer reaction
* Corresponding author at: TEFAA at Serres, Aristotle University of Thessaloniki, Ag. Ioannis, 62110 Serres, Greece. Tel.: +30 2310 991082. ** Laboratory of Neuromechanics, TEFAA at Serres, Aristotle University of Thessaloniki, Serres, Greece. E-mail address: [email protected] (A. Zafeiridis). 0891-4222/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2009.10.003
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and motor times (Davis, Sparrow, & Ward, 1991; LeClair, Pollock, & Elliot, 1993); and the associations of intelligence and/or general mental ability with peripheral (Tan, 1996) and brain (Reed, Vernon, & Johnson, 2004) nerve conduction velocities and with neural transmission (McRorie & Cooper, 2003, 2004). Finally, individuals with mental retardation demonstrate damage in the integrity of white matter tracts that are responsible for the processing and control of sensory and motor information controlling arousal and motor function (Yu et al., 2008) that may affect motoneuronal recruitment and movement control during sustained effort. Thus, the lower strength, the impaired central nervous system, and their association with fatigue suggest that fatigue profile during exercise may be different between individuals with and without mental retardation. While several studies examined muscular fatigue during exercise in individuals with typical development (Clark, Collier, Manini, & Ploutz-Snyder, 2005; Hicks et al., 2001; Hunter, Griffith, Schlachter, & Kufahl, 2009; Kanehisa, Okuyama, Ikegawa, & Fukunaga, 1996; Pincivero, Gandaio, & Ito, 2003; Russ, Towse, Wigmore, Lanza, & Kent-Braun, 2008; Wu¨st, Morse, de Haan, Jones, & Degens, 2008), information on fatigue profile during intermittent exercise in adults with mental retardation is lacking. Muscular fatigue that occurs during intermittent exercise is a characteristic of many exercise training programs and sports. Exercise training has essential implications for individuals with mental disabilities since they demonstrate low physical fitness that has been directly related to their productivity in the work settings (Fernhall, 1993). Furthermore, in the last years individuals with mental retardation are regularly involved in intensive training to achieve a high level of physical fitness in order to participate in athletic competitions. Thus, the knowledge on the ability of the muscles to resist fatigue in individuals with mental retardation should be of great interest to rehabilitation and sport professionals because it provides a more complete profile of their neuromuscular function. In addition, understanding the ability to repeat exercise bouts during intermittent exercise (fatigue resistance) in these individuals is essential for planning and designing exercise programs for recreational and social purposes, as well as for the development of motor skills and physical fitness in rehabilitation and sport settings. Therefore, the aim of this study was to examine the fatigue profile during intermittent exercise in individuals with mental retardation vs. that in individuals without mental retardation. Furthermore, we investigated the ability of individuals with mental retardation to produce work during short-term continuous muscular effort (anaerobic capacity). 2. Methods 2.1. Participants Ten healthy men with typical development and 10 healthy individuals with mental retardation participated in the study. All volunteers engaged in recreational physical activities three times per week. The institutional review board approved the experimental protocol and the participants with typical development provided written consent; the informed consent for the individuals with mental retardation was provided by their parents or legal guardians. The IQ of participants with mental retardation was determined by a Weschler Intelligence Scale test. Participants with mental retardation had intelligence quotients (IQ) that was within a range for individuals with mild-moderate mental retardation (51 5). 