THE EFFECTS OF ELECTROMYOSTIMULATION TRAINING ON NEURAL ADAPTATION AND SPORTS PERFORMANCE

Öz

Electromyostimulation (EMS), being applied for rehabilitation and treatment, attrached to the trainers, athletes and sport scientiests as a popular training method. EMS can be defined as electrical currents are applied to the muscle tissue or motor points. The muscles are activated in different ways during voluntary and electrically evoked contractions. Past studies showed that EMS training increases muscular strength less time is required for muscle hypertrophy and also strength development without a statistically significant hypertrophy is the most important evidence of neural adaptations. Therefore, EMS training brings to mind the possibility of an increase in magnitude of neural output from spinal and supraspinal centers to active muscles, spinal plasticity, amount of activated motor units and synchronisation. In addition, unilateral EMS training increases in contralateral homologous muscle strength that shows EMS training influences in supraspinal centers and different cortical regions. The purpose of this review was to investigate of neural adaptation related to EMS training and effects of EMS training for sedentary people and athletes in their sport performances.

Anahtar Kelimeler

• Electromyostimulation, Motor unit, Neural drive, Hypertrophy, Sports performance

ELEKTROMYOSTİMÜLASYON ANTRENMANLARININ NÖRAL ADAPTASYON VE SPORTİF PERFORMANS ÜZERİNE ETKİLERİ.

Öz

Başlangıçta rehabilitasyon ve tedavi amaçlı olarak uygulanan elektromyostimülasyon (EMS) daha sonra popüler bir antrenman yöntemi olarak antrenörlerin, sporcuların ve spor bilimcilerin ilgisini çekmiştir. EMS, kas dokusu ya da motor noktalar üzerine uygulanan elektriksel akımlar olarak tanımlanabilir. Elektriksel uyarılı ve istemli kasılmalar sırasında kaslar farklı şekilde aktive olmaktadır. Yapılan çalışmalar EMS antrenmanlarının kas hipertrofisi için gereken kas kuvvetini daha kısa zamanda arttırdığını ve istatistiksel olarak anlamlı bir hipertrofi olmaksızın artan kuvvetin nöral gelişimin en önemli kanıtı olduğunu göstermektedir. EMS antrenmanlarının maksimal istemli kuvvette artış sağlaması spinal ve supraspinal merkezlerden aktif kaslara olan nöral sürüşte, spinal uyarılabilirlikte, aktive olan motor ünite miktarında ve senkronizasyonunda artış olasılığını da akla getirmektedir. Bunun yanında ünilateral uygulanan EMS antrenmanlarının kontralateral homolog kasta da kuvvet artışları sağlaması EMS antrenmanlarının supraspinal merkezleri ve farklı kortikal bölgeleri etkilediğini göstermektedir. Bu kapsam dahilinde yapılan çalışmaların ışığında derlemenin amacı EMS antrenmanlarına dayalı nöral adaptasyonlar ve EMS antrenmanlarının sedanter ve sporcuların sportif performanlarında meydana getirdiği etkileri incelemektir.

Anahtar Kelimeler

• Elektromyostimülasyon, Motor ünite, Nöral sürüş, Hipertrofi, Sportif

Kaynakça

1. Aagaard, P., Simonsen, E. B., Andersen, J. L., Magnusson, P., & Dyhre-Poulsen, P. (2002). Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. Journal of Applied Physiology, 92(6), 2309-2318.
2. Amiridis, I. G., Arabatzi, F., Violaris, P., Stavropoulos, E., & Hatzitaki, V. (2005). Static balance improvement in elderly after dorsiflexors electrostimulation training. European journal of applied physiology, 94(4), 424-433.
3. Babault, N., Cometti, G., Bernardin, M., Pousson, M., & Chatard, J. C. (2007). Effects of electromyostimulation training on muscle strength and power of elite rugby players. The Journal of Strength and Conditioning Research, 21(2), 431-437.
