• Users Online: 509
  • Print this page
  • Email this page

 Table of Contents  
Year : 2023  |  Volume : 13  |  Issue : 1  |  Page : 65-71

Force generation and muscle activation of knee extensor and flexor muscles in type 2 diabetes mellitus patients

1 Department of Physical Therapy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
2 Department of Nutrition and Movement Science, Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, The Netherlands
3 Department of Physiotherapy, School of Rehabilitation, Tabriz University of Medical Science, Tabriz, Iran

Date of Submission11-Jun-2021
Date of Decision16-Feb-2022
Date of Acceptance25-Nov-2022
Date of Web Publication27-Mar-2023

Correspondence Address:
Farid Bahrpeyma
Jalal Aleahmad, Nasr, P. O. Box: 14115-111, Tehran
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmss.jmss_129_21

Rights and Permissions

Background: Type 2 diabetes mellitus (T2DM) is associated with decreased muscle force generation. The disturbed force generation process in T2DM could be attributed to either or both agonist and antagonist muscles activation. The present study aims to assess the effects of T2DM on the interaction of antagonist and agonist muscles in the knee joint. Methods: The peak torque, root mean square (RMS) of the SEMG signals, the ratio of torque/RMS, and the interaction of antagonists and agonist muscles were compared between healthy and T2DM patients. Surface ElectroMyoGraphy (SEMG) of knee flexor and extensor muscles were recorded during concentric contraction with an isokinetic dynamometer at 60°/s in 13 T2DM and 12 healthy subjects. The independent sample t-tests were used to compare diabetic and healthy subjects. The significance level was set at 0.05. Results: The antagonist/agonist interaction during maximal extension (P = 0.010) and flexion (P = 0.022) torques of the knee joint showed significantly lower activation of antagonist muscles in T2DM patients than in healthy subjects. Lower knee flexion (41.3%) and extension torques (49.1%) and RMS of agonist and antagonist muscles were observed in T2DM. The torque/RMS ratio (P > 0.05) showed no significant differences in T2DM and healthy subjects. Conclusion: The reduced maximal knee flexor and extensor torques in T2DM are accompanied with the decreased myoelectric activity of corresponding muscles. The related mechanism could be attributed to lower values of antagonist/agonist interaction, which may point out some neural compensatory processes to preserve the functional capacity of the neuromuscular system in T2DM.

Keywords: Force generation, muscle activation, type 2 diabetes mellitus

How to cite this article:
Shahrjerdi S, Bahrpeyma F, C. M. Savelberg HH, Bagherian SA, Jamshidpour B. Force generation and muscle activation of knee extensor and flexor muscles in type 2 diabetes mellitus patients. J Med Signals Sens 2023;13:65-71

How to cite this URL:
Shahrjerdi S, Bahrpeyma F, C. M. Savelberg HH, Bagherian SA, Jamshidpour B. Force generation and muscle activation of knee extensor and flexor muscles in type 2 diabetes mellitus patients. J Med Signals Sens [serial online] 2023 [cited 2023 May 31];13:65-71. Available from: https://www.jmssjournal.net/text.asp?2023/13/1/65/372556

  Introduction Top

Type 2 diabetes mellitus (T2DM) is associated with a gradual loss of muscle strength and power.[1] Decreased muscle strength is a risk factor for functional activities and may decrease the quality of life in T2DM.[2],[3] Functional capacity results from the function of neuromuscular system,[4],[5] that is the force-generating capacity of muscles, the activation of muscles by the neural system, and the tuning of agonistic and antagonistic muscle activation. In people with T2DM, the functional capacity of the neuromuscular system is impaired,[6] various studies investigated impairments at different levels.[7],[8],[9],[10]

Numerous studies reported reduced muscle strength and maximal joint torques in T2DM.[11],[12],[13] Other studies focused on impaired bioelectrical activities of agonist muscles during the maximal or submaximal joint torque generation in T2DM.[14],[15],[16],[17] Decreased agonist activation during maximal force production in T2DM has been well demonstrated.[9],[13],[16] The resultant joint torques are the effect of the mechanical interaction of antagonistic and agonistic muscles. The antagonist and agonist interaction is regulated with the neural strategy of the movement.[18] The magnitude of antagonist and agonist co-contraction during force production is modified in older adults.[19] Despite the pathophysiological changes of the neuromuscular system that arise by T2DM,[6] the magnitude of bioelectrical activities of antagonistic and agonistic muscles during force production is not well documented.