2.2. Study design Each participant reported to the exercise laboratory in the morning of the testing. Following orientation and assessment of physical characteristics, they performed an intermittent exercise protocol that involved 4 sets of 30 s (18 maximal flexions and extensions of the knee joint), with a 60 s rest interval between sets. Peak torque of knee flexors (PTFL) and extensors (PTEX), and total work (TW) produced were measured at each set and fatigue was calculated. Pre-motor time was measured before the fatiguing protocol and blood lactate concentrations were measured at rest and 5 min after the completion of the exercise protocol. The participants were asked to abstain from exercise activity for 48 h before the study, to have sufficient rest the night prior the experiment, and to refrain from caffeine ingestion the day of the experiment. 2.3. Testing procedures and instrumentation Upon arrival to the laboratory height and body weight (Seca, Hamburg, Germany) were measured. Following a 10-min rest, a blood sample (5 mL) was obtained from the fingertip for the determination of baseline lactate concentration (LACTATE PRO, Akray, Japan). Next, the participants underwent a 5-min warm up on a bicycle ergometer at a heart rate of 120–130 bpm, and 5 min of stretching exercises. Following warm-up, the skin was shaved and cleaned with alcohol and bipolar surface electrodes (Model SS2, Biopac Systems, Inc., Goleta, CA, bipolar silver/silver chloride electrodes, center-to-center interelectrode distance = 2 cm) were applied to the belly of vastus medialis and on the patella for bipolar EMG recording (MP100, Biopac System, Inc.) in order to measure pre-motor time. The electrodes were interfaced to a portable amplifier/transmitter (Model TEL100M, Biopac Systems, Inc., Goleta, CA, Common mode rejection ratio > 110 db at 50/60 Hz, bandwidth = 10–500 Hz; gain = 1000). The unit was interfaced to a Biopac MP100 Data Acquisition unit (Biopac Systems, Inc., Goleta, CA) and converted into digital form at a rate of 1000 Hz. Pressing the PC mouse a lamp was turned on and at the same time a signal was given to initiate the EMG recording. The participants were asked to perform a knee extension movement as fast as possible after the visual signal to assess pre-motor time. Pre-motor time (ms) was defined as a period between the onset of a visual stimulus and the beginning of muscle activity as recorded by change in EMG (Horvat, Ramsey, Amestoy, & Croce, 2003).
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Fig. 1. The course of absolute torque of knee extensors and flexors over 18 repetitions during the first set in individuals with mental retardation.
The fatiguing protocol was performed on the Kin Com isokinetic dynamometer (Chatanooga Group Inc., USA). The subjects assumed a seated position and their body was adjusted and secured to minimize extraneous movements. The axis of rotation of the dynamometer was carefully aligned with the approximate knee joint axis of rotation (lateral femoral epicondyle), the gravity correction was performed, and the angular velocity was set at 1208 s 1. Only the leg of preference was tested. Next, the participants performed three submaximal and three maximal efforts of the knee extensors and flexors to determine PTEX and PTFL. After a 5-min rest, the participants performed the main testing protocol that consisted of 4 30 s maximum knee extensions and flexions at angular velocity 1208 s 1 (18-reps for each movement). The selection of 30 s for each set was based on the facts that in several published studies, individuals with moderate mental retardation have been engaged in maximal efforts for at least 30 s (i.e. Wingate test, last stage of VO2max test, sit-up and other endurance tests) (Chia, Lee, & Teo-Koh, 2002; Fernhall et al., 1998; MacDonncha, Watson, McSweeney, & O’Donovan, 1999; Pommering et al., 1994; van de Vliet et al., 2006) and because a longer duration may result in a drop of subjects’ motivation. Isokinetic dynamometry was chosen as several studies have assessed fatigue using 30–50 maximal reps (Kanehisa et al., 1996; Laforest, St-Pierre, Cyr, & Gayton, 1990; Pincivero et al., 2003; Pincivero, Gear, & Sterner, 2001), and because isokinetic dynamometry has been consistently used in individuals with mental retardation to measure peak torque (Angelopoulou, Tsimaras, Christoulas, Kokaridas, & Mandroukas, 1999; Croce et al., 1996; Horvat et al., 1997, 1999; Pitetti, Climstein, Mays, & Barrett, 1992). This protocol has been previously used to assess muscle fatigue (Dipla et al., 2009). In this study, every attempt was made to have the participants to perform their maximum. These included practice sessions for the movement