Utilizing Physiological Principles of Motor Unit Recruitment to Reduce Fatigability of Electrically-Evoked Contractions: A Narrative Review

  • Trevor S. Barss
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
  • Emily N. Ainsley
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada

    Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
  • Francisca C. Claveria-Gonzalez
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada

    Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
  • M. John Luu
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada

    Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
  • Dylan J. Miller
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
  • Matheus J. Wiest
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada

    Biomechanics Laboratory, Department of Physical Education, Federal University of Santa Catarina, Florianópolis, Brazil
    Search for articles by this author
  • David F. Collins
    Corresponding author David F. Collins, PhD, 4-219 Van Vliet Complex, University of Alberta, Edmonton, AB T6G 2H9, Canada.
    Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, AB, Canada

    Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB, Canada
    Search for articles by this author
Published:September 18, 2017DOI:


      Neuromuscular electrical stimulation (NMES) is used to produce contractions to restore movement and reduce secondary complications for individuals experiencing motor impairment. NMES is conventionally delivered through a single pair of electrodes over a muscle belly or nerve trunk using short pulse durations and frequencies between 20 and 40Hz (conventional NMES). Unfortunately, the benefits and widespread use of conventional NMES are limited by contraction fatigability, which is in large part because of the nonphysiological way that contractions are generated. This review provides a summary of approaches designed to reduce fatigability during NMES, by using physiological principles that help minimize fatigability of voluntary contractions. First, relevant principles of the recruitment and discharge of motor units (MUs) inherent to voluntary contractions and conventional NMES are introduced, and the main mechanisms of fatigability for each contraction type are briefly discussed. A variety of NMES approaches are then described that were designed to reduce fatigability by generating contractions that more closely mimic voluntary contractions. These approaches include altering stimulation parameters, to recruit MUs in their physiological order, and stimulating through multiple electrodes, to reduce MU discharge rates. Although each approach has unique advantages and disadvantages, approaches that minimize MU discharge rates hold the most promise for imminent translation into rehabilitation practice. The way that NMES is currently delivered limits its utility as a rehabilitative tool. Reducing fatigability by delivering NMES in ways that better mimic voluntary contractions holds promise for optimizing the benefits and widespread use of NMES-based programs.


      List of abbreviations:

      H-reflex (Hoffman reflex), M-wave (motor wave), MU (motor unit), NMES (neuromuscular electrical stimulation), SCI (spinal cord injury)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Sheffler L.R.
        • Chae J.
        Neuromuscular electrical stimulation in neurorehabilitation.
        Muscle Nerve. 2007; 35: 562-590
        • Chae J.
        • Sheffler L.R.
        • Knutson J.S.
        Neuromuscular electrical stimulation for motor restoration in hemiplegia.
        Top Stroke Rehabil. 2008; 15: 412-426
        • Gan L.S.
        • Ravid E.
        • Kowalczewski J.A.
        • Olson J.L.
        • Morhart M.
        • Prochazka A.
        First permanent implant of nerve stimulation leads activated by surface electrodes, enabling hand grasp and release: the stimulus router neuroprosthesis.
        Neurorehabil Neural Repair. 2012; 26: 335-343
        • Gillette J.C.
        • Stevermer C.A.
        • Quick N.E.
        • Abbas J.J.
        Alternative foot placements for individuals with spinal cord injuries standing with the assistance of functional neuromuscular stimulation.
        Gait Posture. 2008; 27: 280-285
        • Everaert D.G.
        • Thompson A.K.
        • Chong S.L.
        • Stein R.B.
        Does functional electrical stimulation for foot drop strengthen corticospinal connections?.
        Neurorehabil Neural Repair. 2010; 24: 168-177
        • Wheeler G.D.
        • Andrews B.
        • Lederer R.
        • et al.
        Functional electric stimulation-assisted rowing: increasing cardiovascular fitness through functional electric stimulation rowing training in persons with spinal cord injury.
        Arch Phys Med Rehabil. 2002; 83: 1093-1099
        • Griffin L.
        • Decker M.J.
        • Hwang J.Y.
        • et al.
        Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury.