4. Babault, N., Cometti, C., Maffiluetti, N. A., & Deley, G. (2011). Does electrical stimulation enhance post-exercise recovery? European Journal of Applied Physiology, 111(10), 2501-2507.
5. Banerjee, P., Caulfield B., Crowe, L., & Clark, A. (2005). Prolonged electrical muscle stimulation exercise improves strength and aerobic capacity in healthy sedentary adults. Journal of Applied Physiology, 99(6), 2307-2311.
6. Bezerra, P., Zhou S., Crowley, Z., Brooks, L., & Hooper, A. (2009). Effects of unilateral electromyostimulation superimposed on voluntary training on strength and cross sectional area. Muscle & Nerve, 40(3), 430-437.
7. Bickel, C. S., Gregory, C. M., & Dean, J. C. (2011). Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. European Journal of Applied Physiology, 111(10), 2399-2407.
8. Billot, M., Martin, A., Paizis, C., Cometti, C., & Babault, N. (2010). Effects of an electrostimulation training program on strength, jumping, and kicking capacities in soccer players. The Journal of Strength and Conditioning Research, 24(5), 1407-1413.

9. Binder-Macleod, S. A., Halden, E. E., & Jungles, K. A. (1995). Effects of stimulation intensity on the physiological responses of human motor units. Med. Sci. Sports Exerc, 27(4), 556-565.
10. Blickenstorfer, A., Kleiser, R., Keller, T., Keisker, B., Meyer, M., Riener, R., ve diğ. (2009). Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI. Human Brain Mapping, 30(3), 963-975.
11. Brocherie, F., Babault, N., Cometti, G., Maffiuletti, N., & Chatard, J. C. (2005). Electrostimulation training effects on the physical performance of ice hockey players. Medicine and Science in Sports and Exercise, 37(3), 455-460.
12. Collins, D. F., Burke, D., & Gandevia, S. C. (2001). Large involuntary forces consistent with plateau-like behavior of human motoneurons. The Journal of Neuroscience, 21(11), 4059- 4065.
13. Collins, D. F. (2007). Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exercise and Sport Sciences Reviews, 35(3), 102-109.
14. Colson, S. S., Martin, A., & Hoecke, J. V. (2009). Effects of electromyostimulation versus voluntary isometric training on elbow flexor muscle strength. Journal of Electromyography and Kinesiology, 19(5), 311-319.
15. Deley, G., Cometti, C., Fatnassi, A., Paizis, C., & Babault, N. (2011). Effects of combined electromyostimulation and gymnastics training in prepubertal girls. The Journal of Strength and Conditioning Research, 25(2), 520-526.
16. Delitto, A., Rose, S. J., McKowen, J. M., Lehman, R. C., Thomas, J. A., & Shively, R. A. (1988). Electrical stimulation versus voluntary exercise in strengthening thigh musculature after anterior cruciate ligament surgery. Physical Therapy, 68(5), 660-663.
17. Delitto, A., & Snyder-Mackler, L. (1990). Two Theories of Muscle Strength Augmentation Using Percutaneous Electrical Stimulation. Physical Therapy, 70(3), 158-164.
18. Dragert, K., & Zehr, E. P. (2011). Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Experimental Brain Research, 208(2), 217-227.
19. Duchateau, J., & Hainaut, K. (1988). Training effects of sub-maximal electrostimulation in a human muscle. Medicine and Science in Sports and Exercise, 20(1), 99-104.
20. Dudley, G. A., & Stevenson, S. W. (2008). Use of Electrical Stimulation in Strength and Power Training, in Strength and Power in Sport, Second Edition (ed P. V. Komi), Blackwell Science Ltd, Oxford, UK. 426-437.
21. Enoka, R. M. (2002). Activation order of motor axons in electrically evoked contractions. Muscle Nerve, 25(6),763–764.
22. Everaert, D. G., Thompson, A. K., Chong, S. L., & Stein, R. B. (2010). Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabilitation and Neural Repair, 24(2), 168-177.