before testing, continuous verbal motivation to the participants to work as hard as possible in both directions of the movement. Also, the coach of individuals with mental retardation was present during all practice and testing sessions to supervise the procedures. The course of peak torques of extensors and flexors values over the 18 repetitions in individuals with mental retardation (Fig. 1) was typical to that observed during fatiguing isokinetic protocol using maximal contractions (slight increase in the second-third repetition and then gradual decline). Five minutes after the completion of the exercise, a blood sample (5 mL) was obtained from the fingertip and analyzed for lactate concentration (mmol L 1). 2.4. Measurements and calculations The absolute PTEX (Nm) and PTFL (Nm), and TW (J) of each set were directly computed and recorded by the Kin Com software. TW in each set was calculated by the summation of work produced during each movement. Fatigue was calculated using the magnitude and the rate of decline. The fatigue resistance was calculated as the % of the PTEX, PTFL, and TW value achieved in the 4th set relative to the 1st set [i.e. fatigue resistance = (4th set value/1st set value) 100]; where higher (%) values indicate greater fatigue resistance. The rate of decline was calculated for TW by using the slope of linear regression from the 1st to the 4th set for each participant. The presentation of muscle fatigue by linear slope has been previously used (Halin, Germain, Bercier, Kapitaniak, & Buttelli, 2003; Pincivero et al., 2001, 2003) and has been suggested to quantify muscle fatigue during high-intensity, short-term exercise more reliably compared to the % decline (Pincivero et al., 2001). 2.5. Statistical analysis All data are presented as means SD and were analyzed by Statistica (version 7.0, StatSoft Inc., Tulsa, OK). The physical characteristics, pre-motor time, and fatigue were analyzed using t-tests for independent groups. Two-way ANOVA with repeated measures were used to analyze data for absolute PTFL, PTEX, TW, and lactate. Tukey post hoc tests were used to locate the significantly different means. The relationships between: (a) fatigue resistance for TW and peak TW values and (b) fatigue
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resistance for TW and peak lactate concentration were examined using Pearson’s correlation analysis. The level of significance for all statistical analyses was set at p < 0.05. 3. Results 3.1. Physical and physiological characteristics There were no differences between individuals with and without mental retardation in age (24.0 3.3 yrs vs. 23.5 4.2 yrs) and body mass (78.4 8.4 kg vs. 73.2 12.9 kg; BMI 24.7 1.9 vs. 24.6 4.8). However, individuals with mental retardation (MR) were significantly shorter compared to their counterparts without mental retardation (173 6 cm vs. 178 5 cm; p < 0.05). Individuals without mental retardation (C) exhibited significantly greater absolute and relative peak torques of flexors and extensors, and total work than MR (p < 0.05), while pre-motor time was significantly greater in MR vs. C (p < 0.05). The peak torque and total work parameters, as well as, pre-motor times in the two groups are presented in Table 1. Table 1 Physiological characteristics. Variable
MR (n = 10)
Control (n = 10)
PTFL Absolute (Nm) Relative (Nm/kg)
92 23 1.3 0.3
133 36** 1.7 0.5*
PTEX Absolute (Nm) Relative (Nm/kg)
126 29 1.7 0.4
165 30** 2.1 0.4*
2893 388 40.1 5.6 276 60
4324 710** 55.3 8.6** 215 52*
TW (FL + EX) Absolute (J) Relative (J/kg) Pre-motor time (ms) * **
p < 0.05 vs. MR. p < 0.01 vs. MR.
Fig. 2. Absolute values (means SD) of peak torque of flexors (PTFL) and extensors (PTEX), and total work (TW) for individuals with mental retardation (MR) and those with typical intelligence (control) in 4 sets. *Significantly different (p < 0.001–0.05) from the respective value of the 1st set. #Significantly different (p < 0.01) between MR and control for the respective set.
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Fig. 3. Magnitude of decline (%) = [(1st set value 4th set value)/1st set value) 100] of peak torque (PT) and total work (TW) of flexors (FL) and extensors (EX) for individuals with mental retardation (MR) and those with typical intelligence (control). *Significant difference between MR and control at p < 0.01–0.05.