        J Electromyogr Kinesiol. 2009; 19: 614-622
        • Baldi J.C.
        • Jackson R.D.
        • Moraille R.
        • Mysiw W.J.
        Muscle atrophy is prevented in patients with acute spinal cord injury using functional electrical stimulation.
        Spinal Cord. 1998; 36: 463-469
        • Dirks M.L.
        • Hansen D.
        • Van Assche A.
        • Dendale P.
        • Van Loon L.J.
        Neuromuscular electrical stimulation prevents muscle wasting in critically ill comatose patients.
        Clin Sci (Lond). 2015; 128: 357-365
        • Scremin A.M.
        • Kurta L.
        • Gentili A.
        • et al.
        Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program.
        Arch Phys Med Rehabil. 1999; 80: 1531-1536
        • Frotzler A.
        • Coupaud S.
        • Perret C.
        • et al.
        High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury.
        Bone. 2008; 43: 169-176
        • Bélanger M.
        • Stein R.B.
        • Wheeler G.D.
        • Gordon T.
        • Leduc B.
        Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals?.
        Arch Phys Med Rehabil. 2000; 81: 1090-1098
        • Bajd T.
        • Kralj A.
        • Turk R.
        • Benko H.
        • Šega J.
        Use of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injuries.
        J Biomed Eng. 1989; 11: 96-102
        • Crameri R.M.
        • Weston A.
        • Climstein M.
        • Davis G.M.
        • Sutton J.R.
        Effects of electrical stimulation-induced leg training on skeletal muscle adaptability in spinal cord injury.
        Scand J Med Sci Sports. 2002; 12: 316-322
        • Yan T.
        • Hui-Chan C.W.
        • Li L.S.
        Functional electrical stimulation improves motor recovery of the lower extremity and walking ability of subjects with first acute stroke: a randomized placebo-controlled trial.
        Stroke. 2005; 36: 80-85
        • Davis G.M.
        • Hamzaid N.A.
        • Fornusek C.
        Cardiorespiratory, metabolic, and biomechanical responses during functional electrical stimulation leg exercise: health and fitness benefits.
        Artif Organs. 2008; 32: 625-629
        • McCormack K.
        • Carty A.
        • Coughlan G.F.
        • Crowe L.M.
        • Caulfield B.M.
        The effects of a neuromuscular electrical stimulation training intervention on physiological measures in a spinal cord injured male: a case study.
        Physiother Irel. 2010; 31: 30-35
        • Demircioglu D.T.
        • Paker N.
        • Erbil E.
        • Bugdayci D.
        • Emre T.Y.
        The effect of neuromuscular electrical stimulation on functional status and quality of life after knee arthroplasty: a randomized controlled study.
        J Phys Ther Sci. 2015; 27: 2501-2506
        • Maffiuletti N.A.
        Physiological and methodological considerations for the use of neuromuscular electrical stimulation.
        Eur J Appl Physiol. 2010; 110: 223-234
        • Enoka R.M.
        • Duchateau J.
        Muscle fatigue: what, why and how it influences muscle function.
        J Physiol. 2008; 5861: 11-23
        • Kluger B.M.
        • Krupp L.B.
        • Enoka R.M.
        Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy.
        Neurology. 2013; 80: 409-416
        • Eser P.C.
        • Donaldson Nde N.
        • Knecht H.
        • Stüssi E.
        Influence of different stimulation frequencies on power output and fatigue during FES-cycling in recently injured SCI people.
        IEEE Trans Neural Syst Rehabil Eng. 2003; 11: 236-240
        • Janssen T.W.
        • Bakker M.
        • Wyngaert A.
        • Gerrits K.H.
        • de Haan A.
        Effects of stimulation pattern on electrical stimulation-induced leg cycling performance.
        J Rehabil Res Dev. 2004; 41: 787-796
        • Downey R.J.
        • Bellman M.J.
        • Kawai H.
        • Gregory C.M.
        • Dixon W.E.
        Comparing the induced muscle fatigue between asynchronous and synchronous electrical stimulation in able-bodied and spinal cord injured populations.
        IEEE Trans Neural Syst Rehabil Eng. 2015; 23: 964-972
        • Castro M.J.