To measure the co-contraction of agonistic and antagonistic muscles, the surface electromyographic (SEMG) of these muscles can be extracted during joint torque generation.[18] The ratio of bioelectrical activities of antagonistic-to-agonistic muscles is a measure for the antagonist/agonist interaction. The co-contraction level provides an indirect estimation of neuromuscular system capacities and characterizes the neuromuscular deficient.[20] We hypothesized that T2DM-related adaptations in the co-contraction of agonistic and antagonistic muscles play a role in the reduced joint torques observed in people with T2DM. Hence, the main goal of the present study was to assess differences in antagonist/agonist interaction of knee flexor and extensor muscles during maximal contraction between short-term T2DM patients and healthy participants.

  Materials and Methods Top

Thirteen T2DM patients (mean ± standard deviation [SD]: age 55.0 ± 6.5 years, weight 79.4 ± 11.5 kg, height 167.0 ± 8.0 cm, body mass index 28.3 ± 3.3 kg/m2, duration of T2DM 6.8 ± 2.1 years, and 58% men) and 12 nondiabetic healthy, well-matched subjects (mean ± SD: age 50.4 ± 6.4 years, weight 77.3 ± 8.7 kg, height 166.0 ± 8.0 cm, body mass index 27.8 ± 1.7 kg/m2, and 58% men) participated in this study. T2DM was clinically diagnosed by an endocrinologist. All patients suffered from T2DM for 4 to 10 years. All patients used oral medications to control diabetes. The T2DM subjects had fasting blood sugar (FBS) between 110 and 150 mg/dl and 2 h after taking 75-g glucose, the oral glucose tolerance test (OGTT) was more than 200 mg/dl. The glycated hemoglobin (HbA1c) was between 7% and 9%.

The well-matched control group had FBS <100 mg/dl, OGTT <130 mg/dl, and HbA1c <5.7%. The Michigan Questionnaire Score, to examine peripheral neuropathy, ranged between 4 and 7 scores for both control and T2DM groups. None of the subjects suffered from central or peripheral neurological or orthopedic diseases, retinopathy, foot ulcers, renal failure, hepatic, respiratory, or cardiovascular diseases. There was no history of regular or professional exercise during the last 6 months. There was no history of drug and alcohol addiction and smoking. If autonomic neuropathy symptoms emerged during tests, participants were excluded from the study. All testing protocols were approved by Tarbiat Modares University ethics committee. All volunteers filled out an informed consent form before participation in the study.

Peak torque evaluation

The knee flexor and extensor concentric peak torques of the dominant leg were evaluated by an isokinetic dynamometer (HUMAC NORM 2009). All participants were asked to flex and extend their knee joint over a range from 0° flexion to 90° of knee flexion (full extension of the knee joint represented 0°). The velocity of isokinetic concentric contraction was adjusted at 60°/s. The tests were performed at the seated position with 90° flexion of hip and knee joints and the ankle was placed at the neutral position. The axis of rotation of the isokinetic dynamometer was aligned with the frontal axis of the knee. The ankle pad was placed above the lateral malleolus. To produce the maximal effort during tests, visual and verbal feedback were given to encourage to generate maximal knee extensor and flexor contraction. The test protocol included five isokinetic concentric contractions with 6 s hold and 120 s rest between each repetition to prevent fatigue. The normalized maximum values of knee extensor and flexor peak torques to weight were considered the test values.