3.2. Fatigue parameters The two-way ANOVA indicated a significant ‘‘group set’’ interaction for absolute PTFL (Nm) (p < 0.05), PTEX (Nm) (p < 0.001), and TW (J) (p < 0.001) (Fig. 2). During the fatiguing protocol, peak torques of flexors and extensors and total work demonstrated a significant decline in both groups (p < 0.001). PTEX and PTFL started to decline from the 2nd and 3rd set, respectively, in C group, and from 3rd and 4th set in MR (p < 0.001). In both groups TW started to declined from the 2nd set; the decline was continuous in C group throughout the protocol (p < 0.05), whereas it was stabilized after the 3rd set in the
Fig. 4. The relationships between fatigue resistance and fatigue slopes (rate of decline) of TW with the peak values of TW and peak lactate concentration at the end of protocol.
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Fig. 5. *p < 0.001 rest vs. mid-point and vs. 5 min recovery within both groups; #p < 0.01–0.001 between MR and control.
MR group. Pair-wise comparisons between groups within each set, revealed that the absolute values for all variables were significantly higher in C than in MR in all 4 sets (p < 0.01). The magnitude (%) of decline in the 4th set was significantly greater (p < 0.05) in participants with typical development vs. MR for PTEX (28.2 9.8% vs. 19.4 8.7%; p < 0.05) and for TW (41.4 5.5% vs. 32.3 8.2%; p < 0.01). No differences were detected in the magnitude of decline for PTFL (21.8 5.7% vs. 18.8 13.6%) (Fig. 3). When the rate of decline was examined, the regression coefficients (R2) of the linear fit for TW values ranged from 0.88 to 1.00 in participants with typical development (0.94 0.05; p < 0.05) and from 0.80 to 0.99 in MR (0.90 0.06; p < 0.05). The results revealed significantly steeper slope (greater rate of fatigue) in participants with typical development compared to MR for TW ( 600 142 J/set vs. 312 84 J/set; p < 0.001). Pearson’s correlation analysis documented significant associations between the fatigue resistance and fatigue slopes of TW with the peak values of TW (r = 53 and r = 90 for fatigue resistance and fatigue slope, respectively; p < 0.05 and 0.001; Fig. 4) and peak lactate concentration (r = 56 and r = 67 for fatigue resistance and fatigue slope, respectively; p < 0.01 and 0.001; Fig. 4). There was a significant (p < 0.01) ‘‘group time’’ interaction for lactate (Fig. 5). Lactate increased with time in both groups (p < 0.001). MR demonstrated lower lactate values vs. C at mid- (5.44 1.74 vs. 7.99 1.47; p < 0.01) and end-protocol (7.66 3.04 vs. 10.59 2.06; p < 0.001). 4. Discussion The major finding of this study was that although individuals with mental retardation demonstrate lower peak muscular performance, neuromuscular fatigue develops at a slower rate during high-intensity intermittent exercise compared to adults with typical development. The rate and the magnitude of decline in neuromuscular performance were associated with peak strength, short-term anaerobic capacity (total work), and the accumulation of by-products of metabolism. Furthermore, we observed a delayed period between the onset of a visual stimulus and the beginning of muscular activity in individuals with mental retardation. In this study, adults with mental retardation attained 70% and 77% of the peak torque of extensors and flexors, respectively, of those observed in typically developing adults. Previous studies have reported slightly larger differences in peak torque generating capacity when individuals with typical development were compared with untrained mentally retarded individuals (Angelopoulou et al., 1999; Croce et al., 1996; Horvat et al., 1997, 1999; Pitetti et al., 1992), but smaller differences when typically developing individuals were compared to elite athletes with mental retardation (van de Vliet et al., 2006). Thus, the differences in the effect size between this and other studies may be the result of the lifestyle of our mentally retarded participants who were regularly involved in athletic training (3–4 times/week for at least 3 yrs), although they were not elite athletes. A noteworthy finding of this study is that adults with mental retardation clearly demonstrate a lower short-term anaerobic capacity that approximates 65% of that observed in their typically developing counterparts. To the best of our knowledge, previous studies that examined muscular function in individuals with mental retardation have focused on their ability to generate maximal force or torque. Our results are in line with Chia et al. (2002) who reported a 56% lower mean anaerobic power (as assessed by the Wingate test) in children with mental retardation compared to those without mental retardation. The lower peak strength/power and anaerobic power of mentally retarded individuals may be attributed to possible differences in neural drive and neuromuscular coordination (Chia et al., 2002). However, it should be pointed out, that these physical and physiological qualities manifest part of their intrinsic characteristic and are evident when they perform exercise training or even during their daily tasks. In support of that, Yu et al. (2008) observed damage of the corticospinal tract in mentally retarded individuals and proposed that there is a possible neural basis for the impaired motor function.