        • Apple Jr., D.F.
        • Staron R.S.
        • Campos G.E.
        • Dudley G.A.
        Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury.
        J Appl Physiol. 1999; 86: 350-358
        • Henneman E.
        • Olson C.B.
        Relations between structure and function in the design of skeletal muscle.
        J Neurophysiol. 1965; 28: 581-598
        • Contessa P.
        • De Luca C.J.
        Neural control of muscle force: indications from a simulation model.
        J Neurophysiol. 2013; 109: 1548-1570
        • Calancie B.
        • Bawa P.
        Recruitment order of motor units during the stretch reflex in man.
        Brain Res. 1984; 292: 176-178
        • Bigland B.
        • Lippold O.
        Motor unit activity in the voluntary contraction of human muscle.
        J Physiol. 1954; 125: 322-335
        • Enoka R.M.
        • Duchateau J.
        Rate coding and the control of muscle force.
        Cold Spring Harb Perspect Med. 2017; 7
        • Bellemare F.
        • Woods J.J.
        • Johansson R.
        • Bigland-Ritchie B.
        Motor-unit discharge rates in maximal voluntary contractions of three human muscles.
        J Neurophysiol. 1983; 50: 1380-1392
        • Reid G.
        The rate of discharge of the extraocular motoneurones.
        J Physiol. 1949; 110: 217-225
        • Connelly D.M.
        • Rice C.L.
        • Roos M.R.
        • Vandervoort A.A.
        Motor unit firing rates and contractile properties in tibialis anterior of young and old men.
        J Appl Physiol. 1999; 87: 843-852
        • Roos M.R.
        • Rice C.L.
        • Connelly D.M.
        • Vandervoort A.A.
        Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men.
        Muscle Nerve. 1999; 22: 1094-1103
        • Kirk E.A.
        • Rice C.L.
        Contractile function and motor unit firing rates of the human hamstrings.
        J Neurophysiol. 2017; 117: 243-250
        • Dalton B.H.
        • Harwood B.
        • Davidson A.W.
        • Rice C.L.
        Triceps surae contractile properties and firing rates in the soleus of young and old men.
        J Appl Physiol. 2009; 107: 1781-1788
        • Graham M.T.
        • Rice C.L.
        • Dalton B.H.
        Motor unit firing rates of the gastrocnemii during maximal brief steady-state contractions in humans.
        J Electromyogr Kinesiol. 2016; 26: 82-87
        • Bigland-Ritchie B.R.
        • Furbush F.H.
        • Gandevia S.C.
        • Thomas C.K.
        Voluntary discharge frequencies of human motoneurons at different muscle lengths.
        Muscle Nerve. 1992; 15: 130-137
        • Stock M.S.
        • Thompson B.J.
        Motor unit interpulse intervals during high force contractions.
        Hum Kinet. 2016; 20: 70-86
        • Clamann H.P.
        Statistical analysis of motor unit firing patterns in a human skeletal muscle.
        Biophys J. 1969; 9: 1233-1251
        • Garland S.J.
        • Griffin L.
        Motor unit double discharges: statistical anomaly or functional entity?.
        Can J Appl Physiol. 1999; 24: 113-130
        • Binder-Macleod S.
        • Kesar T.
        Catchlike property of skeletal muscle: recent findings and clinical implications.
        Muscle Nerve. 2005; 31: 681-693
        • Kudina L.P.
        • Andreeva R.E.
        Triplet firing origin in human motor units: emerging hypotheses.
        Exp Brain Res. 2016; 234: 837-844
        • Desmedt J.E.
        • Godaux E.
        Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle.
        J Physiol. 1977; 264: 673-693
        • Bawa P.
        • Calancie B.
        Repetitive doublets in human flexor carpi radialis muscle.
        J Physiol. 1983; 339: 123-132
        • Kudina L.P.
        • Andreeva R.E.
        Motoneuron double discharges: only one or two different entities?.
        Front Cell Neurosci. 2013; 7: 75
        • Burke D.
        • Gandevia S.C.
        Properties of human peripheral nerves: implications for studies of human motor control.
        Prog Brain Res. 1999; 123: 427-435
        • Bawa P.