Surface electromyography evaluation

A bipolar multichannel SEMG amplifier (Bayamed Co.www.bayamed.com 2016) was used to record the SEMG activity. SEMG activities of knee flexor muscles including biceps femoris (BF) and medial hamstring (MH) and knee extensor muscles including vastus lateralis (VL), vastus medialis oblique (VMO), and rectus femoris (RF) were recorded during maximal concentric contraction of knee flexor and extensor muscles. Before attaching the SEMG electrodes, the skin was shaved and abraded with alcohol. Pairs of disposable Ag-Ag/Cl electrodes (20 mm inter-electrode distance) were positioned according to Surface Electromyography for the NonInvasive Assessment of Muscles recommendation. The ground electrode was attached to the lateral malleolus of the other leg.

Raw SEMG signals were recorded at a sampling frequency of 1000 Hz during maximal isokinetic concentric contraction. A bandpass filter with low and high cutoff frequencies of 20 and 500 Hz was used. The SEMG signals and isokinetic dynamometer were temporally synchronized with a digital switch and LabVIEW software.[21] The root mean square (RMS) value of the SEMG signals of knee flexor and extensor muscles during isokinetic concentric contraction was calculated and considered the amplitude indicator. The maximal RMS value of five repetitions was considered SEMG output. The RMS values were normalized to isometric maximal voluntary contraction values.[22]

Torque to root mean square Ratio

The proportion of the produced force to the amplitude of SEMG signals could be an estimation of neuromuscular system efficiency.[23] The torque-to-RMS ratio of knee extensor muscles (Torque/RMSEXT) is calculated by dividing the isotonic extension peak torque (PTEXT) by the mean of the RMS of knee extensor muscles. The torque-to-RMS ratio of knee flexor muscles (Torque/ RMSEXT) is obtained from deviation of the isotonic flexion peak torque (PTEXT) by the mean of the RMS of knee flexor muscles.

Where PT is peak torque, x̄ RMSVL+VMO+RF is the mean of the RMS of VL, VMO, and RF muscles, x̄ RMSBF+MH is the mean of the RMS of BF and MH muscles.

Antagonist-to-agonist interaction

Antagonist-to-agonist interaction (AAI) is the ratio of the amplitude of SEMG activity of the antagonist muscles to the agonist muscles during force production.[24] AAI EXT is calculated by the ratio of the mean of the RMS of knee flexor muscles to the mean of the RMS of knee extensor muscles. Furthermore, the ratio of the mean of RMS of knee flexor muscles to the mean of the RMS of knee extensor muscles represents the AAI FLEX.

Where (RMSBF + RMSMH) represents the mean of the RMS of BF and MH muscles, (RMSVL + RMSRF) is the mean of the RMS of VL, VMO, and RF muscles.

Data analysis

We performed independent sample t-tests to compare the demographics and peak joint torques and neuromuscular variables between diabetic and healthy subjects. The significance level was set at 0.05.

  Results Top

Knee extension peak torque (49.1%) and knee flexion peak torques (41.3%) in T2DM subjects were significantly lower than in healthy subjects. RMS of agonist muscles including VL (P = 0.040), vastus medialis oblicus (VMO) (P = 0.009), BF (P = 0.035), and MH (P = 0.001) in participants with T2DM was significantly lower than those in healthy subjects; RMS of RF did not differ significantly between both groups of participants [Table 1] and [Figure 1]a. The RMS of antagonist muscles including VL (P = 0.005), vastus medialis (P = 0.001), RF (P = 0.014), BF (P = 0.001), and MH (P = 0.001) during knee flexion and extension was significantly lower in T2DM than healthy subjects [Table 1] and [Figure 1]b. The torque/RMS ratio of knee extensor and flexor muscles in T2DM and healthy subjects showed no significant differences [Table 1]. The antagonist/agonist interactions during maximal knee extension (P = 0.010) and knee flexion (P = 0.022) in T2DM participants were significantly lower than in healthy subjects.
Table 1: Knee extension and flexion peak torques, root mean square of agonist muscles, root mean square of antagonist muscles, ratio of torque/root mean square of knee extensor and flexor muscles, antagonist/agonist interaction of knee extension and flexion

