Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal

Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74:532–537 Baldwin ER, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240 Bellemare F, Woods JJ, Johansson R, Bigland-Ritchie B (1983) Motor-unit discharge rates in maximal voluntary contractions of three human muscles. J Neurophysiol 50:1380–1392 Bergquist AJ, Clair JM, Collins DF (2011) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae. J Appl Physiol 110:627–637 Bickel CS, Slade JM, Dudley GA (2004) Long-term spinal cord injury increases susceptibility to isometric contraction-induced muscle injury. Eur J Appl Physiol 91:308–313 Binder-Macleod SA, McDermond LR (1992) Changes in the force-frequency relationship of the human quadriceps femoris muscle following electrically and voluntarily induced fatigue. Phys Ther 72:95–104 Binder-Macleod SA, Halden EE, Jungles KA (1995) Effects of stimulation intensity on the physiological responses of human motor units. Med Sci Sports Exerc 27:556–565 Blair E, Erlanger J (1933) A comparison of the characteristics of axons through their individual electrical responses. Am J Physiol 106:524–564 Botter A, Merletti R, Minetto MA (2009) Pulse charge and not waveform affects M-wave properties during progressive motor unit activation. J Electromyogr Kinesiol 19:564–573 Carpentier A, Duchateau J, Hainaut K (2001) Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus. J Physiol 534:903–912 Chou LW, Binder-Macleod SA (2007) The effects of stimulation frequency and fatigue on the force-intensity relationship for human skeletal muscle. Clin Neurophysiol 118:1387–1396 Collins S, Ruina A, Tedrake R, Wisse M (2005) Efficient bipedal robots based on passive-dynamic walkers. Science 307:1082–1085 Cronin NJ, Klint RA, Grey MJ, Sinkjaer T (2011) Ultrasonography as a tool to study afferent feedback from the muscle-tendon complex during human walking. J Electromyogr Kinesiol 21:197–207 Crow MT, Kushmerick MJ (1982) Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79:147–166 Decker MJ, Griffin L, Abraham LD, Brandt L (2010) Alternating stimulation of synergistic muscles during functional electrical stimulation cycling improves endurance in persons with spinal cord injury. J Electromyogr Kinesiol 20:1163–1169 Delitto A, Brown M, Strube MJ, Rose SJ, Lehman RC (1989) Electrical stimulation of quadriceps femoris in an elite weight lifter: a single subject experiment. Int J Sports Med 10:187–191 Dudley GA (1996) Is electrical stimulation applicable to improve strength and power in normal humans? In: Marconnet P, Saltin B, Komi PV, Poortmans J (eds) Human muscular function during dynamic exercise, vol 41. Basel, Karger, pp 71–81 Enoka RM (2002) Activation order of motor axons in electrically evoked contractions. Muscle Nerve 25:763–764 Fang ZP, Mortimer JT (1991a) A method to effect physiological recruitment order in electrically activated muscle. IEEE Trans Biomed Eng 38:175–179 Fang ZP, Mortimer JT (1991b) Selective activation of small motor axons by quasi-trapezoidal current pulses. IEEE Trans Biomed Eng 38:168–174 Farina D, Blanchietti A, Pozzo M, Merletti R (2004) M-wave properties during progressive motor unit activation by transcutaneous stimulation. J Appl Physiol 97:545–555 Feiereisen P, Duchateau J, Hainaut K (1997) Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior. Exp Brain Res 114:117–123 Fuentes JP, Armijo Olivo S, Magee DJ, Gross DP (2010) Effectiveness of interferential current therapy in the management of musculoskeletal pain: a systematic review and meta-analysis. Phys Ther 90:1219–1238 Gersh MR (1992) Electrotherapy in rehabilitation. PA, F. A. Davis Company, Philadelphia Gorgey AS, Mahoney E, Kendall T, Dudley GA (2006) Effects