        • Murnaghan C.
        Motor unit rotation in a variety of human muscles.
        J Neurophysiol. 2009; 102: 2265-2272
        • Bawa P.
        • Pang M.Y.
        • Olesen K.A.
        • Calancie B.
        Rotation of motoneurons during prolonged isometric contractions in humans.
        J Neurophysiol. 2006; 96: 1135-1140
        • Jones D.A.
        • Bigland-Ritchie B.
        • Edwards R.H.
        Excitation frequency and muscle fatigue: mechanical responses during voluntary and stimulated contractions.
        Exp Neurol. 1979; 64: 401-413
        • Allen D.G.
        • Lamb G.D.
        • Westerblad H.
        Skeletal muscle fatigue: cellular mechanisms.
        Physiol Rev. 2008; 88: 287-332
        • Westerblad H.
        • Lee J.A.
        • Lännergren J.
        • Allen D.G.
        Cellular mechanisms of fatigue in skeletal muscle.
        Am J Physiol. 1991; 261: C195-209
        • Vanderthommen M.
        • Depresseux J.C.
        • Dauchat L.
        • Degueldre C.
        • Croisier J.L.
        • Crielaard J.M.
        Spatial distribution of blood flow in electrically stimulated human muscle: a positron emission tomography study.
        Muscle Nerve. 2000; 23: 482-489
        • Farina D.
        • Blanchietti A.
        • Pozzo M.
        • Merletti R.
        M-wave properties during progressive motor unit activation by transcutaneous stimulation.
        J Appl Physiol. 2004; 97: 545-555
        • Mesin L.
        • Merlo E.
        • Merletti R.
        • Orizio C.
        Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle.
        J Electromyogr Kinesiol. 2010; 20: 580-589
        • Okuma Y.
        • Bergquist A.J.
        • Hong M.
        • Chan K.M.
        • Collins D.F.
        Electrical stimulation site influences the spatial distribution of motor units recruited in tibialis anterior.
        Clin Neurophysiol. 2013; 124: 2257-2263
        • Adams G.R.
        • Harris R.T.
        • Woodard D.
        • Dudley G.A.
        Mapping of electrical muscle stimulation using MRI.
        J Appl Physiol. 1993; 74: 532-537
        • Rodriguez-Falces J.
        • Place N.
        Recruitment order of quadriceps motor units: Femoral nerve vs. direct quadriceps stimulation.
        Eur J Appl Physiol. 2013; 113: 3069-3077
        • Klakowicz P.M.
        • Baldwin E.R.
        • Collins D.F.
        Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans.
        J Neurophysiol. 2006; 96: 1293-1302
        • Bergquist A.J.
        • Clair J.M.
        • Collins D.F.
        Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae.
        J Appl Physiol. 2011; 110: 627-637
        • Gorgey A.S.
        • Mahoney E.
        • Kendall T.
        • Dudley G.A.
        Effects of neuromuscular electrical stimulation parameters on specific tension.
        Eur J Appl Physiol. 2006; 97: 737-744
        • Jubeau M.
        • Gondin J.
        • Martin A.
        • Sartorio A.
        • Maffiuletti N.A.
        Random motor unit activation by electrostimulation.
        Int J Sports Med. 2007; 28: 901-904
        • Gregory C.M.
        • Bickel C.S.
        Recruitment patterns in human skeletal muscle during electrical stimulation.
        Phys Ther. 2005; 85: 358-364
        • Enoka R.M.
        Activation order of motor axons in electrically evoked contractions.
        Muscle Nerve. 2002; 25: 763-764
        • Grill W.M.
        • Mortimer J.T.
        Stimulus waveforms for selective neural stimulation.
        IEEE Eng Med Biol Mag. 1995; 14: 375-385
        • Jaeger R.J.
        • Yarkony G.M.
        • Smith R.M.
        Standing the spinal cord injured patient by electrical stimulation: refinement of a protocol for clinical use.
        IEEE Trans Biomed Eng. 1989; 36: 720-728
        • Binder-Macleod S.A.
        • McDermond L.R.
        Changes in the force-frequency relationship of the human quadriceps femoris muscle following electrically and voluntarily induced fatigue.
