Individuals with intellectual disability have lower voluntary muscle activation level

Research in Developmental Disabilities 35 (2014) 3574–3581

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Individuals with intellectual disability have lower voluntary

Rihab Borji a,*, Firas Zghal b, Nidhal Zarrouk c, Sonia Sahli a, Haithem Rebai a

a Unite de Recherche Education, Motricite, Sports et sante, Institut Superieur du Sport et de l’Education Physique de Sfax, Universite de Sfax,

Tunisiab Laboratoire Adaptations Metaboliques a l’Exercice en Conditions Physiologiques et Pathologiques (AME2P, EA 3533), Universite Blaise

Pascal, Clermont-Ferrand, Francec Laboratoire des techniques d’imagerie medicale (LR 12ES06, LTIM), Faculte de Medicine de Monastir, Universite de Monastir, Tunisia

A R T I C L E I N F O

Article history:

Received 6 June 2014

Received in revised form 26 August 2014

Accepted 28 August 2014

Available online

Keywords:

Intellectual disability

Electrical stimulation

Twitch interpolation technique

Voluntary activation level

Knee extensor muscles

A B S T R A C T

The aim of this study was to explore the voluntary activation level during maximal

voluntary contraction (MVC) in individuals with intellectual disability (ID) versus

individuals without ID using the twitch interpolation technique. Ten individuals with mild

ID (ID group) and 10 sedentary men without ID (control group) participated in this study.

The evaluation of neuromuscular function consisted in three brief MVCs (3 s) of the knee

extension superimposed with electrical nerve stimulation (NES) to measure voluntary

activation. Muscle activity levels were also measured with surface EMG. The root mean

square (RMS) was extracted from the EMG signal. The RMS/Mmax ratio and the

neuromuscular efficiency (NME) were calculated. Our results reported that individuals

with ID present lower muscle strength (p< 0.001), lower voluntary activation level

(p< 0.001), lower RMS values of vastus lateralis (p< 0.05), vastus medialis (p< 0.05), and

rectus femoris (p< 0.001) muscles. In addition, our results showed lower RMS/Mmax

values in the ID group than in the control group for the VM (0.05� 0.01 mV vs.

0.04� 0.01 mV; p< 0.05) and the RF (0.06� 0.02 mV vs. 0.05� 0.02 mV; p< 0.05) muscles.

However, no significant difference was reported for the VL muscle (0.05� 0.02 mV vs.

0.05� 0.02 mV; p = 0.463). Moreover, Individuals with ID present smaller potentiated twitch

(p< 0.001). However, no significant difference was reported in the NME ratio. These results

suggest that the lower muscle strength known in individuals with ID is related to a central

nervous system failure to activate motor units and to some abnormal intrinsic muscle properties.

It seems that the inactive lifestyle adopted by individuals with ID is one of the most important

factors of their lower voluntary activation levels. Therefore, physical activities should be

introduced in life style of individuals with ID to improve their neuromuscular function.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Individuals with intellectual disabilities (ID) present several abnormalities in their nervous system structure(Gabrielli et al., 1998) localized in the white matter tracts that are responsible for the processing of sensory and motor

* Corresponding author at: Institut Superieur de Sport et de l’Education Physique de Sfax, Route de l’Aerodrome, Km 3.5, BP 1068, 3000 Sfax, Tunisia.

Tel.: +216 22092322.

E-mail addresses: [email protected] (R. Borji), [email protected] (F. Zghal), [email protected] (N. Zarrouk),

[email protected] (S. Sahli), [email protected] (H. Rebai).

http://dx.doi.org/10.1016/j.ridd.2014.08.038

0891-4222/� 2014 Elsevier Ltd. All rights reserved.

R. Borji et al. / Research in Developmental Disabilities 35 (2014) 3574–3581 3575

information (Yu et al., 2008). Several studies have mentioned that individuals with ID present several abnormalities inmotor nervous control and neuromuscular coordination (Chia, Lee, & Teo-Koh, 2002). In addition, individuals with IDpresent lower muscle strength compared to individuals without ID (Angelopoulou, Tsimaras, Christoulas, Kokaridas, &Mandroukas, 1999; Blomqvist, Olsson, Wallin, Wester, & Rehn, 2013; Borji, Sahli, Zarrouk, Zghal, & Rebai, 2013; Carmeli,Ayalon, Barchad, Sheklow, & Reznick, 2002; Horvat, Croce, Pitetti, & Fernhall, 1999). Moreover, in a previous study, wedemonstrated that individuals with ID present lower root mean square (RMS) value in comparison with individualswithout ID (Borji et al., 2013). Nevertheless, the reason for this force deficiency has not been identified yet.

