Advertisement

Anodal Transcranial Direct Current Stimulation Alters Elbow Flexor Muscle Recruitment Strategies

  • Chandramouli Krishnan
    Correspondence
    Corresponding author. Neuromuscular & Rehabilitation Robotics Laboratory (NeuRRo Lab), Department of Physical Medicine and Rehabilitation, University of Michigan, 325 E Eisenhower Parkway, Suite 3013, Ann Arbor, MI 48108, USA. Tel.: +1 319 321 0117; fax: +1 734 615 1770.
    Affiliations
    Department of Physical Medicine and Rehabilitation, University of Michigan Medical School, Ann Arbor, MI, USA

    Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL, USA

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
    Search for articles by this author
  • Rajiv Ranganathan
    Affiliations
    Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL, USA

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
    Search for articles by this author
  • Shailesh S. Kantak
    Affiliations
    Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL, USA

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
    Search for articles by this author
  • Yasin Y. Dhaher
    Affiliations
    Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL, USA

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
    Search for articles by this author
  • William Z. Rymer
    Affiliations
    Sensory Motor Performance Program, Rehabilitation Institute of Chicago, IL, USA

    Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
    Search for articles by this author
Published:January 31, 2014DOI:https://doi.org/10.1016/j.brs.2014.01.057

      Abstract

      Background

      Transcranial direct current stimulation (tDCS) is known to reliably alter motor cortical excitability in a polarity dependent fashion such that anodal stimulation increases cortical excitability and cathodal stimulation inhibits cortical excitability. However, the effect of tDCS on agonist and antagonist volitional muscle activation is currently not known.

      Objective

      This study investigated the effect of motor cortical anodal tDCS on EMG/force relationships of biceps brachii (agonist) and triceps brachii (antagonist) using surface electromyography (EMG).

      Methods

      Eighteen neurologically intact adults (9 tDCS and 9 controls) participated in this study. EMG/force relationships were established by having subjects perform submaximal isometric contractions at several force levels (12.5%, 25%, 37.5%, and 50% of maximum).

      Results

      Results showed that anodal tDCS significantly affected the EMG/force relationship of the biceps brachii muscle. Specifically, anodal tDCS increased the magnitude of biceps brachii activation at 37.5% and 50% of maximum. Anodal tDCS also resulted in an increase in the peak force and EMG values during maximal contractions as compared to the control condition. EMG analyses of other elbow muscles indicated that the increase in biceps brachii activation after anodal tDCS was not related to alterations in synergistic or antagonistic muscle activity.

      Conclusions

      Our results indicate that anodal tDCS significantly affects the voluntary EMG/force relationship of the agonist muscles without altering the coactivation of the antagonistic muscles. The most likely explanation for the observed greater EMG per unit force after anodal tDCS appears to be related to alterations in motor unit recruitment strategies.

      Keywords

      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'

