Advertisement

Brain Topography

, Volume 29, Issue 4, pp 590–597 | Cite as

The Hand Motor Hotspot is not Always Located in the Hand Knob: A Neuronavigated Transcranial Magnetic Stimulation Study

  • Rechdi Ahdab
  • Samar S. Ayache
  • Pierre Brugières
  • Wassim H. Farhat
  • Jean-Pascal Lefaucheur
Original Paper

Abstract

The hand motor hot spot (hMHS) is one of the most salient parameters in transcranial magnetic stimulation (TMS) practice, notably used for targeting. It is commonly accepted that the hMHS corresponds to the hand representation within the primary motor cortex (M1). Anatomical and imaging studies locate this representation in a region of the central sulcus called the “hand knob”. The aim of this study was to determine if the hMHS location corresponds to its expected location at the hand knob. Twelve healthy volunteers and eleven patients with chronic neuropathic pain of various origins, but not related to a brain lesion, were enrolled. Morphological magnetic resonance imaging of the brain was normal in all participants. Both hemispheres were studied in all participants except four (two patients and two healthy subjects). Cortical mapping of the hand motor area was conducted using a TMS-dedicated navigation system and recording motor evoked potentials (MEPs) in the contralateral first dorsal interosseous (FDI) muscle. We then determined the anatomical position of the hMHS, defined as the stimulation site providing the largest FDI-MEPs. In 45 % of hemispheres of normal subjects and 25 % of hemispheres of pain patients, the hMHS was located over the central sulcus, most frequently at the level of the hand knob. However, in the other cases, the hMHS was located outside M1, most frequently anteriorly over the precentral or middle frontal gyrus. This study shows that the hMHS does not always correspond to the hand knob and M1 location in healthy subjects or patients. Therefore, image-guided navigation is needed to improve the anatomical accuracy of TMS targeting, even for M1.

Keywords

Motor cortex Motor hotspot Navigation Sulcal anatomy Transcranial magnetic stimulation 