Click here to view
Figure 1: (a) RMS (a.u.) of knee extensor and flexor agonist muscles in healthy and T2DM, (b) RMS (a.u.) of knee extensor and flexor antagonist muscles in healthy and T2DM. VMO – Vastus medialis oblique; VL – Vastus lateralis; RF – Rectus femoris; MH – Medial hamstring; BF – Biceps femoris; RMS – Root mean square; T2DM – Type 2 Diabetes Mellitus

Click here to view

  Discussion Top

The results showed that the maximal knee extension and flexion torques and the RMS of the knee flexor and extensor muscles in T2DM were significantly lower than in healthy participants. In line with the current study results, previous studies showed that T2DM patients have lower values of knee flexor and extensor peak torques.[12] Hatef et al. showed that lower RMS of agonist muscles is correlated with reduced peak torque in T2DM.[14] The present study results showed that the bioelectrical activity of all knee flexor and extensor muscles in T2DM is less than in healthy subjects except for the activation of the RF. The RF is a biartricular, small, and pinnate muscle which may represent different patterns of electromyography activity.[25] [Figure 1]a and [Figure 1]b show the contribution of agonist and antagonist muscles activity during knee extension and flexion torques. The antagonist muscles activation showed lower RMS in T2DM than in healthy subjects, and no specific pattern of changes between muscles was observed. The results suggest that possibly no discriminate of muscles specific adaptations in T2DM patients occurred.

To answer the question of whether any changes in joint torques are proportional to muscular activation, the ratio of torque/RMS of the agonist muscles was calculated. The proportion of maximal torque to the amplitude of muscular bioelectric activity provides an indirect estimation of neuromuscular system efficiency.[26] Decreased neuromuscular efficiency is attributed to neural and muscular degenerative changes in T2DM.[6] The results showed no significant changes in the torque/RMS ratio of knee extensor and flexor muscles between T2DM and healthy subjects. Preserved torque/RMS ratio in T2DM could be attributed to the absence of neuropathy symptoms and/or short duration of suffering from T2DM in the present study and/or intervention of neural compensatory mechanisms[10] such as agonist/antagonist co-contraction.[27]

Inability to generate maximal torque is attributed to agonist muscles deactivation.[28] In addition, the interaction of agonist and antagonist muscles may interfere in the resultant torque.[29] The primary outcome of the present study showed that the antagonist/agonist interactions of knee flexion and extension in T2DM were lower than in healthy subjects. Indicating that in T2DM, the antagonists to a lesser extent counteract the effect of the agonistic muscles. [Figure 2] illustrates that the reduced antagonist/agonist interaction of knee flexor and extensor muscles in T2DM results from a decreased agonist activation and an even more decreased antagonist activation. Billot et al. (2014) indicated that a higher decline of antagonists muscles activation is necessary to maintaining maximal torque.[20] Błażkiewicz et al. showed that activation of antagonist muscles in the ankle joint during the maximal effort of agonist muscles is decreased in T2DM patients. They indicated that the central nervous system may modulate the antagonist/agonist co-activation in T2DM patients to increase the ability of maximal force-generating.[27]
Figure 2: The mean ± SD of knee antagonist and agonist extensor and flexor muscles activation in diabetic and healthy subjects. SD – Standard deviation

Click here to view

In contrast to the present study results, Petrofsky et al. and Kwon et al. showed higher agonist and antagonist co-contraction in the knee and ankle joints in diabetic patients during gait.[30],[31] Required joint stability is responsible for increased agonist–antagonist co-contraction in T2DM during gait. This inconsistency with our results could be related to differences of the task properties and severity of force production. The magnitude of antagonist activation is dependent on the force level, accuracy, and velocity of movements.[32] Gait is a balance-challenging task, which requires joint stabilization. To facilitate stability and accuracy in gait, high co-activation of antagonist and agonist muscles is required.[33] Whereas the T2DM participants in the present study were assessed in a stable position which intended to achieve maximal force. We suppose antagonist muscle deactivation may occur to indemnify the decreased agonist muscle activation to reach the required maximal force in T2DM patients.