In individuals without ID, it has been demonstrated that muscle force level depends on several factors such as muscularfiber typology (Fitts & Widrick, 1996), training status (Fitts & Widrick, 1996), sex difference (Miller, MacDougall,Tarnopolsky, & Sale, 1993), and age difference (Lindle et al., 1997). Muscle force level depends also on neural mechanismssuch as the voluntary activation level of motor units (Gandevia, 2001, 1992). Voluntary activation describes the level ofneural drive of muscle during voluntary contractions (Gandevia, Allen, & McKenzie, 1995). One of the methods to evaluatethe activation of motor units by the central nervous system is the superimposed twitch technique (Gandevia, 2001; Milletet al., 2012). The presence of a superimposed twitch produced by motor nerve stimulation during a MVC indicates that thewhole motor units are not totally recruited by the central nervous system (Merton, 1954). If voluntary activation isincomplete, failure to drive the muscle should occur at or above the site of stimulation of the motor axons (Merton, 1954).

Using this technique, many studies have attempted to investigate the relationship between the reduced voluntary forceproduction and the voluntary activation levels in general population (Belanger & McComas, 1981; Bigland-Ritchie, Donovan, &Roussos, 1981), athletic population (Huber, Suter, & Herzog, 1998), and clinical populations (Hurley, Jones, & Newham, 1994;Rutherford, Jones, & Newham, 1986). Studies investigating this relationship in elderly persons and individuals with cerebralpalsy found that the lower muscle force noted in both populations had been related to the activation deficit (AD) from centralnervous system (Stackhouse et al., 2001; Stackhouse, Binder-Macleod, & Lee, 2005; Yue, Ranganathan, Siemionow, Liu, & Sahgal,1999). Nevertheless, to our knowledge no data is available about the voluntary activation in individuals with ID.

Thus, the aims of this study were to compare the force production and the level of voluntary activation betweenindividuals with ID and individuals without ID as well as to investigate the implication of the central nervous systemdeficiency in the force production in individuals with ID.

2. Methods

2.1. Participants

The sample population consisted of 20 sedentary men who met the same criteria in terms of socioeconomic status andethnicity. Ten men with ID (age = 24.9� 4.9 years; height = 1.7� 0.1 m; weight = 77.9� 8.3 kg; BMI = 25.7� 2.5 kg/m2)participated in the study as an experimental group. The control group consisted of 10 sedentary and healthy (no cardiovascular,metabolic, immunologic, or neuromuscular disorders) men without ID matched for age, height, and weight:(age = 25.2 � 2.7 years; height = 1.7 � 0.1 m; weight = 75.3 � 9.2 kg; BMI = 23.9 � 1.7 kg/m2).

All participants with ID suffered from a mild ID with an intelligence quotient (IQ) between 50 and 55 and 70 (TheAmerican Psychiatric Association, 2000) determined by the WAIS-IV test (Wechsler, 2008) elaborated by the educationalcenter psychologist (IQ = 62� 3.5). Participants with ID have been recruited randomly from the Tunisian Union of Aid to MentalInsufficiency (TUAMI). The sample excluded individuals with down syndrome, and with multiple disabilities. The participant’smorphological characteristics showed no statistical differences in terms of age, weight, height and BMI between the two groups.The participants were fully informed of the procedure and the risks involved and gave their written consent. The informed consentfor the individuals with ID was provided by their parents or legal guardians.