        Phys Ther. 1992; 72: 95-104
        • Behringer M.
        • Grützner S.
        • Montag J.
        • McCourt M.
        • Ring M.
        • Mester J.
        Effects of stimulation frequency, amplitude, and impulse width on muscle fatigue.
        Muscle Nerve. 2016; 53: 608-616
        • Vanderthommen M.
        • Duteil S.
        • Wary C.
        • et al.
        A comparison of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans.
        J Appl Physiol. 2003; 94: 1012-1024
        • Michlovitz S.
        • Bellew J.
        • Nolan T.
        Modalities for therapeutic intervention.
        6th ed. FA Davis Company, Philadelphia2012
        • Doucet B.M.
        • Lam A.
        • Griffin L.
        Neuromuscular electrical stimulation for skeletal muscle function.
        Yale J Biol Med. 2012; 85: 201-215
        • Merton P.A.
        Voluntary strength and fatigue.
        J Physiol. 1954; 123: 553-564
        • Kent-Braun J.A.
        Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort.
        Eur J Appl Physiol Occup Physiol. 1999; 80: 57-63
        • Quiñonez M.
        • González F.
        • Morgado-Valle C.
        • DiFranco M.
        Effects of membrane depolarization and changes in extracellular [K(+)] on the Ca (2+) transients of fast skeletal muscle fibers. Implications for muscle fatigue.
        J Muscle Res Cell Motil. 2010; 31: 13-33
        • Bezanilla F.
        • Caputo C.
        • Gonzalez-Serratos H.
        • Venosa R.A.
        Sodium dependence of the inward spread of activation in isolated twitch muscle fibres of the frog.
        J Physiol. 1972; 223: 507-523
        • Badier M.
        • Guillot C.
        • Danger C.
        • Tagliarini F.
        • Jammes Y.
        M-wave changes after high- and low-frequency electrically induced fatigue in different muscles.
        Muscle Nerve. 1999; 22: 488-496
        • Jones D.A.
        High- and low-frequency fatigue revisited.
        Acta Physiol Scand. 1996; : 265-270
        • Grosprêtre S.
        • Gueugneau N.
        • Martin A.
        • Lepers R.
        Central contribution to electrically induced fatigue depends on stimulation frequency.
        Med Sci Sport Exerc. 2017; 49: 1530-1540
        • Vagg R.
        • Mogyoros I.
        • Kiernan M.C.
        • Burke D.
        Activity-dependent hyperpolarization of human motor axons produced by natural activity.
        J Physiol. 1998; 507: 919-925
        • Kiernan M.C.
        • Lin C.S.
        • Burke D.
        Differences in activity-dependent hyperpolarization in human sensory and motor axons.
        J Physiol. 2004; 558: 341-349
        • Matkowski B.
        • Lepers R.
        • Martin A.
        Torque decrease during submaximal evoked contractions of the quadriceps muscle is linked not only to muscle fatigue.
        J Appl Physiol. 2015; 118: 1136-1144
        • Papaiordanidou M.
        • Stevenot J.D.
        • Mustacchi V.
        • Vanoncini M.
        • Martin A.
        Electrically induced torque decrease reflects more than muscle fatigue.
        Muscle Nerve. 2014; 50: 604-607
        • Bostock H.
        • Cikurel K.
        • Burke D.
        Threshold tracking techniques in the study of human peripheral nerve.
        Muscle Nerve. 1998; 21: 137-158
        • Kiernan M.C.
        • Burke D.
        • Andersen K.V.
        • Bostock H.
        Multiple measures of axonal excitability: a new approach in clinical testing.
        Muscle Nerve. 2000; 23: 399-409
        • Chiou-Tan F.Y.
        • Tim R.W.
        • Gilchrist J.M.
        • et al.
        Literature review of the usefulness of repetitive nerve stimulation and single fiber EMG in the electrodiagnostic evaluation of patients with suspected myasthenia gravis or Lambert-Eaton myasthenic syndrome.
        Muscle Nerve. 2001; 24: 1239-1247
        • Bergquist A.J.
        • Wiest M.J.
        • Collins D.F.
        Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris.