of neuromuscular electrical stimulation parameters on specific tension. Eur J Appl Physiol 97:737–744 Gorgey AS, Black CD, Elder CP, Dudley GA (2009) Effects of electrical stimulation parameters on fatigue in skeletal muscle. J Orthop Sports Phys Ther 39:684–692 Graham GM, Thrasher TA, Popovic MR (2006) The effect of random modulation of functional electrical stimulation parameters on muscle fatigue. IEEE Trans Neural Syst Rehabil Eng 14:38–45 Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85:358–364 Gregory CM, Dixon W, Bickel CS (2007) Impact of varying pulse frequency and duration on muscle torque production and fatigue. Muscle Nerve 35:504–509 Han YS, Proctor DN, Geiger PC, Sieck GC (2001) Reserve capacity for ATP consumption during isometric contraction in human skeletal muscle fibers. J Appl Physiol 90:657–664 Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 126:1345–1347 Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28:560–580 Hennings K, Arendt-Nielsen L, Andersen OK (2005) Orderly activation of human motor neurons using electrical ramp prepulses. Clin Neurophysiol 116:597–604 Hillegass EA, Dudley GA (1999) Surface electrical stimulation of skeletal muscle after spinal cord injury. Spinal Cord 37:251–257 Hopkins JT, Ingersoll CD, Krause BA, Edwards JE, Cordova ML (2001) Effect of knee joint effusion on quadriceps and soleus motoneuron pool excitability. Med Sci Sports Exerc 33:123–126 Houghton PE, Campbell KE, Fraser CH, Harris C, Keast DH, Potter PJ et al (2010) Electrical stimulation therapy increases rate of healing of pressure ulcers in community-dwelling people with spinal cord injury. Arch Phys Med Rehabil 91:669–678 Hughes AC, Guo L, Deweerth SP (2010) Interleaved multichannel epimysial stimulation for eliciting smooth contraction of muscle with reduced fatigue. Conf Proc IEEE Eng Med Biol Soc 2010:6226–6229 Indurthy M, Griffin L (2007) Effect of random interpulse interval modulation on neuromuscular fatigue. Muscle Nerve 36:807–815 Ishikawa M, Komi PV, Grey MJ, Lepola V, Bruggemann GP (2005) Muscle-tendon interaction and elastic energy usage in human walking. J Appl Physiol 99:603–608 Jabre JF, Spellman NT (1996) The demonstration of the size principle in humans using macro electromyography and precision decomposition. Muscle Nerve 19:338–341 Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129 Johnston TE, Smith BT, Mulcahey MJ, Betz RR, Lauer RT (2009) A randomized controlled trial on the effects of cycling with and without electrical stimulation on cardiorespiratory and vascular health in children with spinal cord injury. Arch Phys Med Rehabil 90:1379–1388 Jubeau M, Gondin J, Martin A, Sartorio A, Maffiuletti NA (2007) Random motor unit activation by electrostimulation. Int J Sports Med 28:901–904 Kim CK, Bangsbo J, Strange S, Karpakka J, Saltin B (1995) Metabolic response and muscle glycogen depletion pattern during prolonged electrically induced dynamic exercise in man. Scand J Rehabil Med 27:51–58 Knaflitz M, Merletti R, De Luca CJ (1990) Inference of motor unit recruitment order in voluntary and electrically elicited contractions. J Appl Physiol 68:1657–1667 Kubiak RJ, Whitman KM, Johnston RM (1987) Changes in quadriceps femoris muscle strength using isometric exercise versus electrical stimulation. J Orthop Sports Phys Ther 8:537–541 Lewek M, Stevens J, Snyder-Mackler L (2001) The use of electrical stimulation to increase quadriceps femoris muscle force in an elderly patient following a total knee arthroplasty. Phys Ther 81:1565–1571 Lichtwark GA, Wilson AM (2006) Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J Exp Biol 209:4379–4388 Llewellyn ME, Thompson KR, Deisseroth K, Delp SL (2010) Orderly recruitment of motor units