Variability in Muscle Adaptation to Electrical Stimulation

Abstract

The aims were to investigate the plasticity of the myosin heavy chain (MHC) phenotype following neuromuscular electrical stimulation (NMES) and to assess the correlation between MHC isoform distribution and muscle fibre conduction velocity (MFCV).

14 men were subjected to 24 sessions of quadriceps NMES. Needle biopsies were taken from the dominant vastus lateralis and neuromuscular tests were performed on the dominant thigh before and after training. NMES significantly increased the quadriceps maximal force by 14.4±19.7% (P=0.02), vastus lateralis thickness by 10.7±8.6% (P=0.01), vastus lateralis MFCV by 11.1±3.5% (P<0.001), vastus medialis MFCV by 8.4±1.8% (P<0.001). The whole spectrum of possible MHC isoform adaptations to training was observed: fast-to-slow transition (4 subjects), bi-directional transformation from MHC-1 and MHC-2X isoforms toward MHC-2A isoform (7 subjects), shift toward MHC-2X (2 subjects), no MHC distribution change (1 subject). No significant correlation was observed between MHC-2 relative content and vastus lateralis MFCV (pre-training: R²=0.04, P=0.46; post-training: R²=0.02, P=0.67). NMES elicited distinct adaptations in the MHC composition and increased force, muscle thickness, and MFCV. The MHC isoform distribution did not correlate with MFCV, thus implying that the proportion of different fibre types cannot be estimated from this electrophysiological variable.

Key words

electromyography - myosin heavy chain ­distribution - muscle fibre conduction velocity - muscle thickness - neuromuscular electrical stimulation