23. Farina, D., Roberto, M., & Enoka, R. M. (2004) The extraction of neural strategies from the surface EMG. Journal of Applied Physiolgy, 96(4), 1486-1495.
24. Farina, D., Holobar, A., Merletti, R., & Enoka, R. M. (2010). Decoding the neural drive to muscles from the surface electromyogram. Clinical Neurophysiology, 121(10) 1616-1623.
25. Farthing, J. P. (2009). Cross-education of strength depends on limb dominance: implications for theory and application. Exercise and Sport Sciences Reviews, 37(4), 179-187.
26. Feiereisen, P., Duchateau, J., & Hainaut, K. (1997). Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior. Experimental Brain Research, 114(1), 117-123.
27. Francis, S., Lin X., Aboushoushah, S., White, T. P., Phillips, M., Bowtell, R., ve diğ. (2009). fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage, 44(2), 469-479.
28. Folland, J. P., & Williams, A. G. (2007). The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Medicine, 37(2), 145-68.
29. Fuentes, I., Cobos, A. R., & Segade, L. A. D. (1998). Muscle fibre types and their distribution in the biceps and triceps brachii of the rat and rabbit. Journal of Anatomy, 192(2), 203-210.
30. Gabriel, D. A., Kamen, G., & Frost, G. (2006). Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Medicine, 36(2), 133-149.
31. Garhammer, J. (1983). An introduction to the use of electrical muscle stimulation with athletes. NSCA Journal, 5(4), 44-45.
32. Geoffrey, R. S., Giovanni, D. D. (1986). Torque production in human upper and lower limb muscles with voluntary and electrically stimulated contractions. The Australian journal of Phsiotherapy, 32(1), 38-49.
33. Gondin, J., Guette, M., Ballay, Y., & Martin, A. (2005). Electromyostimulation training effects on neural drive and muscle architecture. Medicine and Science in Sports and Exercise, 37(8), 1291-1299.
34. Gondin, J., Guette, M., Ballay, Y., & Martin, A. (2006). Neural and muscular changes to detraining after electrostimulation training. European Journal of Applied Physiology, 97(2), 165-173.
35. Gondin, J., Duclay, J., & Martin, A. (2006a). Soleus- and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. Journal of Neurophysiology, 95(6), 3328-3335.
36. Gondin, J., Duclay, J., & Martin, A. (2006b). Neural drive preservation after detraining following neuromuscular electrical stimulation training. Neuroscience Letters, 409(3), 210-214.
37. Gondin, J., Brocca, L., Bellinzona, E., D’Antona, G., Maffiuletti, N. A., Miotti, D., ve diğ. (2011). Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. Journal of Applied Physiology, 110(2), 433-450.
38. Gregory, C. M., & Bickel, C. S. (2005). Recruitment Patterns in Human Skeletal Muscle During Electrical Stimulation. Physical Therapy, 85(4) ,358-364.
39. Gulick, D. T., Castel, J. C., Palermo, F. X., & Draper, D. O. (2011). Effect of patterned electrical neuromuscular stimulation on vertical jump in collegiate athletes. Sports Health, 3(2), 152-157.
40. Hainaut, K., & Duchateau, J. (1992). Neuromuscular electrical stimulation and voluntary exercise. Sports Medicine, 14(2), 100-113.
41. Hamdy, S., Rothwell, J. C., Aziz, Q., Singh, K. D., & Thompson, D. G. (1998). Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nature Neuroscience, 1(1), 64-8.
42. Han, B. S., Jang, S. H., Chang, Y., Byun, W. M., Lim, S. K., & Kang, D. S. (2003). Functional magnetic resonance image finding of cortical activation by neuromuscular electrical stimulation on wrist extensor muscles. American Journal of Physical Medicine and Rehabilitation, 82(1), 17-20.
43. Henneman, E., Somjen, G., & Carpenter, D. O. (1965a). Excitability and inhibitibility of motoneurons of different sizes. Journal of Neurophysiology, 28(3), 599–620.