        J Appl Physiol. 2012; 113: 78-89
        • Bergquist A.J.
        • Clair J.M.
        • Lagerquist O.
        • Mang C.S.
        • Okuma Y.
        • Collins D.F.
        Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley.
        Eur J Appl Physiol. 2011; 111: 2409-2426
        • Collins D.F.
        • Burke D.
        • Gandevia S.C.
        Large involuntary forces consistent with plateau-like behavior of human motoneurons.
        J Neurosci. 2001; 21: 4059-4065
        • Lagerquist O.
        • Walsh L.D.
        • Blouin J.S.
        • Collins D.F.
        • Gandevia S.C.
        Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation.
        J Appl Physiol. 2009; 107: 161-167
        • Collins D.F.
        Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation.
        Exerc Sport Sci Rev. 2007; 35: 102-109
        • Bergquist A.J.
        • Wiest M.J.
        • Okuma Y.
        • Collins D.F.
        H-reflexes reduce fatigue of evoked contractions after spinal cord injury.
        Muscle Nerve. 2014; 50: 224-234
        • Grill W.M.
        • Mortimer J.T.
        The effect of stimulus pulse duration on selectivity of neural stimulation.
        IEEE Trans Biomed Eng. 1996; 43: 161-166
        • Veale J.L.
        • Mark R.F.
        • Rees S.
        Differential sensitivity of motor and sensory fibres in human ulnar nerve.
        J Neurol Neurosurg Psychiatry. 1973; 36: 75-86
        • Burke D.
        • Kiernan M.C.
        • Bostock H.
        Excitability of human axons.
        Clin Neurophysiol. 2001; 112: 1575-1585
        • Mogyoros I.
        • Kiernan M.C.
        • Burke D.
        Strength-duration properties of human peripheral nerve.
        Brain. 1996; 119: 439-447
        • Wegrzyk J.
        • Foure A.
        • Le Fur Y.
        • et al.
        Responders to wide-pulse, high-frequency neuromuscular electrical stimulation show reduced metabolic demand: a 31P-MRS study in humans.
        PLoS One. 2015; 10: e0143972
        • Martin A.
        • Grospretre S.
        • Vilmen C.
        • et al.
        The etiology of muscle fatigue differs between two electrical stimulation protocols.
        Med Sci Sports Exerc. 2016; 48: 1474-1484
        • Baldwin E.R.
        • Klakowicz P.M.
        • Collins D.F.
        Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation.
        J Appl Physiol. 2006; 101: 228-240
        • Nguyen R.
        • Masani K.
        • Micera S.
        • Morari M.
        • Popovic M.R.
        Spatially distributed sequential stimulation reduces fatigue in paralyzed triceps surae muscles: a case study.
        Artif Organs. 2011; 35: 1174-1180
        • Malešević N.M.
        • Popović L.Z.
        • Schwirtlich L.
        • Popović D.B.
        Distributed low-frequency functional electrical stimulation delays muscle fatigue compared to conventional stimulation.
        Muscle Nerve. 2010; 42: 556-562
        • Popović L.Z.
        • Malešević N.M.
        Muscle fatigue of quadriceps in paraplegics: comparison between single vs. multi-pad electrode surface stimulation.
        Conf Proc IEEE Eng Med Biol Soc. 2009; 2009: 6785-6788
        • Sayenko D.G.
        • Nguyen R.
        • Hirabayashi T.
        • Popovic M.R.
        • Masani K.
        Method to reduce muscle fatigue during transcutaneous neuromuscular electrical stimulation in major knee and ankle muscle groups.
        Neurorehabil Neural Repair. 2015; 29: 722-733
        • Downey R.J.
        • Tate M.
        • Kawai H.
        • Dixon W.E.
        Comparing the force ripple during asynchronous and conventional stimulation.
        Muscle Nerve. 2014; 50: 549-555
        • Lou J.W.
        • Bergquist A.J.
        • Aldayel A.
        • Czitron J.
        • Collins D.F.
        Interleaved neuromuscular electrical stimulation reduces muscle fatigue.
        Muscle Nerve. 2017; 55: 179-189
        • Zehr E.P.