The muscle force generation could be affected by peripheral and central components of movement.[20],[34] The peripheral components including sarcopenia, decreased muscle membrane excitability, and impaired contractile materials may lead to decrease resultant torque. The central control of movements including motor learning, synchronization, and antagonist/agonist interaction could modify the capacity of the entire activation of muscles. The antagonist/agonist interaction provides an indirect estimation of motor control strategies.[35] The antagonist activity during torque generating is preliminary controlled by the neural mechanism of movement.[36] Changed antagonist/agonist interaction in T2DM may modulate the efficacy of force production in these patients.[30] Hence, the reduced antagonist/agonist interaction may preserve the optimal function of the modified neuromuscular system in T2DM.[37]

The specification, methods, and results of similar previous studies are inserted in [Table 2]. The different results could be attributed to subject characteristics and methods differences, therefore, to generalize the present study results, the conditions of the experiment or the specifications of the subjects should be considered. The limitations of SEMG signals recording, processing, and analyzing may interfere with the results.[38] In addition, the biomechanical factor during knee flexion/extension movement including joint angle, gravity effect, muscle length, and momentum of arm may lead to misestimating of findings. To minimize the limitations effects, we normalized the SEMG signals, aligned the dynamometer axis with the axis of rotation of the knee joint, and normalized maximal torques to body weight. On the other hand, this study is one of few studies that investigate the mechanism of force production in T2DM patients. According to previous studies, the mechanism of muscle force generation in diabetic patients is defined by muscle strength and electromyography activities separately.[9],[12],[14] However, the analysis of the force generation mechanism often combines the EMG activity and kinesiology method.[39] The present study innovated an interaction method of bioelectrical muscle activity during muscle force production to estimate the force generation mechanism and muscle activation among T2DM patients.
Table 2: Characteristics of similar previous studies