44. Henneman, E., Somjen, G., & Carpenter, D. O. (1965b). Functional significance of cell size in spinal motoneurons. Journal of Neurophysiology, 28(3), 560-580.
45. Herrero, J. A., Izquierdo, M., Maffiuletti, N. A., & Garcia-Lopez, J. (2006). Electromyostimulation and plyometric training effects on jumping and sprint time. International Journal of Sports Medicine, 27(7), 533-539.
46. Hettinga, D. M., & Andrews, B. J. (2007). The feasibility of functional electrical stimulation indoor rowing for high-energy training and sport. International Neuromodulation Society, 10(3), 291-297.
47. Holcomb, W. R. (2005). Is neuromuscular electrical stimulation an effective alternative to resistance training. Strength and Conditioning Journal, 27(3), 76-79.
48. Holcomb, W. R. (2006). Effect of training with neuromuscular electrical stimulation on elbow flexion strength. Journal of Sports Science and Medicine, 5(2), 276-281.
49. Hortobágyi, T., & DeVita, P. (2000). Favorable neuromuscular and cardiovascular responses to 7 days of exercise with an eccentric overload in elderly women. The Journals of Gerontology. Series A, Biological Sciences Medical Sciences, 55(8), B401-B410.
50. Hortobágyi, T., & Maffiuletti, N. A. (2011). Neural adaptations to electrical stimulation strength training. European Journal of Applied Physiology, 111(10), 2439-2449.
51. Huang, Y. M., Hsu, M. J., Lin, C. H., Wei, H. S., & Chang, Y. J. (2010). The Non-linear Relationship between Muscle Voluntary Activation Level and Voluntary Force Measured by the Interpolated Twitch Technique. Sensors, 10, 796-807.
52. Hultman, E., Sjoholm, H., Jaderholm-Ek, I., & Krynicki, J. (1983). Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflüegers Archiv: European Journal of Physiology, 398(2), 139-141.
53. Jubeau, M., Zory, R., Gondin, J., Martin, A., & Maffiuletti, N. A. (2006). Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. European Journal of Applied Physiology, 98(2), 202-211.
54. Jubeau, M., Gondin, J., Martin, A., Sartorio, A., & Maffiuletti, N. A. (2007). Random motor unit activation by electrostimulation. International Journal of Sports Medicine, 28(11), 901-904.
55. Jubeau, M., Gondin, J., Martin, A., Van Hoecke, J., & Maffiuletti, N. A. (2010). Differences in twitch potentiation between voluntary and stimulated quadriceps contractions of equal intensity. Scandinavian Journal of Medicine & Science in Sports, 20(1), 56-62.
56. Kampe, K. K., Jones, R. A., & Auer, D. P. (2000). Frequency dependence of the functional MRI response after electrical median nerve stimulation. Human Brain Mapping, 9(2), 106-14.
57. Kaelin-Lang, A., Luft, A. R., Sawaki, L., Burstein, A. H., Sohn, Y. H., & Cohen, L. G. (2002). Modulation of human corticomotor excitability by somatosensory input. Journal of Physiology, 540(Pt2), 623-633.
58. Khaslavskaia, S., & Sinkjaer, T. (2005). Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Experimental Brain Research, 162(4), 497-502.
59. Kırdı, N., Tunca, Ö., & Meriç, A. (1998). Fonksiyonel elektrik stimülasyonu. Ankara: Hacettepe Üniversitesi Fizik Tedavi ve Rehabilitasyon Yüksekokulu Yayınları.
60. Kimberley, T. J., Lewis, S. M., Auerbach, E. J., Dorsey, L. L., Lojovich, J. M., & Carey, J. R. (2004). Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Experimental Brain Research, 154(4), 450-460.
61. Knaflitz, M., Merletti, R., & De Luca, C. J., (1990). Inference of motor unit recruitment order in voluntary and electrically elicited contractions, Journal of Applied Physiology, 68(4), 1657-1667.