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Muscular fatigue has been extensively studied in individuals with typical development (Clark et al., 2005; Hicks et al., 2001; Hunter et al., 2009; Kanehisa et al., 1996; Pincivero et al., 2003; Russ et al., 2008; Wu¨st et al., 2008); however, this is the first study to examine neuromuscular fatigue in adults with mental retardation. Individuals with mental retardation maintain better their maximal performances during intermittent exercise compared to those with typical development. The differences in the fatigue profile between individuals with and without mental retardation was expressed by: (i) the significant ‘‘group set’’ interaction and the delayed onset of reduction in peak muscular performance parameters in MR (Fig. 2), (ii) the lower magnitude of reduction in neuromuscular performance at the completion of the entire protocol in MR (Fig. 3), and (iii) an approximately two-fold reduced rate in the decrease of total work in MR. Our findings are not in agreement with those of Auxter (1966) who examined muscular fatigue in children 9–11 yrs of age with moderate mental retardation. The author reported that the ability of children with mental retardation to sustain 4–5-s maximal isometric contractions on handgrip dynamometer was significantly lower compared to their typically developing counterparts. At that time, the author stated that in the absence of known physiological differences between children with and without mental retardation, psychological factors should be considered as explanations to these differences. However, since then several physiological differences have been reported between individuals with and without mental retardation, such as disturbed central and peripheral processing components and deformities in the integrity of brain white mater (Davis et al., 1991; LeClair et al., 1993; McRorie & Cooper, 2003; Tan, 1996; Yu et al., 2008). The explanations behind the differences in the ability to resist fatigue between individuals with and without mental retardation are not readily available. However, three of the most prudent hypotheses to explain fatigue differences in individuals with mental retardation might be: (i) the lower ability of individuals with mental retardation to achieve maximal voluntary activation, (ii) the lower absolute forces developed during the fatiguing protocol (Table 1) in individuals with mental retardation, and (iii) the lower reliance on glycolytic metabolism for energy production in individuals with mental retardation as suggested by their lower lactate concentration (Fig. 5). Although, there is scientific evidence that each of the above factors alone may influence the ability of an individual to resist fatigue, the interrelation/interdependence among them is apparent. It has been demonstrated that individuals with poor ability to achieve full activation during a maximal voluntary contraction develop less peripheral fatigue (Nordlund et al., 2004) and longer endurance time during a fatiguing protocol (Yamada et al., 2002). In fact, Nordlund et al. (2004) reported that the level of activation in the first bout of intermittent isometric fatiguing protocol could explain 39% of the peripheral fatigue. The logic behind the above idea is that individuals with a lower ability to achieve full activation will recruit less fast-twitch motor units at the beginning of exercise and therefore have greater ability to sustain the initially generated force and experience less fatigue (Nordlund et al., 2004). Pincivero et al. (2001) also suggested that higher motor unit activation at the beginning of exercise may result in a faster rate of fatigue during an isokinetic protocol. Despite the fact that neither we nor others have assessed the ability of maximal voluntary activation in individuals with mental retardation, there is ample evidence to suggest that they may be classified as a low voluntary activation population. This is supported by several facts collectively. First, individuals with mental retardation demonstrate a low maximal muscular force that is independent of their body dimensions (this study; Horvat et al., 1999). Second, maximal voluntary force depends on the extent of motor unit activation (Gandevia, 2001) and movement coordination (Van Praagh & Dore´, 2002) that are influenced by the development of the CNS and its integration with periphery. Third, in individuals with mental retardation there is damage in the integrity of corpus callosum and corticospinal tract (Yu et al., 2008)—important structures for communication