Click here to view

  Conclusion Top

T2DM patients have decreased resultant torque, lower antagonist/agonist interaction, decreased myoelectric activity of agonist muscle, and higher decreased of antagonist muscles activation. The modified antagonist/agonist interaction in T2DM patients may happen to compensate for insufficient activation of agonist muscles to preserve maximal force generation. The antagonist muscles deactivation may allow T2DM patients to increase their net joint torque to some extent. Although this study provided a preliminary insight into the co-contraction of antagonist and agonist muscles in T2DM, further study is required to explore the exact source of rescued muscle force in T2DM.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Izzo A, Massimino E, Riccardi G, Della Pepa G. A narrative review on sarcopenia in type 2 diabetes mellitus: Prevalence and associated factors. Nutrients 2021;13:183.  Back to cited text no. 1
Leenders M, Verdijk LB, van der Hoeven L, Adam JJ, van Kranenburg J, Nilwik R, et al. Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 2013;14:585-92.  Back to cited text no. 2
Nomura T, Kawae T, Kataoka H, Ikeda Y. Aging, physical activity, and diabetic complications related to loss of muscle strength in patients with type 2 diabetes. Phys Ther Res 2018;21:33-8.  Back to cited text no. 3
Clamann HP. Motor unit recruitment and the gradation of muscle force. Phys Ther 1993;73:830-43.  Back to cited text no. 4
Moura BM, Sakugawa RL, Orssatto LB, de Lima LA, Pinto RS, Walker S, et al. Functional capacity improves in-line with neuromuscular performance after 12 weeks of non-linear periodization strength training in the elderly. Aging Clin Exp Res 2018;30:959-68.  Back to cited text no. 5
Orlando G, Balducci S, Bazzucchi I, Pugliese G, Sacchetti M. Neuromuscular dysfunction in type 2 diabetes: Underlying mechanisms and effect of resistance training. Diabetes Metab Res Rev 2016;32:40-50.  Back to cited text no. 6
Sacchetti M, Balducci S, Bazzucchi I, Carlucci F, Scotto di Palumbo A, Haxhi J, et al. Neuromuscular dysfunction in diabetes: Role of nerve impairment and training status. Med Sci Sports Exerc 2013;45:52-9.  Back to cited text no. 7
Sardar MH, Hossain MM, Hossain MZ, Bari A. Study on neuromuscular manifestations in patients with diabetes mellitus - a study of 100 cases. Journal of Dhaka Medical College, 2015;23:84-8. https://doi.org/10.3329/jdmc.v23i1.22700.  Back to cited text no. 8
Bazzucchi I, De Vito G, Felici F, Dewhurst S, Sgadari A, Sacchetti M. Effect of exercise training on neuromuscular function of elbow flexors and knee extensors of type 2 diabetic patients. J Electromyogr Kinesiol 2015;25:815-23.  Back to cited text no. 9
Shahrjerdi S, Bahrpeyma F, Savelberg HH, Mohajeri-Tehrani MR. Effect of a 6-week strength-training program on neuromuscular efficiency in type 2 diabetes mellitus patients. Diabetol Int 2020;11:376-82.  Back to cited text no. 10
Almurdhi MM, Reeves ND, Bowling FL, Boulton AJ, Jeziorska M, Malik RA. Reduced lower-limb muscle strength and volume in patients with type 2 diabetes in relation to neuropathy, intramuscular fat, and vitamin d levels. Diabetes Care 2016;39:441-7.  Back to cited text no. 11
IJzerman TH, Schaper NC, Melai T, Meijer K, Willems PJ, Savelberg HH. Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life. Diabetes Res Clin Pract 2012;95:345-51.  Back to cited text no. 12
Hatef B, Bahrpeyma F, Mohajeri Tehrani MR. The comparison of muscle strength and short-term endurance in the different periods of type 2 diabetes. J Diabetes Metab Disord 2014;13:22.  Back to cited text no. 13
Hatef B, Ghanjal A, Meftahi GH, Askary-Ashtiani A. Isokinetic and electromyographic properties of muscular endurance in short and long-term type 2 diabetes. Glob J Health Sci 2016;8:54366.  Back to cited text no. 14
Watanabe K, Gazzoni M, Holobar A, Miyamoto T, Fukuda K, Merletti R, et al. Motor unit firing pattern of vastus lateralis muscle in type 2 diabetes mellitus patients. Muscle Nerve 2013;48:806-13.  Back to cited text no. 15
Butugan MK, Sartor CD, Watari R, Martins MC, Ortega NR, Vigneron VA, et al. Multichannel EMG-based estimation of fiber conduction velocity during isometric contraction of patients with different stages of diabetic neuropathy. J Electromyogr Kinesiol 2014;24:465-72.  Back to cited text no. 16
Savelberg HH, Ilgin D, Angin S, Willems PJ, Schaper NC, Meijer K. Prolonged activity of knee extensors and dorsal flexors is associated with adaptations in gait in diabetes and diabetic polyneuropathy. Clin Biomech (Bristol, Avon) 2010;25:468-75.  Back to cited text no. 17