62. Koesler, I. B., Dafotakis, M., Ameli, M., Fink, G. R., & Nowak, D. A. (2009). Electrical somatosensory stimulation improves movement kinematics of the affected hand following stroke. Journal of Neurology, Neurosurgery & Psychiatry, 80(6), 614-619.
63. Laughman, R. K., Youdas, J. W., Garrett, T. R., & Chao, E. Y. S. (1983). Strength changes in the normal quadriceps femoris muscle as a result of electrical stimulation. Physical Therapy, 63(4), 494-499.
64. Lieber, R. L., Silva, P. D., & Daniel, D. M. (1996). Equal effectiveness of electrical and volitional strength training for quadriceps femoris muscles after anterior cruciate ligament surgery. Journal of Orthopaedic Research, 14(1), 131-138.
65. Lindquist, A. R. R., Prado, C. L., Barros, R. M. L., Mattioli, R., Costa, P. H. L, & Salvini, T. F. (2007). Gait training combining partial body-weight support a treadmill, and functional electrical stimulation: effects on poststroke gait. Physical Therapy, 87(9), 1144-1154.
66. Maffiuletti, N. A., Cometti, G., Amiridis, I. G., Martin, A., Pousson, M., & Chatard, J. C. (2000). The effects of electromyostimulation training and basketball practice on muscle strength and jumping ability. International Journal of Sports Medicine, 21(6), 437-443.
67. Maffiuletti, N. A., Pensini, M., & Martin, A. (2002a). Activation of human plantar flexor muscles increases after electromyostimulation training. Journal of Applied Physiology, 92(4), 1383–1392.
68. Maffiuletti, N. A., Dugnani, S., Folz, M., Di Pierno, E., & Mauro, E. (2002b). Effect Of combined electrostimulation and plyometric training on vertical jump height. Medicine and Science in Sports and Exercise, 34(10), 1638-1644.
69. Maffiuletti, N. A., Pensini, M., Scaglioni, G., Ferri, A., Ballay, Y., & Martin, A. (2003). Effect of electromyostimulation training on soleus and gastrocnemii H- and T-reflex properties. European Journal of Applied Physiology, 90(5-6), 601-607.
70. Maffiuletti, N. A., Zory, R., Miotti, D., Pellegrino, M. A., Jubeau, M., & Bottinelli, R. (2006). Neuromuscular adaptations to electrostimulation resistance training. American Journal of Physical Medicine & Rehabilitation, 85(2), 167-75.
71. Maffiuletti, N. A., Bramanti, J., Jubeau, M., Bizzini, M., Deley, G., & Cometti, G. (2009). Feasibility and efficacy of progressive electrostimulation strength training for competitive tennis players. The Journal of Strength and Conditioning Research, 23(2), 677-682.
72. Maffiuletti, N. A. (2010). Physiological and methodological considerations for the use of neuromuscular electrical stimulation. European Journal of Applied Physiology, 110(2), 223-234.
73. Malatesta, D., Cattaneo, F., Dugnani, S., & Maffiuletti, N. A. (2003). Effects of Electromyostimulation Training and Volleyball Practice on Jumping Ability. Journal of Strength and Conditioning Research, 17(3), 573–579.
74. Martin, L., Cometti, G., Pousson, M., & Morlon, B. (1993). Effect Of Electrical stimulation on the contractile characteristics of the triceps surae muscle. European Journal of Applied Physiology, 67(5), 457-461.
75. Marqueste, T., Hug, F., Decherchi, P., & Mes, Y. (2003). Changes in neuromuscular function after training by functional electrical stimulation. Muscle & Nerve, 28(2), 181-188.
76. Marqueste, T., Messan, F., Hug, F., Laurin, J., Dousset, E., Grelot, L., ve diğ. (2010). Effect of repetitive biphasic muscle electrostimulation training on vertical jump performances in female volleyball players. International Journal of Sport and Health Science, 8, 0-55.