2.2. Study design

Three days after a familiarization session with the experimental procedures, participants engaged in the experimentalsession. The experimental session was preceded by a warm-up consisting of several submaximal contractions (12–15) ofknee extension muscles at a freely chosen intensity. The evaluation of neuromuscular function consisted in three brief (3 s)maximal voluntary contractions (MVCs) of the knee extension superimposed with nerve electrical stimulation (NES) tomeasure voluntary activation. Muscle activity levels were also measured with surface electromyography (EMG). To excludethe confounding effect of fatigue induced by repeated muscular contractions, the three MVCs were separated by a 2-minrecovery period. The comparison of data obtained during the first and the third MVC did not reveal any significant difference,suggesting that the experimental procedures did not induce any fatigue.

2.3. Testing procedures and instrumentation

2.3.1. Force measurement

The participants performed three MVCs with strong encouragement by the investigator. During testing, the participantswere seated on an isometric dynamometer (Good Strength, Metitur, Finland) equipped with a cuff attached to a strain gauge.This cuff was adjusted �2 cm above the lateral malleolus using a Velcro strap. The participants stabilized themselves by

R. Borji et al. / Research in Developmental Disabilities 35 (2014) 3574–35813576

grasping handles on the side of the chair during contractions. Safety belts were strapped across the chest, thighs and hips toavoid lateral, vertical or frontal displacements. All measurements were taken from the participant’s dominant leg, with thehip and knee angles set at 908 from full extension (= 08). All participants in our study presented the right leg as the dominantleg (determined by the leg used to kick a ball).

2.3.2. Electromyographic recordings

The EMG signals of the vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) muscles were recorded usingbipolar silver chloride surface electrodes (Blue Sensor N-00-S, Ambu, Denmark) during MVC and stimulations. The recordingelectrodes were taped lengthwise on the skin over the muscle belly following SENIAM recommendations (Hermens, Feriks,Disselhorst-Klug, & Rau, 2000), with an inter-electrode distance of 20 mm. The position of the electrodes was marked on theskin in case they needed to be repositioned during the experiment. The reference electrode was attached to the patella. Lowimpedance (Z< 5 kV) at the skin-electrode surface was obtained by shaving, abrading the skin with thin sand paper andcleaning with alcohol. EMG signals were amplified (Octal Bio Amp ML 138, ADInstruments, Australia) with a bandwidthfrequency ranging from 10 Hz to 1 kHz (common mode rejection ratio> 96 dB, gain = 1000) and simultaneously digitizedtogether with the force signals using an acquisition card (Powerlab 16SP, ADInstruments, Australia) and Labchart7.0 software (ADInstruments, Australia). The sampling frequency was 2 kHz. MVC force was determined as the peak forcereached during maximal efforts. RMS values of the VL, VM and RF EMG activities were calculated during the MVC trials over a0.5 s period after the force had reached a plateau and before the superimposed stimulation was evoked.

Neuromuscular efficiency (NME) was calculated as the ratio of peak force to the sum RMS of the VL, RF, and VM muscles toprovide an overall representation of quadriceps muscle group activity (Deschenes et al., 2002; Woods & Bigland-Ritchie,1983; Zarrouk et al., 2012).

2.3.3. Peripheral nerve stimulation (NES)

The twitch interpolation method, proposed by Merton (1954), involves interpolation of a single supramaximal electricalstimulus to the motor nerve during MVC. Voluntary activation is thus quantified by comparing the amplitude of thesuperimposed twitch with the force evoked by the same stimulus intensity at rest, and immediately following thecorresponding MVC (Kufel, Pineda, & Mador, 2002). The femoral nerve was stimulated percutaneously with a single square-wave stimulus of 1 ms duration with maximal voltage of 400 V delivered by a constant current stimulator (Digitimer DS7A,Hertfordshire, United Kingdom). The cathode (self-adhesive electrode: Ag–AgCl, 10 mm diameter) was positioned in thefemoral triangle and pressed firmly into place by an experimenter. The anode, a 10� 5 cm self-adhesive stimulationelectrode (Medicompex SA, Ecublens, Switzerland) was placed midway between the greater trochanter and the iliac crest.Optimal stimulation intensity was determined from M-wave and force measurements before each testing session. Briefly,the stimulation intensity was increased by 5 mA until there was no further increase in either peak twitch force (i.e., thehighest value of the knee extension twitch force was reached) or in concomitant VL, VM and RF peak-to-peak M-waveamplitudes (Mmax). During the subsequent testing procedures, the intensity was set to 150% of the optimal intensity toovercome the potential confounding effect of axonal hyperpolarization (Burke, 2002). MVC superimposed with NES wereused to calculate the voluntary activation level as follows:

Voluntary activation ð%Þ ¼ 1� superimposed twitch

potentiated twitch

� �� 100

where ‘‘superimposed twitch’’ is the amplitude of the twitch evoked with NES during MVC and ‘‘potentiated twitch’’ is theamplitude of the twitch evoked by a single stimulation delivered 3 s after the end of the MVC. This provided the opportunityto obtain a potentiated mechanical response and so reduce the variability in voluntary activation values (Kufel et al., 2002).The ID group AV was calculated as follows:

AV ð%Þ ¼ 1� voluntary activation of ID group

voluntary activation of control group

� �� 100

2.4. Statistical analysis

All data are presented as means� SD and were analyzed by the Statistica for Windows software (version 6.0, StatSoft, Inc.,Tulsa, OK). Data distribution normality was confirmed with the Shapiro–Wilk W-test. Independent sample t-tests were executedin order to analyze group differences in characteristics (age, height, weight and BMI), MVC, voluntary activation, potentiatedresting twitch, RMS, RMS/Mmax and NME values. The level of significance for all statistical analyses was set at p< 0.05.

3. Results

3.1. Mechanical responses

The independent sample t-test demonstrated a significant (p< 0.001) difference in MVC between ID group and controlgroup. Individuals with ID demonstrated lower maximal force producing capacity (439.6� 62.7 N vs. 704.1� 125.4 N; Fig. 1).

[(Fig._1)TD$FIG]

MVC

(N)

0

100

200

300

400

500

600

700

800

900

Controls ID

Fig. 1. Mean (� SD) values of maximal voluntary contraction (MVC) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant

difference at p< 0.001.

[(Fig._2)TD$FIG]

Volu

ntar

y A

ctiv

atio

n Le

vel N

ES (%

)

0

10

20

30

40

50

60

70

80

90

100

Contrrols ID

Fig. 2. Mean (� SD) values of voluntary activation level for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference

at p< 0.001.

[(Fig._3)TD$FIG]

0

50

100

150

200

250

Pote

ntia

ted

Rest

ing

Twitc

h (N

)

Controols ID

Fig. 3. Mean (� SD) values of potentiated resting twitch (PRT) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant

difference at p< 0.001.

R. Borji et al. / Research in Developmental Disabilities 35 (2014) 3574–3581 3577

Table 1

Root mean square (RMS), RMS/Mmax values of the vastus lateralis (VL), vastus medialis (VM), and rectus femoris (FR) muscles and neuromuscular efficiency

(NME) ratio for individuals with intellectual disability (ID group) and those without ID (controls).

Control group (n = 10)

Mean (SD)

ID group (n = 10)

Mean (SD)

Independent t-tests (p-value)

RMS VL (mV) 0.42 (0.15) 0.27 (0.15) 2.13 (0.046)*

RMS VM (mV) 0.51 (0.22) 0.29 (0.07) 2.79 (0.012)*

RMS RF (mV) 0.47 (0.17) 0.29 (0.06) 3.02 (0.007)***

RMS/Mmax VL (mV) 0.05 (0.02) 0.05 (0.02) 0.74 (0.463)

RMS/Mmax VM (mV) 0.05 (0.01) 0.04 (0.01) 2.59 (0.018)*

RMS/Mmax RF (mV) 0.06 (0.02) 0.05 (0.02) 2.55 (0.020)*

NME 536.8 (158.7) 539.3 (144.7) �0.03 (0.970)

* Significant differences at p< 0.05.

*** Significant differences at p< 0.001.

R. Borji et al. / Research in Developmental Disabilities 35 (2014) 3574–35813578

In addition, the independent sample t-test indicated a significant (p< 0.001) differences for both voluntary activation andpotentiated resting twitch between the ID group and the control group. Individuals with ID presented lower voluntary activationlevel (65.8� 8.0% vs. 85.6� 5.0%; Fig. 2) and potentiated resting twitch (115.8� 18.9 N vs. 186.3� 24.3 N; Fig. 3).

