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J Neurol Surg A Cent Eur Neurosurg 2020; 81(02): 147-154
DOI: 10.1055/s-0040-1701624
Original Article
Georg Thieme Verlag KG Stuttgart · New York

1 Hz Repetitive Transcranial Magnetic Stimulation of the Primary Motor Cortex: Impact on Excitability and Task Performance in Healthy Subjects

Melina Engelhardt
1   Department of Neurosurgery, Charité Universitatsmedizin Berlin, Berlin, Germany
2   Einstein Center for Neurosciences, Charité Universitatsmedizin Berlin, Berlin, Germany
,
Thomas Picht
1   Department of Neurosurgery, Charité Universitatsmedizin Berlin, Berlin, Germany
3   Cluster of Excellence, Matters of Activity, Image Space Material, Humboldt University of Berlin, Berlin, Germany
› Author Affiliations
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Publication History

11 December 2018

08 February 2019

Publication Date:
11 February 2020 (online)

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Abstract

Objective Neuronavigated repetitive transcranial stimulation (rTMS) at a frequency of 1 Hz was shown to reduce excitability in underlying brain areas while increasing excitability in the opposite hemisphere. In stroke patients, this principle is used to normalize activity between the lesioned and healthy hemispheres and to facilitate rehabilitation. However, standardization is lacking in applied protocols, and there is a poor understanding of the underlying physiologic mechanisms. Furthermore, the influence of hemispheric dominance on the intervention has not been studied before. A systematic evaluation of the effects in healthy subjects would deepen the understanding of these mechanisms and offer insights into ways to improve the intervention.

Methods Twenty healthy subjects underwent five 15-minute sessions of neuronavigated rTMS or sham stimulation over their dominant or nondominant motor cortex. Dominance was assessed with the Edinburgh Handedness Inventory. Changes in both hemispheres were measured using behavioral parameters (finger tapping, grip force, and finger dexterity) and TMS measures (resting motor threshold, recruitment curve, motor area, and cortical silent period).

Results All subjects tolerated the stimulation well. A pronounced improvement was noted in finger tapping scores over the nonstimulated hemisphere as well as a nonsignificant reduction of the cortical silent period in the stimulated hemisphere, indicating a differential effect of the rTMS on both hemispheres. Grip force remained at the baseline level in the rTMS group while decreasing in the sham group, suggesting the rTMS counterbalanced the effects of fatigue. Lastly, dominance did not influence any of the observed effects.

Conclusions This study shows the capability of the applied low-frequency rTMS protocol to modify excitability of underlying brain areas as well as the contralateral hemisphere. It also highlights the need for a better understanding of underlying mechanisms and the identification of predictors for responsiveness to rTMS. However, results should be interpreted with caution because of the small sample size.

Keywords

repetitive transcranial magnetic stimulation - neuronavigated brain stimulation - motor cortex - cortical excitability
 