77. McDonnell, M. N., & Ridding, M. C. (2006). Afferent stimulation facilitates performance on a novel motor task. Experimental Brain Research, 170(1), 109-115.
78. Meesen, R. L., Cuypers, K., Rothwell, J. C., Swinnen, S. P., & Levin, O. (2011). The effect of long-term TENS on persistent neuroplastic changes in the human cerebral cortex. Human Brain Mapping, 32(6), 872-82.
79. Mendell, L. M. (2005). The size principle: a rule describing the recruitment of motoneurons. J. Neurophysiol, 93(6), 3024–3026.
80. Nudo, R. J., Plautz, E. J., & Frost, S. B. (2001). Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle & Nerve, 24(8), 1000-1019.
81. Paillard, T. (2008). Combined Application of Neuromuscular Electrical Stimulation and Voluntary Muscular Contractions. Sports Medicine, 38(2), 161-177.
82. Paillard, T., Noe, F., Bernard, N., Dupui, P., & Hazard, C. (2008). Effects of two types of neuromuscular electrical stimulation training on vertical jump performance. The Journal of Strength and Conditioning Research, 22(4), 1273-1278.
83. Peckham, P. H., Knutson, J. S., (2005). Functional Electrical Stimulation for Neuromuscular Applications. Annual Review of Biomedical Engineering, 7, 327-360.
84. Perez, M., Lucia, A., Rivero, J. L., Serrano, A. L., Calbet, J. A., Delgado, M. A., ve diğ. (2002). Effects of transcutaneous short-term electrical stimulation on M.vastus lateralis characteristics of healthy young men. Pflüegers Archiv: European Journal of Physiology, 443(5-6), 866-874.
85. Pichon, F., Chatard, J. C., Martin, A., & Cometti, G. (1995). Electrical stimulation and swimming performance. Medicine & Science in Sports & Exercise, 27(12), 1671-1676.
86. Porcari, J. P., McLean, K. P., Foster, C., Kernozek, T., Crenshaw, B., & Swenson, C. (2002). Effects of electrical muscle stimulation on body composition, muscle strength, and physical appearance. The Journal of Strength and Conditioning Research, 16(2), 165-172.
87. Porcari, J. P., Miller, J., Cornwell, K., Foster, C., Gibson, M., McLean, K., ve diğ. (2005). The effects of neuromuscular electrical stimulation training of abdominal strength, endurance, and selected anthropometric measures. Journal of Sports Science and Medicine, 4(1), 66-75.
88. Ridding, M. C., Brouwer, B., Miles, T. S., Pitcher, J. B., & Thompson, P. D. (2000). Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Experimental Brain Research, 131(1), 135-143.
89. Ridding, M. C., McKay, D. R., Thompson, P. D., & Miles, T. S. (2001). Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clinical Neurophysiology, 112(8), 1461-1469.
90. Sale, D. G. (1988). Neural adaptation to resistance training. Medicine and Science in Sports and Exercise, 20(5), 135-45.
91. Sale, D. G. (2003). Neural Adaptation to Strength Training. (PV Komi, Ed.) Strength and Power in Sport, 2nd Edition, s. 281-314. Blackwell, London.
92. Sanchez, B. R., Puche, P. P., & Gonzalez-Badillo, J. J. (2005). Percutaneous electrical stimulation in strength training: an update. The Journal of Strength and Conditioning Research, 19(2), 438-448.
93. Seyri, M. K., & Maffiuletti, N. A. (2011). Effect of Electromyostimulation Training on Muscle Strength and Sports Performance. Strength Conditioning Journal, 33(1), 70-75.
94. Sheffler, L. R., & Chae, J. (2007). Neuromuscular Electrical Stimulation in Neurorehabilitation. Muscle & Nerve, 35(5), 562-590.
95. Shield, A., & Zhou, S. (2004). Assessing voluntary muscle activation with the twitch interpolation technique. Sports Medicine, 34(4), 253-67.