3.2. EMG responses

The independent sample t-test indicated significantly lower RMS values in the ID group than the control group for the VL(0.27� 0.15 mV vs. 0.42� 0.15 mV; p< 0.05), the VM (0.29� 0.07 mV vs. 0.51� 0.22 mV; p< 0.05), and the RF (0.29� 0.06 mVvs. 0.47� 0.17 mV; p< 0.001) muscles. Moreover, the independent sample t-test indicated significantly lower RMS/Mmax valuesin the ID group than the control group for the VM (0.05� 0.01 mV vs. 0.04� 0.01 mV; p< 0.05) and the RF (0.06� 0.02 mV vs.0.05� 0.02 mV; p< 0.05) muscles. However, no significant difference was reported for the VL muscle (0.05� 0.02 mV vs.0.05� 0.02 mV; p = 0.463; Table 1). Concerning the NME ratio, the independent sample t-test indicated no significant differencebetween the ID group and the control group (539.3� 144.7 vs.536.8� 158.7; p = 0.97; Table 1).

4. Discussion

The aims of this study were to compare the force production and the level of voluntary activation between individualswith ID and individuals without ID as well as to investigate the implication of the central nervous system deficiency in theforce production in individuals with ID. Our results showed that individuals with ID develop lower MVC than individualswithout ID. This result is consistent with previous studies investigating muscle force level in sedentary individuals with ID(Angelopoulou et al., 1999; Borji et al., 2013; Carmeli et al., 2002; Croce, Pitetti, Horvat, & Miller, 1996; Horvat et al., 1999;Pitetti & Boneh, 1995; Zafeiridis et al., 2010). Besides, smaller differences in force level were reported when comparing eliteathletes with ID to physical education students without ID (van de Vliet et al., 2006). Moreover, it has been demonstratedthat, in individuals without ID, the muscle force level depends on the training status (Fitts & Widrick, 1996) and thevoluntary activation level (Gandevia, 2001, 1992).

The main result of our study showed that individuals with ID have lower ability to activate motor units than individualswithout ID. They were only able to activate 65% of their motor units versus 85% in the control group. Moreover, our ID grouppresents an AD of 23.13% compared with the control group. Even in individuals without ID, it is well known that the centralnervous system fails to generate maximal evocable force (Gandevia, 2001; Strojnik, 1995). Therefore, concerning our controlgroup, our results were in agreement with those of Shield and Zhou (2004) who found that the quadriceps voluntaryactivation was between 85% and 95% of total motor units in sedentary individuals without ID. Moreover, Babault, Pousson,Ballay, and Van Hoecke (2001) found that the mean activation levels during MVC are 95.2% in individuals practicing regularphysical activities. Unfortunately, no data are available concerning the voluntary activation level in individuals with ID.Nevertheless, the AD in the ID group is similar in magnitude to deficits reported for the quadriceps femoris in someindividuals with central nervous system disorders. This AD was at 25–40% in adults after a stroke (Newham & Hsiao, 2001), at25% in individuals with multiple sclerosis (de Haan, de Ruiter, van der Woude, & Jongen, 2000), and at 33% in individuals withcerebral palsy (Stackhouse et al., 2005). The voluntary activation failure could be explained by the several central nervoussystem abnormalities. It has been documented that individuals with ID present a failure of growth and maturation in brainareas during the developmental years (Gabrielli et al., 1998). Post-mortem neuropathological studies in ID showed severalalterations in the cerebral cortex structure and in the hippocampus and a reduction in the number of neurons (Dierssen &Ramakers, 2006). Individuals with ID present also dendritic abnormalities (Dierssen & Ramakers, 2006; Fodale, Mafrica,Caminiti, & Grasso, 2006), and neurotransmitter system dysfunction with abnormal neuronal connectivity, resulting indeficient information processing (Kaufmann & Moser, 2000). They present also several abnormalities localized in the whitematter tracts that are responsible for the motor function (Yu et al., 2008). The maturational differences in neuromuscularfunction could be also responsible for the lower central activation level in individuals with ID. Therefore, while ourindividuals with ID sample are adults (24.9� 4.9 years), they demonstrated a voluntary activation level comparable with that

R. Borji et al. / Research in Developmental Disabilities 35 (2014) 3574–3581 3579

demonstrated by children without ID (65% vs. 68% respectively) as it has been reported by O’Brien, Reeves, Baltzopoulos, Jones,and Maganaris (2009). In fact, ID is defined as a condition of arrest or incomplete development of the mind, which does not onlyaffect cognitive functions, but motor functions as well (World Health Organization, 2007). An inactive lifestyle could be animportant factor of this lower central voluntary activation because individuals with ID are less active than general population(Hall & Thomas, 2008). For instance, it has been shown that sedentary individuals without ID have lower voluntary activation thantrained ones (Yamada, Kaneko, & Masuda, 2002).

