Advertisement
Clinical Research|Articles in Press

Targeting Lower Limb, Upper Limb, and Face Representation in the Primary Motor Cortex for the Practice of Neuronavigated Transcranial Magnetic Stimulation

      Abstract

      Objective

      The primary motor cortex (M1) is a usual target for therapeutic application of repetitive transcranial magnetic stimulation (rTMS), especially the region of hand motor representation. However, other M1 regions can be considered as potential rTMS targets, such as the region of lower limb or face representation. In this study, we assessed the localization of all these regions on magnetic resonance imaging (MRI) with the aim of defining three standardized M1 targets for the practice of neuronavigated rTMS.

      Materials and Methods

      A pointing task of these targets was performed by three rTMS experts on 44 healthy brain MRI data to assess interrater reliability (including the calculation of intraclass correlation coefficients [ICCs] and coefficients of variation [CoVs] and the construction of Bland-Altman plots). In addition, two “standard” brain MRI data were randomly interspersed with the other MRI data to assess intrarater reliability. A barycenter was calculated for each target (with x-y-z coordinates provided in normalized brain coordinate systems), in addition to the geodesic distance between the scalp projection of the barycenters of these different targets.

      Results

      Intrarater and interrater agreement was good, according to ICCs, CoVs, or Bland-Altman plots, although interrater variability was greater for anteroposterior (y) and craniocaudal (z) coordinates, especially for the face target. The scalp projection of the barycenters between the different cortical targets ranged from 32.4 to 35.5 mm for either the lower-limb-to-upper-limb target distance or the upper-limb-to-face target distance.

      Conclusions

      This work clearly delineates three different targets for the application of motor cortex rTMS that correspond to lower limb, upper limb, and face motor representations. These three targets are sufficiently spaced to consider that their stimulation can act on distinct neural networks.

      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'

      Subscribe:

      Subscribe to
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Lefaucheur J.P.
        Transcranial magnetic stimulation.
        Handb Clin Neurol. 2019; 160: 559-580
        • Lefaucheur J.P.
        • Aleman A.
        • Baeken C.
        • et al.
        Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014–2018).
        Clin Neurophysiol. 2020; 131: 474-528
        • Lefaucheur J.P.
        Cortical neurostimulation for neuropathic pain: state of the art and perspectives.
        Pain. 2016; 157: S81-S89
        • Lefaucheur J.P.
        • Hatem S.
        • Nineb A.
        • et al.
        Somatotopic organization of the analgesic effects of motor cortex rTMS in neuropathic pain.
        Neurology. 2006; 67: 1998-2004
        • Andre-Obadia N.
        • Magnin M.
        • Simon E.
        • Garcia-Larrea L.
        Somatotopic effects of rTMS in neuropathic pain? A comparison between stimulation over hand and face motor areas.
        Eur J Pain. 2018; 22: 707-715
        • Nguyen J.P.
        • Lefaucheur J.P.
        • Decq P.
        • et al.
        Chronic motor cortex stimulation in the treatment of central and neuropathic pain. Correlations between clinical, electrophysiological and anatomical data.
        Pain. 1999; 82: 245-251
        • Penfield W.
        • Boldrey E.
        Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation.
        Brain. 1937; 60: 389-443
        • Lefaucheur J.P.
        • de Andrade D.C.
        Intraoperative neurophysiologic mapping of the central cortical region for epidural electrode placement in the treatment of neuropathic pain by motor cortex stimulation.
        Brain Stimul. 2009; 2: 138-148
        • Ayache S.S.
        • Ahdab R.
        • Chalah M.A.
        • et al.
        Analgesic effects of navigated motor cortex rTMS in patients with chronic neuropathic pain.
        Eur J Pain. 2016; 20: 1413-1422
        • Lefaucheur J.P.
        • Nguyen J.P.
        A practical algorithm for using rTMS to treat patients with chronic pain.
        Neurophysiol Clin. 2019; 49: 301-307
        • Lefaucheur J.P.
        Why image-guided navigation becomes essential in the practice of transcranial magnetic stimulation.
        Neurophysiol Clin. 2010; 40: 1-5
        • Ahdab R.
        • Ayache S.S.
        • Brugières P.
        • Goujon C.
        • Lefaucheur J.P.
        Comparison of "standard" and "navigated" procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression.
        Neurophysiol Clin. 2010; 40: 27-36
        • Mylius V.
        • Ayache S.S.
        • Ahdab R.
        • et al.
        Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: inter-rater reliability, accuracy, and influence of gender and age.
        Neuroimage. 2013; 78: 224-232
        • Holmes C.J.
        • Hoge R.
        • Collins L.
        • Woods R.
        • Toga A.W.
        • Evans A.C.
        Enhancement of MR images using registration for signal averaging.
        J Comput Assist Tomogr. 1998; 22: 324-333
        • Lalys F.
        • Haegelen C.
        • Ferre J.C.
        • El-Ganaoui O.
        • Jannin P.
        Construction and assessment of a 3-T MRI brain template.
        Neuroimage. 2010; 49: 345-354
        • Yousry T.A.
        • Schmid U.D.
        • Alkadhi H.
        • et al.
        Localization of the motor hand area to a knob on the precentral gyrus. A new landmark.
        Brain. 1997; 120: 141-157
        • Ahdab R.
        • Ayache S.S.
        • Farhat W.H.
        • et al.
        Reappraisal of the anatomical landmarks of motor and premotor cortical regions for image-guided brain navigation in TMS practice.
        Hum Brain Mapp. 2014; 35: 2435-2447
        • Shrout P.E.
        • Fleiss J.L.
        Intraclass correlations: uses in assessing rater reliability.
        Psychol Bull. 1979; 86: 420-428
        • Bland J.M.
        • Altman D.G.
        Statistical methods for assessing agreement between two methods of clinical measurement.
        Lancet. 1986; 1: 307-310
        • Carstensen B.
        • Simpson J.
        • Gurrin L.C.
        Statistical models for assessing agreement in method comparison studies with replicate measurements.
        Int J Biostat. 2008; 4 (Article 16)
        • Boërio D.
        • Hogrel J.Y.
        • Lefaucheur J.P.
        • et al.
        Stimulus-response curve of human motor nerves: multicenter assessment of various indexes.
        Neurophysiol Clin. 2008; 38: 31-38
        • Talairach J.
        • Tournoux P.
        Co-planar Stereotactic Atlas of the Human Brain: 3- Dimensional Proportional System: An Approach to Cerebral Imaging.
        Thieme Medical Publishers, 1988
        • Collins D.L.
        • Zijdenbos A.P.
        • Kollokian V.
        • et al.
        Design and construction of a realistic digital brain phantom.
        IEEE Trans Med Imaging. 1998; 17: 463-468
        • Säisänen L.
        • Julkunen P.
        • Kemppainen S.
        • et al.
        Locating and outlining the cortical motor representation areas of facial muscles with navigated transcranial magnetic stimulation.
        Neurosurgery. 2015; 77 ([discussion: 405]): 394-405
        • Weiss C.
        • Nettekoven C.
        • Rehme A.K.
        • et al.
        Mapping the hand, foot and face representations in the primary motor cortex - retest reliability of neuronavigated TMS versus functional MRI.
        Neuroimage. 2013; 66: 531-542
        • Deng Z.D.
        • Lisanby S.H.
        • Peterchev A.V.
        Electric field depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs.
        Brain Stimul. 2013; 6: 1-13
        • Gomez L.J.
        • Goetz S.M.
        • Peterchev A.V.
        Design of transcranial magnetic stimulation coils with optimal trade-off between depth, focality, and energy.
        J Neural Eng. 2018; 15046033
        • Gomez-Tames J.
        • Hamasaka A.
        • Laakso I.
        • Hirata A.
        • Ugawa Y.
        Atlas of optimal coil orientation and position for TMS: a computational study.
        Brain Stimul. 2018; 11: 839-848
        • Schmidt S.
        • Bathe-Peters R.
        • Fleischmann R.
        • Rönnefarth M.
        • Scholz M.
        • Brandt S.A.
        Nonphysiological factors in navigated TMS studies; confounding covariates and valid intracortical estimates.
        Hum Brain Mapp. 2015; 36: 40-49
        • Thielscher A.
        • Kammer T.
        Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency.
        Clin Neurophysiol. 2004; 115: 1697-1708
        • Jetté F.
        • Côté I.
        • Meziane H.B.
        • Mercier C.
        Effect of single-session repetitive transcranial magnetic stimulation applied over the hand versus leg motor area on pain after spinal cord injury.
        Neurorehabil Neural Repair. 2013; 27: 636-643
        • Hodaj H.
        • Payen J.F.
        • Lefaucheur J.P.
        Therapeutic impact of motor cortex rTMS in patients with chronic neuropathic pain even in the absence of an analgesic response. A case report.
        Neurophysiol Clin. 2018; 48: 303-308
        • Hodaj H.
        • Payen J.F.
        • Hodaj E.
        • et al.
        Long-term treatment of chronic orofacial, pudendal, and central neuropathic limb pain with repetitive transcranial magnetic stimulation of the motor cortex.
        Clin Neurophysiol. 2020; 131: 1423-1432
        • Nguyen J.P.
        • Nizard J.
        • Keravel Y.
        • Lefaucheur J.P.
        Invasive brain stimulation for the treatment of neuropathic pain.
        Nat Rev Neurol. 2011; 7: 699-709
        • Ruohonen J.
        • Karhu J.
        Navigated transcranial magnetic stimulation.
        Neurophysiol Clin. 2010; 40: 7-17
        • Nauczyciel C.
        • Hellier P.
        • Morandi X.
        • et al.
        Assessment of standard coil positioning in transcranial magnetic stimulation in depression.
        Psychiatry Res. 2011; 186: 232-238

      Comment