of sensorimotor information and major motor pathway in CNS that transmits the neural drive to motoneurons. Fourth, corticospinal lesions in several pathological conditions impair the voluntary drive (Gandevia, 2001). Further evidence for the disturbed central and peripheral processing components in individuals with mental retardation may be provided by their longer pre-motor and/or motor times (this study; Davis et al., 1991; Horvat et al., 2003) and the associations of intelligence with neural transmission (McRorie & Cooper, 2003) and nerve conduction velocities (Reed et al., 2004; Tan, 1996). In the present study, individuals with mental retardation produced significantly lower absolute forces and total work (Fig. 2) throughout the fatiguing protocol. Furthermore, the rate of decline and fatigue resistance were correlated with total work production in the first set ( 0.90 and 0.53, respectively). These results support the general view that the greater the force exerted, work done or rate of work during a task the more the muscle will fatigue (Enoka & Stuart, 1992). Nordlund et al., 2004 reported that the maximal voluntary torque in the first bout of intermittent fatiguing protocol explained as much as 55% of the peripheral fatigue. The explanation for the inverse relationship between the ability to generate greater absolute forces and fatigue resistance may be linked to muscle fibre composition, muscle metabolism, and the ability of an individual to achieve full activation (activate type II muscle fibres). Lactate concentration was significantly lower in participants with mental retardation; this provides indirect evidence that they relied less on the glycolytic system for energy production. This is in line with Chia et al. (2002) who found lower blood lactate levels in children with mental retardation vs. typically developing children after a Wingate test. It has been discussed that the increased accumulation of by-products of anaerobic metabolism may impair the excitation-contraction coupling and cross-bridges formation (peripheral fatigue), as well as decrease the motoneuron excitability by an increase input of metabolically sensitive group III and IV muscle afferents (central fatigue). However, it should be pointed out that the effect of metabolites on the involvement of group III and IV muscle afferents on decreased motoneuron excitability is still uncertain and controversial effects have been reported for different muscle groups (Martin, Smith, Butler, Gandevia, & Taylor, 2006; Taylor & Gandevia, 2008).
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5. Conclusion In conclusion, the results of this study confirm previous findings that individuals with mental retardation have inferior strength compared to those with typical development. The present study extends the knowledge on neuromuscular function of individuals with mental retardation reporting that they also have limited ability to produce work at high rates during short continuous muscular effort (anaerobic capacity). Thus, exercise training is imperative for individuals with mental retardation since physical fitness (in particular muscular strength) has been related to their productivity in the work settings (Fernhall, 1993) and overall health. This study also provides evidence that albeit individuals with mental retardation have lower maximal performances, they maintain better their maximal strength and anaerobic capacity during an intermittent exercise, suggesting greater recovery potentials after maximal efforts. This supports the general view that the lower the force exerted, work done or rate of work during a task the less the muscle will fatigue (Enoka & Stuart, 1992). However, it should be kept in mind that this ability may not be evident when individuals with mental retardation perform daily tasks that require a specific amount of absolute work because they will be working at higher relative intensities. Insights into the ability of individuals with mental retardation to repeat exercise bouts during intermittent training is important in rehabilitation and sport settings in order to design exercise programs to optimize improvements in physical fitness and in skill acquisition; and to reduce the risk of musculoskeletal injury due to fatigue during training. Yet, the perspective that individuals with mental retardation may be less capable of maximally activate their motoneuron pool appears as an appealing view to explain their different fatigue profile during intermittent exercise. 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