96. Sinacore, D. R., Delitto, A., King, D. S., & Roset, S. J. (1990). Type II Fiber Activation with Electrical Stimulation: A Preliminary-Report. Physical Therapy, 70(7), 416-422.
97. Singer, K. P. (1986). The influence of unilateral electrical muscle stimulation on motor unit activity patterns in atrophic human quadriceps. The Australian Journal of Physiotherapy, 32(1), 31-37.
98. Smith, G. V., Alon, G., Roys, S. R., & Gullapalli, R. P. (2003). Functional MRI determination of a dose-response relationship to lower extremity neuromuscular electrical stimulation in healthy subjects. Experimental Brain Research, 150(1), 33–39.
99. Smith, J. C., & Motl, R. W. (2005). Electromyographic indices of neuromuscular reflexes. International Journal of Sport and Exercise Psychology, 3(3), 322-337.
100. Solomonow, M., Baratta, R., Shoji, H., & Ambrosia, R. (1986). The myoelectric signal of electrically stimulated muscle during recruitment: an inherent feedback parameter for a closed loop control scheme. IEEE Transactions on Biomedical Engineering, 33(8), 735–745.
101. Spiegel, J., Tintera, J., Gawehn, J., Stoeter, P., & Treede, R. D. (1999). Functional MRI of human primary somatosensory and motor cortex during median nerve stimulation. Clinical Neurophysiology, 110(1), 47-52.
102. Stein, R. B., Everaert, D. G., Thompson, A. K., & Chong, S. L., Whittaker, M., Robertson, J., ve diğ. (2010). Longterm therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabilitation Neural Repair, 24(2), 152-167.
103. Stevens, J. E., Mizner, R. L., & Snyder-Mackler, L. (2004). Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series. Journal of Orthopaedic & Sports Physical Therapy, 34(1), 21–29.
104. Tamaki, T., Uchiyama, S., Uchiyama, Y., Akatsuka, A., Yoshimura, S., Roy, R. R., ve diğ. (2000). Limited myogenic response to a single bout of weight-lifting exercise in old rats. American Journal of Physiology-Cell Physiology, 278(6), C1143–C1152.
105. Trimble, M. H., & Enoka, R. M. (1991). Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Physical Therapy, 71(4), 273-280.
106. Vanderthommen, M., & Duchateau, J. (2007). Electrical stimulation as a modality to improve performance of the neuromuscular system. Exercise and Sport Sciences Reviews, 35(4), 180-185.
107. Venable, M., Collins, M. A., O’Bryant, H. S., Denegar, C. R., Sedivec, M. J., & Alon, G. (1991). Effect of supplemental electrical stimulation on the development of strength, vertical jump performance and power. Journal of Applied Sport Science Research, 5(3), 139-143.
108. Yu, J. H., Zhou, S., Huang, L. P., Cao, L. J., Liu, J., & Hu, Z. (2007). Assessment of muscle activation with twitch interpolation technique in a unilateral electromyostimulation training program. Annual Meeting of Chinese Medical Association, Sports Medicine, Beijing China, 6-9 April.
109. Ward, A. R., & Shkuratova, N. (2002). Russian electrical stimulation: the early experiments. Physical Therapy, 82(10), 1019-1030.
110. Willoughby, D. S., & Simpson, S. (1996). The effects of electromyostimulation and dynamic muscular contractions on the strength of college basketball players. The Journal of Strength and Conditioning Research, 10(1), 40-44.
111. Willoughby, D. S., & Simpson, S. (1998). Supplemental EMS and dynamic weigth training: Effects on knee extensor strength and vertical jump of female college track&field athletes. The Journal of Strength and Conditioning Research, 12(3), 131-137.
112. Zatsiorsky, V. M., & Kraemer, W. J. (2006). Science and Practice of Strength Training, Second Edition. Human Kinetics. 132.
113. Zhou, S. (2003). Cross education and neuromuscular adaptations during early stage of strength training. Journal of Exerise Science and Fitness, 1(1), 54-60.