under optical control in vivo. Nat Med 16:1161–1165 Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234 Mahoney ET, Bickel CS, Elder C, Black C, Slade JM, Apple D et al (2005) Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury. Arch Phys Med Rehabil 86:1502–1504 Malesevic NM, Popovic LZ, Schwirtlich L, Popovic DB (2010) Distributed low-frequency functional electrical stimulation delays muscle fatigue compared to conventional stimulation. Muscle Nerve 42:556–562 Mesin L, Merletti R (2008) Distribution of electrical stimulation current in a planar multilayer anisotropic tissue. IEEE Trans Biomed Eng 55:660–670 Milner-Brown HS, Stein RB, Yemm R (1973) The orderly recruitment of human motor units during voluntary isometric contractions. J Physiol 230:359–370 Nalty T, Sabbahi M (2001) Electrotherapy: clinical procedures manual, McGraw-Hill, New York Nardone A, Romano C, Schieppati M (1989) Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J Physiol 409:451–471 Popovic LZ, Malesevic NM (2009) Muscle fatigue of quadriceps in paraplegics: comparison between single vs multi-pad electrode surface stimulation. Conf Proc IEEE Eng Med Biol Soc 2009:6785–6788 Robinson AJ, Snyder-Mackler L (1995) Clinical electrophysiology: electrotherapy and electrophysiologic testing. Lippincott Williams & Wilkins, Baltimore Rubinstein S, Kamen G (2005) Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults. J Electromyogr Kinesiol 15:536–543 Ruther CL, Golden CL, Harris RT, Dudley GA (1995) Hypertrophy, resistance training, and the nature of skeletal muscle activation. J Strength Cond Res 9:155–159 Sharma N, Stegath K, Gregory CM, Dixon WE (2009) Nonlinear neuromuscular electrical stimulation tracking control of a human limb. IEEE Trans Neural Syst Rehabil Eng 17:576–584 Sinacore DR, Delitto A, King DS, Rose SJ (1990) Type II fiber activation with electrical stimulation: a preliminary report. Phys Ther 70:416–422 Slade JM, Bickel CS, Warren GL, Dudley GA (2003) Variable frequency trains enhance torque independent of stimulation amplitude. Acta Physiol Scand 177:87–92 Snyder-Mackler L, Delitto A, Stralka SW, Bailey SL (1994) Use of electrical stimulation to enhance recovery of quadriceps femoris muscle force production in patients following anterior cruciate ligament reconstruction. Phys Ther 74:901–907 Solomonow M (1984) External control of the neuromuscular system. IEEE Trans Biomed Eng 31:752–763 Stein RB, Chong SL, James KB, Kido A, Bell GJ, Tubman LA et al (2002) Electrical stimulation for therapy and mobility after spinal cord injury. Prog Brain Res 137:27–34 Stein RB, Everaert DG, Thompson AK, Chong SL, Whittaker M, Robertson J et al (2010) Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabil Neural Repair 24:152–167 Stevens JE, Mizner RL, Snyder-Mackler L (2004) Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series. J Orthop Sports Phys Ther 34:21–29 Stevenson SW, Dudley GA (2001) Dietary creatine supplementation and muscular adaptation to resistive overload. Med Sci Sports Exerc 33:1304–1310 Thomas CK, Nelson G, Than L, Zijdewind I (2002) Motor unit activation order during electrically evoked contractions of paralyzed or partially paralyzed muscles. Muscle Nerve 25:797–804 Trimble MH, RM Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273–280; discussion 280–272 van Bolhuis AI, Holsheimer J, Savelberg HH (2001) A nerve stimulation method to selectively recruit smaller motor-units in rat skeletal muscle. J Neurosci Methods 107:87–92 Vila-Cha C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following 6 weeks of either endurance or strength training. J Appl Physiol 109:1455–1466 Vollestad NK, Blom PC (1985) Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand 125:395–405