Our results showed that individuals with ID present a lower potentiated resting twitch than individuals without ID, whichmeans that they have less muscle volume than individuals without ID. Although muscle size or volume was not directlymeasured in the present study, the reduced MVC is probably due to muscle atrophy usually reported in individuals with ID(Fryns et al., 1993; Hino-Fukuyo et al., 2006; Van’t Padje et al., 2009), which could be attributed to the inactive lifestyle.Moreover, it seems reasonable to expect that intrinsic muscle properties disorders such as reduced sarcolemmal and/or T-tubules excitability and reduced release of Ca++ from SR may additionally contribute to the lower potentiated twitchreported in individuals with ID. In fact, it has been documented that individuals with ID demonstrate different muscle lacticprofile compared to individuals without ID during maximal effort (Chia et al., 2002; Zafeiridis et al., 2010).

In the present study, individuals with ID present lower RMS and RMS/Mmax values during MVC than individuals withoutID. Nevertheless, no significant difference in the NME ratio was noted between individuals with and without ID. In fact, theNME was defined as ‘‘the responsiveness of muscle to neural excitation’’ (Deschenes et al., 2002). This result suggests that thelower force level is not resulting from functional muscle abnormalities but is related to neural factors. Our results are in linewith our previous study (Borji et al., 2013). In this previous study we have reported that, in spite of their lower MVC andlower RMS values, individuals with ID present similar NME values with individuals without ID. Moreover, some studiesestablished a relationship between muscle force level and different incapacities in individuals with ID such as cardiovascularreduced capacities (Pitetti & Boneh, 1995), and lower anaerobic power (Chia et al., 2002; Zafeiridis et al., 2010). In addition,some studies demonstrated that the force deficit in individuals with ID is strongly related to the degree of hypotonia reportedin these individuals (Morris, Vaughan, & Vacarro, 1982).

There are some limitations that should be addressed. First, while statistical analysis demonstrated no significantdifference on BMI between groups, we have not measured the % of body fat for both groups. In this context, it should benoted, that EMG signal may be affected by body fat and skinfold thickness individual differences (Nordander et al., 2003).Second, the original twitch interpolation technique described by Merton (1954) and subsequently employed by many others(Belanger & McComas, 1981; Bigland-Ritchie, Furbush & Woods, 1986) involved a single stimulus interpolated overvoluntary contractions. However, recently, it has become common for two or more stimuli (50–100 Hz) to be employedbecause the evoked force increments are larger and more readily detected (Strojnik, 1995; Suter & Herzog, 2001). Moreover,it has been reported that supramaximal twin, triple and quadruple stimuli (at 125 Hz) evoke less variable force incrementsthan single stimuli (Suter & Herzog, 2001). Finally, although the twitch interpolation technique is an efficient technique toexplore voluntary activation, spinal and supraspinal contributions on the AD in individuals with ID are still unknown. Futurestudy should explore cortical activation in individuals with ID during exercise using the transcranial magnetic stimulation.

5. Conclusion

The results of our study showed that individuals with ID have lower ability to activate their motor units. Moreover, ourstudy showed a muscle structure difference between individuals with and without ID. These results could have importantimplications for coaches of ID athletes. They should focus on neuromuscular function improvement in order to increase thenervous system efficiency to activate motor unit. As in individuals without ID, neuromuscular function and muscle structureimprovement could be possible in individuals with ID by inserting strength training program in their physical activities.

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgements

The authors would like to thank all participants for their understanding and availability. Special gratitude is due to allcollaborating and volunteers of the Tunisian Union of Aid to Mental Insufficiency (TUAMI) for their contribution in this study.

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