• References

• 1 Bamman MM, Petrella JK, Kim JS, Mayhew DL, Cross JM. Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans. J Appl Physiol 2007; 102: 2232-2239
• 2 Bland JM, Altman DG. Calculating correlation coefficients with repeated observations: Part 1 – Correlation within subjects. BMJ 1995; 310: 446
• 3 Blijham PJ, Drost G, Stegeman DF, Zwarts MJ. Reduced muscle-fibre conduction but normal slowing after cold exposure in paramyotonia congenita. Muscle Nerve 2008; 37: 23-26
• 4 Blijham PJ, ter Laak HJ, Schelhaas HJ, van Engelen BG, Stegeman DF, Zwarts MJ. Relation between muscle fibre conduction velocity and fibre size in neuromuscular disorders. J Appl Physiol 2006; 100: 1837-1841
• 5 Bottinelli R, Reggiani C. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 2000; 73: 195-262
• 6 D’Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R, Rossi R, Moro G, Miotti D, Canepari M, Bottinelli R. Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol 2006; 570: 611-627
• 7 Delitto A, Brown M, Strube MJ, Rose SJ, Lehman RC. Electrical stimulation of quadriceps femoris in an elite weight lifter: a single subject experiment. Int J Sports Med 1989; 10: 187-191
• 8 Elias LJ, Bryden MP, Bulman-Fleming MB. Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia 1998; 36: 37-43
• 9 Farina D, Arendt-Nielsen L, Graven-Nielsen T. Spike-triggered average torque and muscle fiber conduction velocity of low-threshold motor units following submaximal endurance contractions. J Appl Physiol 2005; 98: 1495-1502
• 10 Farina D, Arendt-Nielsen L, Graven-Nielsen T. Effect of temperature on spike-triggered average torque and electrophysiological properties of low-threshold motor units. J Appl Physiol 2005; 99: 197-203
• 11 Farina D, Ferguson RA, Macaluso A, De Vito G. Correlation of average muscle fibre conduction velocity measured during cycling exercise with myosin heavy chain composition, lactate threshold, and VO2max. J Electromyogr Kinesiol 2007; 17: 393-400
• 12 Farina D, Merletti R, Disselhorst-Klug C. Multi-channel techniques for information extraction from the surface EMG. In: Merletti R, Parker PA. (eds.). Electromyography: Physiology, Engineering, and Non-Invasive Applications. Hoboken, USA: J. Wiley – IEEE Press; 2004: 169-203
• 13 Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 2004; 96: 1486-1495
• 14 Gerdle B, Henriksson-Larsén K, Lorentzon R, Wretling ML. Dependence of the mean power frequency of the electromyogram on muscle force and fibre type. Acta Physiol Scand 1991; 142: 457-465
• 15 Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, Pellegrino MA, Bottinelli R. Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 2011; 110: 433-450
• 16 Gondin J, Guette M, Ballay Y, Martin A. Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 2005; 37: 1291-1299
• 17 Harridge SD, Bottinelli R, Canepari M, Pellegrino MA, Reggiani C, Esbjörnsson M, Saltin B. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflugers Arch 1996; 432: 913-920
• 18 Harriss DJ, Atkinson G. Update – ethical standards in sport and exercise science research. Int J Sports Med 2011; 32: 819-821
• 19 Hortobágyi T, Maffiuletti NA. Neural adaptations to electrical stimulation strength training. Eur J Appl Physiol 2011; 111: 2439-2449
• 20 Jubeau M, Zory R, Gondin J, Martin A, Maffiuletti NA. Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. Eur J Appl Physiol 2006; 98: 202-211
• 21 Klaver-Król EG, Henriquez NR, Oosterloo SJ, Klaver P, Kuipers H, Zwarts MJ. Distribution of motor unit potential velocities in the biceps brachii muscle of sprinters and endurance athletes during short static contractions at low force levels. J Electromyogr Kinesiol 2010; 20: 1107-1114
• 22 Klaver-Król EG, Henriquez NR, Oosterloo SJ, Klaver P, Kuipers H, Zwarts MJ. Distribution of motor unit potential velocities in the biceps brachii muscle of sprinters and endurance athletes during prolonged dynamic exercises at low force levels. J Electromyogr Kinesiol 2010; 20: 1115-1124
• 23 Kupa EJ, Roy SH, Kandarian SC, De Luca CJ. Effects of muscle fiber type and size on EMG median frequency and conduction velocity. J Appl Physiol 1995; 79: 23-32
• 24 Lexell J, Henriksson-Larsén K, Sjöström M. Distribution of different fiber types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 1983; 117: 115-122
• 25 Lexell J, Taylor CC. Variability in muscle fiber areas in whole human quadriceps muscle. How much and why?. Acta Physiol Scand 1989; 136: 561-568
• 26 Lexell J, Taylor C, Sjöström M. Analysis of sampling errors in biopsy techniques using data from whole muscle cross sections. J Appl Physiol 1985; 59: 1228-1235
• 27 Liu Y, Heinichen M, Wirth K, Schmidtbleicher D, Steinacker JM. Response of growth and myogenic factors in human skeletal muscle to strength training. Br J Sports Med 2008; 42: 989-993
• 28 Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 2010; 110: 223-234
• 29 Maffiuletti NA, Zory R, Miotti D, Pellegrino MA, Jubeau M, Bottinelli R. Neuromuscular adaptations to electrostimulation resistance training. Am J Phys Med Rehabil 2006; 85: 167-175
• 30 Mannion AF, Dumas GA, Stevenson JM, Cooper RG. The influence of muscle fiber size and type distribution on electromyographic measures of back muscle fatigability. Spine 1998; 23: 576-584
• 31 Merletti R, Knaflitz M, De Luca CJ. Myoelectric manifestations of fatigue in voluntary and electrically elicited contractions. J Appl Physiol 1990; 69: 1810-1820
• 32 Merletti R, Lo Conte LR, Cisari C, Actis MV. Age related changes in surface myoelectric signals. Scand J Rehabil Med 1992; 24: 25-36
• 33 Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, Fialka-Moser V, Quittan M, Pette D. Functional and biochemical properties of chronically stimulated human skeletal muscle. Eur J Appl Physiol 2003; 89: 202-208
• 34 Parente V, D’Antona G, Adami R, Miotti D, Capodaglio P, De Vito G, Bottinelli R. Long-term resistance training improves force and unloaded shortening velocity of single muscle fibers of elderly women. Eur J Appl Physiol 2008; 104: 885-893
• 35 Pellegrino MA, Canepari M, Rossi R, D’Antona G, Reggiani C, Bottinelli R. Orthologous myosin isoforms and scaling of shortening velocity with body size in mouse, rat, rabbit and human muscles. J Physiol 2003; 546: 677-689
• 36 Pérez M, Lucia A, Rivero JL, Serrano AL, Calbet JA, Delgado MA, Chicharro JL. Effects of transcutaneous short-term electrical stimulation on M. vastus lateralis characteristics of healthy young men. Pflugers Arch 2002; 443: 866-874
• 37 Rainoldi A, Gazzoni M, Melchiorri G. Differences in myoelectric manifestations of fatigue in sprinters and long distance runners. Physiol Meas 2008; 29: 331-340
• 38 Rainoldi A, Gazzoni M, Merletti R, Minetto MA. Mechanical and EMG responses of the vastus lateralis and changes in biochemical variables to isokinetic exercise in endurance and power athletes. J Sports Sci 2008; 26: 321-331
• 39 Rainoldi A, Melchiorri G, Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 2004; 134: 37-43
• 40 Rasmussen MK, Juel C, Nordsborg NB. Exercise induced regulation of muscular Na+, K+ pump, FXYD1 and NHE1 mRNA and protein expression – importance of training status, intensity and muscle type. Am J Physiol 2011; 300: R1209-R1220
• 41 Sadoyama T, Masuda T, Miyata H, Katsuta S. Fiber conduction velocity and fiber composition in human vastus lateralis. Eur J Appl Physiol 1988; 57: 767-771
• 42 Salmons S. Adaptive change in electrically stimulated muscle: a framework for the design of clinical protocols. Muscle Nerve 2009; 40: 918-935
• 43 Thomassen M, Christensen PM, Gunnarsson TP, Nybo L, Bangsbo J. Effect of 2-wk intensified training and inactivity on muscle Na+-K+ pump expression, phospholemman (FXYD1) phosphorylation, and performance in soccer players. J Appl Physiol 2010; 108: 898-905
• 44 Timmons JA. Variability in training-induced skeletal muscle adaptation. J Appl Physiol 2011; 110: 846-853
• 45 Vila-Chã C, Falla D, Correia MV, Farina D. Adjustments in motor unit properties during fatiguing contractions after training. Med Sci Sports Exerc 2012; 44: 616-624
• 46 Vila-Chã C, Falla D, Farina D. Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 2010; 109: 1455-1466
• 47 Wretling ML, Gerdle B, Henriksson-Larsén K. EMG: a non-invasive method for determination of fiber type proportion. Acta Physiol Scand 1987; 131: 627-628
• 48 Zhang LQ, Wang G, Nuber GW, Press JM, Koh JL. In vivo load sharing among the quadriceps components. J Orthop Res 2003; 21: 565-571