  • References

  • 1 Broeks JG, Lankhorst GJ, Rumping K, Prevo AJH. The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil 1999; 21 (08) 357-364
    CrossrefPubMedGoogle Scholar
  • 2 Rossini PM, Burke D, Chen R. , et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015; 126 (06) 1071-1107
    CrossrefPubMedGoogle Scholar
  • 3 Lefaucheur JP, André-Obadia N, Antal A. , et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 2014; 125 (11) 2150-2206
    CrossrefPubMedGoogle Scholar
  • 4 Hsu WY, Cheng CH, Liao KK, Lee IH, Lin YY. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke 2012; 43 (07) 1849-1857
    CrossrefPubMedGoogle Scholar
  • 5 Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke?. Lancet Neurol 2006; 5 (08) 708-712
    CrossrefPubMedGoogle Scholar
  • 6 Kinsbourne M. Mechanisms of hemispheric interaction in man. In: Kinsbourne M. , ed. Hemispheric Disconnection and Cerebral Function. Springfield, IL: Thomas; 1974: 260-285
    Google Scholar
  • 7 Nowak DA, Grefkes C, Dafotakis M. , et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol 2008; 65 (06) 741-747
    PubMedGoogle Scholar
  • 8 Bäumer T, Lange R, Liepert J. , et al. Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 2003; 20 (01) 550-560
    CrossrefPubMedGoogle Scholar
  • 9 Bashir S, Edwards D, Pascual-Leone A. Neuronavigation increases the physiologic and behavioral effects of low-frequency rTMS of primary motor cortex in healthy subjects. Brain Topogr 2011; 24 (01) 54-64
    CrossrefPubMedGoogle Scholar
  • 10 Lüdemann-Podubecká J, Bösl K, Theilig S, Wiederer R, Nowak DA. The effectiveness of 1 Hz rTMS over the primary motor area of the unaffected hemisphere to improve hand function after stroke depends on hemispheric dominance. Brain Stimul 2015; 8 (04) 823-830
    CrossrefPubMedGoogle Scholar
  • 11 Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9 (01) 97-113
    CrossrefPubMedGoogle Scholar
  • 12 Picht T, Schmidt S, Brandt S. , et al. Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 2011; 69 (03) 581-588 ; discussion 588
    CrossrefPubMedGoogle Scholar
  • 13 Rosenstock T, Grittner U, Acker G. , et al. Risk stratification in motor area-related glioma surgery based on navigated transcranial magnetic stimulation data. J Neurosurg 2017; 126 (04) 1227-1237
    CrossrefPubMedGoogle Scholar
  • 14 Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 1997; 114 (02) 329-338
    CrossrefPubMedGoogle Scholar
  • 15 Vaalto S, Julkunen P, Säisänen L, Könönen M, Määttä S, Karhu J. Long-term plasticity may be manifested as reduction or expansion of cortical representations of actively used muscles in motor skill specialists. Neuroreport 2013; 24 (11) 596-600
    CrossrefPubMedGoogle Scholar
  • 16 Reitan RM. Manual for Administration of Neuropsychological Test Batteries for Adults and Children. Indianapolis, IN: Neuropsychology Laboratory; 1969
    Google Scholar
  • 17 Wang Y-C, Bohannon RW, Kapellusch J, Garg A, Gershon RC. Dexterity as measured with the 9-Hole Peg Test (9-HPT) across the age span. J Hand Ther 2015; 28 (01) 53-59 ; quiz 60
    CrossrefPubMedGoogle Scholar
  • 18 West BT. Analyzing longitudinal data with the linear mixed models procedure in SPSS. Eval Health Prof 2009; 32 (03) 207-228
    CrossrefPubMedGoogle Scholar
  • 19 Fitzgerald PB, Fountain S, Daskalakis ZJ. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 2006; 117 (12) 2584-2596
    CrossrefPubMedGoogle Scholar
  • 20 Lee M, Kim SE, Kim WS. , et al. Cortico-cortical modulation induced by 1-Hz repetitive transcranial magnetic stimulation of the temporal cortex. J Clin Neurol 2013; 9 (02) 75-82
    CrossrefPubMedGoogle Scholar
  • 21 Fierro B, Piazza A, Brighina F, La Bua V, Buffa D, Oliveri M. Modulation of intracortical inhibition induced by low- and high-frequency repetitive transcranial magnetic stimulation. Exp Brain Res 2001; 138 (04) 452-457
    CrossrefPubMedGoogle Scholar
  • 22 Fitzgerald PB, Brown TL, Marston NAU. , et al. Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophr Res 2004; 71 (01) 17-26
    CrossrefPubMedGoogle Scholar
  • 23 Kallioniemi E, Säisänen L, Könönen M, Awiszus F, Julkunen P. On the estimation of silent period thresholds in transcranial magnetic stimulation. Clin Neurophysiol 2014; 125 (11) 2247-2252
    CrossrefPubMedGoogle Scholar
  • 24 Säisänen L, Julkunen P, Niskanen E. , et al. Motor potentials evoked by navigated transcranial magnetic stimulation in healthy subjects. J Clin Neurophysiol 2008; 25 (06) 367-372
    CrossrefPubMedGoogle Scholar
  • 25 Harvey RL, Edwards D, Dunning K. , et al; NICHE Trial Investigators *. Randomized sham-controlled trial of navigated repetitive transcranial magnetic stimulation for motor recovery in stroke. Stroke 2018; 49 (09) 2138-2146
    CrossrefPubMedGoogle Scholar
  • 26 Loo CK, Taylor JL, Gandevia SC, McDarmont BN, Mitchell PB, Sachdev PS. Transcranial magnetic stimulation (TMS) in controlled treatment studies: are some “sham” forms active?. Biol Psychiatry 2000; 47 (04) 325-331
    CrossrefPubMedGoogle Scholar
  • 27 Bashir S, Perez JM, Horvath JC. , et al. Differential effects of motor cortical excitability and plasticity in young and old individuals: a transcranial magnetic stimulation (TMS) study. Front Aging Neurosci 2014; 6: 111
    PubMedGoogle Scholar
  • 28 Ridding MC, Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 2010; 588 (Pt 13): 2291-2304
    CrossrefPubMedGoogle Scholar
  • 29 Gratton C, Lee TG, Nomura EM, D'Esposito M. Perfusion MRI indexes variability in the functional brain effects of theta-burst transcranial magnetic stimulation. PLoS One 2014; 9 (07) e101430
    CrossrefPubMedGoogle Scholar
  • 30 Homan P, Kindler J, Hauf M, Hubl D, Dierks T. Cerebral blood flow identifies responders to transcranial magnetic stimulation in auditory verbal hallucinations. Transl Psychiatry 2012; 2: e189
    CrossrefPubMedGoogle Scholar
  • 31 Weiduschat N, Dubin MJ. Prefrontal cortical blood flow predicts response of depression to rTMS. J Affect Disord 2013; 150 (02) 699-702
    CrossrefPubMedGoogle Scholar