        Considerations for use of the Hoffmann reflex in exercise studies.
        Eur J Appl Physiol. 2002; 86: 455-468
        • Misiaszek J.E.
        The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function.
        Muscle Nerve. 2003; 28: 144-160
        • Wiest M.J.
        • Bergquist A.J.
        • Schimidt H.L.
        • Jones K.E.
        • Collins D.F.
        Interleaved neuromuscular electrical stimulation: motor unit recruitment overlap.
        Muscle Nerve. 2016; 55: 490-499
        • Graupe D.
        • Suliga P.
        • Prudian C.
        • Kohn K.H.
        Stochastically-modulated stimulation to slow down muscle fatigue at stimulated sites in paraplegics using functional electrical stimulation for leg extension.
        Neurol Res. 2000; 22: 703-704
        • Aksöz E.A.
        • Laubacher M.
        • Binder-Macleod S.
        • Hunt K.J.
        Effect of stochastic modulation of inter-pulse interval during stimulated isokinetic leg extension.
        Eur J Transl Myol. 2016; 26: 229-234
        • Indurthy M.
        • Griffin L.
        Effect of random interpulse interval modulation on neuromuscular fatigue.
        Muscle Nerve. 2007; 36: 807-815
        • Graham G.M.
        • Thrasher T.A.
        • Popovic M.R.
        The effect of random modulation of functional electrical stimulation parameters on muscle fatigue.
        Rehabilitation. 2006; 14: 38-45
        • Binder-Macleod S.A.
        • Scott W.B.
        Comparison of fatigue produced by various electrical stimulation trains.
        Acta Physiol Scand. 2001; 172: 195-203
        • Binder-Macleod S.A.
        • Lee S.C.
        • Russ D.W.
        • Kucharski L.J.
        Effects of activation pattern on human skeletal muscle fatigue.
        Muscle Nerve. 1998; 21: 1145-1152
        • Bickel C.S.
        • Slade J.M.
        • VanHiel L.R.
        • Warren G.L.
        • Dudley G.A.
        Variable-frequency-train stimulation of skeletal muscle after spinal cord injury.
        J Rehabil Res Dev. 2004; 41: 33-40
        • Routh G.R.
        • Durfee W.K.
        Doublet stimulation to reduce fatigue in electrically stimulated muscle during controlled leg lifts.
        Conf Proc IEEE Eng Med Biol Soc. 2003; 2: 1531-1534
        • Thomas C.K.
        • Griffin L.
        • Godfrey S.
        • Ribot-Ciscar E.
        • Butler J.E.
        Fatigue of paralyzed and control thenar muscles induced by variable or constant frequency stimulation.
        J Neurophysiol. 2003; 89: 2055-2064
        • Kebaetse M.B.
        • Turner A.E.
        • Binder-Macleod S.A.
        Effects of stimulation frequencies and patterns on performance of repetitive, nonisometric tasks.
        J Appl Physiol. 2002; 92: 109-116
        • Holcomb W.R.
        • Rubley M.D.
        • Randolph S.M.
        Increasing neuromuscular electrical stimulation amplitude to reduce the decline in knee extension torque.
        Athl Train Sport Heal Care. 2011; 3: 63-68
        • Kebaetse M.B.
        • Binder-Macleod S.A.
        Strategies that improve human skeletal muscle performance during repetitive, non-isometric contractions.
        Pflugers Arch. 2004; 448: 525-532
        • Kebaetse M.B.
        • Lee S.C.
        • Johnston T.E.
        • Binder-Macleod S.A.
        Strategies that improve paralyzed human quadriceps femoris muscle performance during repetitive, nonisometric contractions.
        Arch Phys Med Rehabil. 2005; 86: 2157-2164
        • Kesar T.
        • Chou L.W.
        • Binder-Macleod S.A.
        Effects of stimulation frequency versus pulse duration modulation on muscle fatigue.
        J Electromyogr Kinesiol. 2008; 18: 662-671
        • Griffin L.
        • Jun B.G.
        • Covington C.
        • Doucet B.M.
        Force output during fatigue with progressively increasing stimulation frequency.
        J Electromyogr Kinesiol. 2008; 18: 426-433