Kellis E. Quantification of quadriceps and hamstring antagonist activity. Sports Med 1998;25:37-62.  Back to cited text no. 18
Hortobágyi T, Devita P. Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 2006;34:29-35.  Back to cited text no. 19
Billot M, Duclay J, Simoneau-Buessinger EM, Ballay Y, Martin A. Is co-contraction responsible for the decline in maximal knee joint torque in older males? Age (Dordr) 2014;36:899-910.  Back to cited text no. 20
Schwartz FP, Bottaro M, Celes R, Pereira MC, Rocha Júnior Vde A, Nascimento FAO, et al. Study of muscle fatigue in isokinetic exercise with estimated conduction velocity and traditional electromyographic indicators. Rev Bras de Engenharia Biomédica 2014;30:312-21.  Back to cited text no. 21
Sousa AS, Tavares JM. Surface electromyographic amplitude normalization methods: A review. In: Electromyography: New Developments, Procedures and Applications. Nova Science Publishers: Hauppauge, NY, US; 2012.  Back to cited text no. 22
Arabadzhiev TI, Dimitrov VG, Dimitrova NA, Dimitrov GV. Interpretation of EMG integral or RMS and estimates of “neuromuscular efficiency” can be misleading in fatiguing contraction. J Electromyogr Kinesiol 2010;20:223-32.  Back to cited text no. 23
Ervilha UF, Graven-Nielsen T, Duarte M. A simple test of muscle coactivation estimation using electromyography. Braz J Med Biol Res 2012;45:977-81.  Back to cited text no. 24
Disselhorst-Klug C, Schmitz-Rode T, Rau G. Surface electromyography and muscle force: Limits in sEMG-force relationship and new approaches for applications. Clin Biomech (Bristol, Avon) 2009;24:225-35.  Back to cited text no. 25
Aragão FA, Schäfer GS, de Albuquerque CE, Vituri RF, de Azevedo FM, Bertolini GR. Neuromuscular efficiency of the vastus lateralis and biceps femoris muscles in individuals with anterior cruciate ligament injuries. Rev Bras Ortop 2015;50:180-5.  Back to cited text no. 26
Błażkiewicz M, Sundar L, Healy A, Ramachandran A, Chockalingam N, Naemi R. Assessment of lower leg muscle force distribution during isometric ankle dorsi and plantar flexion in patients with diabetes: A preliminary study. J Diabetes Complications 2015;29:282-7.  Back to cited text no. 27
Appell HJ, Forsberg S, Hollmann W. Satellite cell activation in human skeletal muscle after training: Evidence for muscle fiber neoformation. Int J Sports Med 1988;9:297-9.  Back to cited text no. 28
Kubo K, Tsunoda N, Kanehisa H, Fukunaga T. Activation of agonist and antagonist muscles at different joint angles during maximal isometric efforts. Eur J Appl Physiol 2004;91:349-52.  Back to cited text no. 29
Petrofsky JS, Macnider M, Navarro E. Motor control and gait characteristics in people with type 1 and type 2 diabetes without sensory impairment in the foot. Basic Appl Myol 2005;15:75-86.  Back to cited text no. 30
Kwon OY, Minor SD, Maluf KS, Mueller MJ. Comparison of muscle activity during walking in subjects with and without diabetic neuropathy. Gait Posture 2003;18:105-13.  Back to cited text no. 31
Pincivero DM, Polen RR, Byrd BN. Contraction mode and intensity effects on elbow antagonist muscle co-activation. J Electromyogr Kinesiol 2019;44:101-7.  Back to cited text no. 32
Hortobágyi T, Solnik S, Gruber A, Rider P, Steinweg K, Helseth J, et al. Interaction between age and gait velocity in the amplitude and timing of antagonist muscle coactivation. Gait Posture 2009;29:558-64.  Back to cited text no. 33
Clark DJ, Fielding RA. Neuromuscular contributions to age-related weakness. J Gerontol A Biol Sci Med Sci 2012;67:41-7.  Back to cited text no. 34
Frey-Law LA, Avin KG. Muscle coactivation: A generalized or localized motor control strategy? Muscle Nerve 2013;48:578-85.  Back to cited text no. 35
Feldman AG, Levin MF, Garofolini A, Piscitelli D, Zhang L. Central pattern generator and human locomotion in the context of referent control of motor actions. Clin Neurophysiol 2021;132:2870-89.  Back to cited text no. 36
Krishnan C, Williams GN. Variability in antagonist muscle activity and peak torque during isometric knee strength testing. Iowa Orthop J 2009;29:149-58.  Back to cited text no. 37
Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol (1985) 2004;96:1486-95.  Back to cited text no. 38
Kostyukov AI, Tomiak T. The force generation in a two-joint arm model: Analysis of the joint torques in the working space. Front Neurorobot 2018;12:77.  Back to cited text no. 39


  [Figure 1], [Figure 2]

  [Table 1], [Table 2]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
   Materials and Me...
   Article Figures
   Article Tables

 Article Access Statistics
    PDF Downloaded10    
    Comments [Add]    

Recommend this journal