      References

        • Bashir S.
        • Mizrahi I.
        • Weaver K.
        • Fregni F.
        • Pascual-Leone A.
        Assessment and modulation of neural plasticity in rehabilitation with transcranial magnetic stimulation.
        PM R. 2010; 2: S253-S268
        • Bolognini N.
        • Pascual-Leone A.
        • Fregni F.
        Using non-invasive brain stimulation to augment motor training-induced plasticity.
        J Neuroeng Rehabil. 2009; 6: 8
        • Najib U.
        • Bashir S.
        • Edwards D.
        • Rotenberg A.
        • Pascual-Leone A.
        Transcranial brain stimulation: clinical applications and future directions.
        Neurosurg Clin N Am. 2011; 22: 233-251
        • Reis J.
        • Robertson E.
        • Krakauer J.W.
        • et al.
        Consensus: “can tDCS and TMS enhance motor learning and memory formation?”.
        Brain Stimul. 2008; 1: 363-369
        • Thibaut A.
        • Chatelle C.
        • Gosseries O.
        • Laureys S.
        • Bruno M.A.
        Transcranial direct current stimulation: a new tool for neurostimulation.
        Rev Neurol (Paris). 2013; 169: 108-120
        • Liebetanz D.
        • Nitsche M.A.
        • Tergau F.
        • Paulus W.
        Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability.
        Brain. 2002; 125: 2238-2247
        • Nitsche M.A.
        • Paulus W.
        Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation.
        J Physiol. 2000; 527: 633-639
        • Brasil-Neto J.P.
        Learning, memory, and transcranial direct current stimulation.
        Front Psychiatry. 2012; 3: 80
        • Nitsche M.A.
        Beyond the target area: remote effects of non-invasive brain stimulation in humans.
        J Physiol. 2011; 589: 3053-3054
        • Galea J.M.
        • Celnik P.
        Brain polarization enhances the formation and retention of motor memories.
        J Neurophysiol. 2009; 102: 294-301
        • Kantak S.S.
        • Mummidisetty C.K.
        • Stinear J.W.
        Primary motor and premotor cortex in implicit sequence learning – evidence for competition between implicit and explicit human motor memory systems.
        Eur J Neurosci. 2012; 36: 2710-2715
        • Madhavan S.
        • Weber 2nd, K.A.
        • Stinear J.W.
        Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation.
        Exp Brain Res. 2011; 209: 9-17
        • Reis J.
        • Schambra H.M.
        • Cohen L.G.
        • et al.
        Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation.
        Proc Natl Acad Sci U S A. 2009; 106: 1590-1595
        • Schambra H.M.
        • Abe M.
        • Luckenbaugh D.A.
        • Reis J.
        • Krakauer J.W.
        • Cohen L.G.
        Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study.
        J Neurophysiol. 2011; 106: 652-661
        • Marshall L.
        • Molle M.
        • Hallschmid M.
        • Born J.
        Transcranial direct current stimulation during sleep improves declarative memory.
        J Neurosci. 2004; 24: 9985-9992
        • Kitago T.
        • Krakauer J.W.
        Motor learning principles for neurorehabilitation.
        Handb Clin Neurol. 2013; 110: 93-103
        • Schweighofer N.
        • Choi Y.
        • Winstein C.
        • Gordon J.
        Task-oriented rehabilitation robotics.
        Am J Phys Med Rehabil. 2012; 91: S270-S279
        • Adeyemo B.O.
        • Simis M.
        • Macea D.D.
        • Fregni F.
        Systematic review of parameters of stimulation, clinical trial design characteristics, and motor outcomes in non-invasive brain stimulation in stroke.
        Front Psychiatry. 2012; 3: 88
        • Butler A.J.
        • Shuster M.
        • O'Hara E.
        • Hurley K.
        • Middlebrooks D.
        • Guilkey K.
        A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors.
        J Hand Ther. 2013; 26 (quiz 71): 162-170
        • Lefebvre S.
        • Laloux P.
        • Peeters A.
        • Desfontaines P.
        • Jamart J.
        • Vandermeeren Y.
        Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients.
        Front Hum Neurosci. 2012; 6: 343
        • Zimerman M.
        • Heise K.F.
        • Hoppe J.
        • Cohen L.G.
        • Gerloff C.
        • Hummel F.C.
        Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand.
        Stroke. 2012; 43: 2185-2191
        • Cogiamanian F.
        • Marceglia S.
        • Ardolino G.
        • Barbieri S.
        • Priori A.
        Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas.
        Eur J Neurosci. 2007; 26: 242-249
        • Hendy A.M.
        • Kidgell D.J.
        Anodal tDCS applied during strength training enhances motor cortical plasticity.
        Med Sci Sports Exerc. 2013; 45: 1721-1729
        • Hummel F.C.
        • Voller B.
        • Celnik P.
        • et al.
        Effects of brain polarization on reaction times and pinch force in chronic stroke.
        BMC Neurosci. 2006; 7: 73
        • Lefebvre S.
        • Thonnard J.L.
        • Laloux P.
        • Peeters A.
        • Jamart J.
        • Vandermeeren Y.
        Single session of dual-tDCS transiently improves precision grip and dexterity of the paretic hand after stroke.
        Neurorehabil Neural Repair. 2014; 28: 100-110
        • Tanaka S.
        • Hanakawa T.
        • Honda M.
        • Watanabe K.
        Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation.
        Exp Brain Res. 2009; 196: 459-465
        • Tanaka S.
        • Takeda K.
        • Otaka Y.
        • et al.
        Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke.
        Neurorehabil Neural Repair. 2011; 25: 565-569
        • Mathiowetz V.
        • Weber K.
        • Volland G.
        • Kashman N.
        Reliability and validity of grip and pinch strength evaluations.
        J Hand Surg Am. 1984; 9: 222-226
        • Petersen P.
        • Petrick M.
        • Connor H.
        • Conklin D.
        Grip strength and hand dominance: challenging the 10% rule.
        Am J Occup Ther. 1989; 43: 444-447
        • Krishnan C.
        • Huston K.
        • Amendola A.
        • Williams G.N.
        Quadriceps and hamstrings muscle control in athletic males and females.
        J Orthop Res. 2008; 26: 800-808
        • Krishnan C.
        • Williams G.N.
        Sex differences in quadriceps and hamstrings EMG-moment relationships.
        Med Sci Sports Exerc. 2009; 41: 1652-1660
        • Ng A.V.
        • Kent-Braun J.A.
        Slowed muscle contractile properties are not associated with a decreased EMG/force relationship in older humans.
        J Gerontol A Biol Sci Med Sci. 1999; 54: B452-B458
        • Krishnan C.
        • Allen E.J.
        • Williams G.N.
        Effect of knee position on quadriceps muscle force steadiness and activation strategies.
        Muscle Nerve. 2011; 43: 563-573
        • Krishnan C.
        • Williams G.N.
        Factors explaining chronic knee extensor strength deficits after ACL reconstruction.
        J Orthop Res. 2011; 29: 633-640
        • Ranganathan R.
        • Krishnan C.
        Extracting synergies in gait: using EMG variability to evaluate control strategies.
        J Neurophysiol. 2012; 108: 1537-1544
        • Krishnan C.
        • Williams G.N.
        Variability in antagonist muscle activity and peak torque during isometric knee strength testing.
        Iowa Orthop J. 2009; 29: 149-158
        • Krishnan C.
        • Williams G.N.
        Error associated with antagonist muscle activity in isometric knee strength testing.
        Eur J Appl Physiol. 2010; 109: 527-536
        • Bigland-Ritchie B.
        EMG/force relations and fatigue of human voluntary contractions.
        Exerc Sport Sci Rev. 1981; 9: 75-117
        • Tang A.
        • Rymer W.Z.
        Abnormal force – EMG relations in paretic limbs of hemiparetic human subjects.
        J Neurol Neurosurg Psychiatry. 1981; 44: 690-698
        • Suresh N.L.
        • Zhou P.
        • Rymer W.Z.
        Abnormal EMG-force slope estimates in the first dorsal interosseous of hemiparetic stroke survivors.
        Conf Proc IEEE Eng Med Biol Soc. 2008; 2008: 3562-3565
        • Henneman E.
        Relation between size of neurons and their susceptibility to discharge.
        Science. 1957; 126: 1345-1347
        • Henneman E.
        • Somjen G.
        • Carpenter D.O.
        Functional significance of cell size in spinal motoneurons.
        J Neurophysiol. 1965; 28: 560-580
        • Kukulka C.G.
        • Clamann H.P.
        Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions.
        Brain Res. 1981; 219: 45-55
        • Keenan K.G.
        • Farina D.
        • Maluf K.S.
        • Merletti R.
        • Enoka R.M.
        Influence of amplitude cancellation on the simulated surface electromyogram.
        J Appl Physiol. 2005; 98: 120-131
        • Keenan K.G.
        • Farina D.
        • Merletti R.
        • Enoka R.M.
        Amplitude cancellation reduces the size of motor unit potentials averaged from the surface EMG.
        J Appl Physiol. 2006; 100: 1928-1937
        • Zhou P.
        • Rymer W.Z.
        Factors governing the form of the relation between muscle force and the EMG: a simulation study.
        J Neurophysiol. 2004; 92: 2878-2886
        • Yao W.
        • Fuglevand R.J.
        • Enoka R.M.
        Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions.
        J Neurophysiol. 2000; 83: 441-452
        • Roche N.
        • Lackmy A.
        • Achache V.
        • Bussel B.
        • Katz R.
        Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects.
        J Physiol. 2011; 589: 2813-2826
        • Kan B.
        • Dundas J.E.
        • Nosaka K.
        Effect of transcranial direct current stimulation on elbow flexor maximal voluntary isometric strength and endurance.
        Appl Physiol Nutr Metab. 2013; 38: 734-739
        • Lampropoulou S.I.
        • Nowicky A.V.
        The effect of transcranial direct current stimulation on perception of effort in an isolated isometric elbow flexion task.
        Motor Control. 2013; 17: 412-426
        • Klein C.S.
        • Brooks D.
        • Richardson D.
        • McIlroy W.E.
        • Bayley M.T.
        Voluntary activation failure contributes more to plantar flexor weakness than antagonist coactivation and muscle atrophy in chronic stroke survivors.
        J Appl Physiol. 2010; 109: 1337-1346
        • Klein C.S.
        • Power G.A.
        • Brooks D.
        • Rice C.L.
        Neural and muscular determinants of dorsiflexor weakness in chronic stroke survivors.
        Motor Control. 2013; 17: 283-297
        • Madhavan S.
        • Krishnan C.
        • Jayaraman A.
        • Rymer W.Z.
        • Stinear J.W.
        Corticospinal tract integrity correlates with knee extensor weakness in chronic stroke survivors.
        Clin Neurophysiol. 2011; 122: 1588-1594
        • Palmieri-Smith R.M.
        • Thomas A.C.
        A neuromuscular mechanism of posttraumatic osteoarthritis associated with ACL injury.
        Exerc Sport Sci Rev. 2009; 37: 147-153
        • Thomas A.C.
        • Stevens-Lapsley J.E.
        Importance of attenuating quadriceps activation deficits after total knee arthroplasty.
        Exerc Sport Sci Rev. 2012; 40: 95-101
        • Williams G.N.
        • Buchanan T.S.
        • Barrance P.J.
        • Axe M.J.
        • Snyder-Mackler L.
        Quadriceps weakness, atrophy, and activation failure in predicted noncopers after anterior cruciate ligament injury.
        Am J Sports Med. 2005; 33: 402-407
        • Snyder-Mackler L.
        • Ladin Z.
        • Schepsis A.A.
        • Young J.C.
        Electrical stimulation of the thigh muscles after reconstruction of the anterior cruciate ligament. Effects of electrically elicited contraction of the quadriceps femoris and hamstring muscles on gait and on strength of the thigh muscles.
        J Bone Joint Surg Am. 1991; 73: 1025-1036
        • Stevens-Lapsley J.E.
        • Balter J.E.
        • Wolfe P.
        • Eckhoff D.G.
        • Kohrt W.M.
        Early neuromuscular electrical stimulation to improve quadriceps muscle strength after total knee arthroplasty: a randomized controlled trial.
        Phys Ther. 2012; 92: 210-226
        • Petterson S.
        • Snyder-Mackler L.
        The use of neuromuscular electrical stimulation to improve activation deficits in a patient with chronic quadriceps strength impairments following total knee arthroplasty.
        J Orthop Sports Phys Ther. 2006; 36: 678-685
        • O'Connell N.E.
        • Cossar J.
        • Marston L.
        • et al.
        Rethinking clinical trials of transcranial direct current stimulation: participant and assessor blinding is inadequate at intensities of 2 mA.
        PLoS One. 2012; 7: e47514