References

  1. Ahdab R, Ayache SS, Brugières P et al (2010) Comparison of “standard” and “navigated” procedures of TMS coil positioning over motor, premotor and prefrontal targets in depressive patients. Neurophysiol Clin 40:27–36CrossRefPubMedGoogle Scholar
  2. Ahdab R, Ayache SS, Farhat WH et al (2014) Reappraisal of the anatomical landmarks of motor and premotor cortical regions for image-guided brain navigation in TMS practice. Hum Brain Mapp 35:2435–2447CrossRefPubMedGoogle Scholar
  3. Brodmann K (1909) Vergleichende Lokalisationslehre der Groβhirnrinde in ihren 883 Prinzipien dargestellt auf Grund des Zellaufbaues. Barth, LeipzigGoogle Scholar
  4. Classen J, Knorr U, Werhahn KJ et al (1998) Multimodal output mapping of human central motor representation on different spatial scales. J Physiol 512:163–179CrossRefPubMedPubMedCentralGoogle Scholar
  5. Danner N, Julkunen P, Könönen M, Säisänen L, Nurkkala J, Karhu J (2008) Navigated transcranial magnetic stimulation and computed electric field strength reduce stimulator-dependent differences in the motor threshold. J Neurosci Methods 174:116–122CrossRefPubMedGoogle Scholar
  6. Deng ZD, Lisanby SH, Peterchev AV (2013) Electric field depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs. Brain Stimul 6:1–13CrossRefPubMedGoogle Scholar
  7. Denslow S, Bohning DE, Bohning PA et al (2005) An increased precision comparison of TMS-induced motor cortex BOLD fMRI response for image-guided versus function-guided coil placement. Cogn Behav Neurol 18:119–126CrossRefPubMedGoogle Scholar
  8. Diekhoff S, Uludag K, Sparing R et al (2011) Functional localization in the human brain: gradient-echo, spin-echo, and arterial spin-labeling fMRI compared with neuronavigated TMS. Hum Brain Mapp 32:341–357CrossRefPubMedGoogle Scholar
  9. Foerster O (1936) The motor cortex in man in the light of Hughlings Jackson’s doctrines. Brain 59:135–159CrossRefGoogle Scholar
  10. Geyer S, Matelli M, Luppino G, Zilles K (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol 202:443–474CrossRefPubMedGoogle Scholar
  11. Ghosh S, Porter R (1988) Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J Physiol 400:617–629CrossRefPubMedPubMedCentralGoogle Scholar
  12. Godschalk M, Mitz AR, van Duin B, van der Burg H (1995) Somatotopy of monkey premotor cortex examined with microstimulation. Neurosci Res 23:269–279CrossRefPubMedGoogle Scholar
  13. Grafton ST, Woods RP, Mazziotta JC, Phelps ME (1991) Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. J Neurophysiol 66:735–743PubMedGoogle Scholar
  14. Graziano MS, Taylor CS, Moore T (2002a) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851CrossRefPubMedGoogle Scholar
  15. Graziano MS, Taylor CS, Moore T, Cooke DF (2002b) The cortical control of movement revisited. Neuron 36:349–362CrossRefPubMedGoogle Scholar
  16. He SQ, Dum RP, Strick PL (1993) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13:952–980PubMedGoogle Scholar
  17. He SQ, Dum RP, Strick PL (1995) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15:3284–3306PubMedGoogle Scholar
  18. Inuggi A, Filippi M, Chieffo R et al (2010) Motor area localization using fMRI-constrained cortical current density reconstruction of movement-related cortical potentials, a comparison with fMRI and TMS mapping. Brain Res 1308:68–78CrossRefPubMedGoogle Scholar
  19. Julkunen P, Ruohonen J, Sääskilahti S et al (2011) Threshold curves for transcranial magnetic stimulation to improve reliability of motor pathway status assessment. Clin Neurophysiol 122:975–983CrossRefPubMedGoogle Scholar
  20. Kahn T, Schwabe B, Bettag M et al (1996) Mapping of the cortical motor hand area with functional MR imaging and MR imaging-guided laser-induced interstitial thermotherapy of brain tumors. Radiology 200:149–157CrossRefPubMedGoogle Scholar
  21. Kantelhardt SR, Fadini T, Finke M et al (2010) Robot-assisted image-guided transcranial magnetic stimulation for somatotopic mapping of the motor cortex: a clinical pilot study. Acta Neurochir 152:333–343CrossRefPubMedGoogle Scholar
  22. Kraus D, Gharabaghi A (2015) Projecting navigated TMS sites on the gyral anatomy decreases inter-subject variability of cortical motor maps. Brain Stimul. doi: 10.1016/j.brs.2015.03.006 PubMedGoogle Scholar
  23. Lefaucheur JP (2010) Why image-guided navigation becomes essential in the practice of transcranial magnetic stimulation. Neurophysiol Clin 40:1–5CrossRefPubMedGoogle Scholar
  24. Lefaucheur JP, André-Obadia N, Antal A et al (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125:2150–2206CrossRefPubMedGoogle Scholar
  25. Lotze M, Kaethner RJ, Erb M et al (2003) Comparison of representational maps using functional magnetic resonance imaging and transcranial magnetic stimulation. Clin Neurophysiol 114:306–312CrossRefPubMedGoogle Scholar
  26. Maier MA, Armand J, Kirkwood PA et al (2002) Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. Cereb Cortex 12:281–296CrossRefPubMedGoogle Scholar
  27. Meincke J, Hewitt M, Batsikadze G, Liebetanz D (2016) Automated TMS hotspot-hunting using a closed loop threshold-based algorithm. Neuroimage 124:509–517CrossRefPubMedGoogle Scholar
  28. Mylius V, Ayache SS, Ahdab R et al (2013) Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: inter-rater reliability, accuracy, and influence of gender and age. Neuroimage 78:224–232CrossRefPubMedGoogle Scholar
  29. Nii Y, Uematsu S, Lesser RP, Gordon B (1996) Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes. Neurology 46:360–367CrossRefPubMedGoogle Scholar
  30. Niskanen E, Julkunen P, Säisänen L, Vanninen R, Karjalainen P, Könönen M (2010) Group-level variations in motor representation areas of thenar and anterior tibial muscles: navigated Transcranial Magnetic Stimulation Study. Hum Brain Mapp 31:1272–1280PubMedGoogle Scholar
  31. Nummenmaa A, Stenroos M, Ilmoniemi RJ et al (2013) Comparison of spherical and realistically shaped boundary element head models for transcranial magnetic stimulation navigation. Clin Neurophysiol 124:1995–2007CrossRefPubMedPubMedCentralGoogle Scholar
  32. Opitz A, Legon W, Rowlands A et al (2013) Physiological observations validate finite element models for estimating subject-specific electric field distributions induced by transcranial magnetic stimulation of the human motor cortex. Neuroimage 81:253–264CrossRefPubMedGoogle Scholar
  33. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443CrossRefGoogle Scholar
  34. Picht T, Mularski S, Kuehn B et al (2009) Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 65:93–99CrossRefPubMedGoogle Scholar
  35. Picht T, Schmidt S, Brandt S et al (2011) Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 69:581–588CrossRefPubMedGoogle Scholar
  36. Puce A, Constable RT, Luby ML et al (1995) Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. J Neurosurg 83:262–270CrossRefPubMedGoogle Scholar
  37. Rademacher J, Burgel U, Geyer S et al (2001) Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. Brain 124:2232–2258CrossRefPubMedGoogle Scholar
  38. Rossini PM, Burke D, Chen R et al (2015) 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 126:1071–1107CrossRefPubMedGoogle Scholar
  39. Rumeau C, Tzourio N, Murayama N et al (1994) Location of hand function in the sensorimotor cortex: MR and functional correlation. AJNR Am J Neuroradiol 15:567–572PubMedGoogle Scholar
  40. Ruohonen J, Karhu J (2010) Navigated transcranial magnetic stimulation. Neurophysiol Clin 40:7–17CrossRefPubMedGoogle Scholar
  41. Schmidt S, Bathe-Peters R, Fleischmann R, Rönnefarth M, Scholz M, Brandt SA (2015) Nonphysiological factors in navigated TMS studies; confounding covariates and valid intracortical estimates. Hum Brain Mapp 36:40–49CrossRefPubMedGoogle Scholar
  42. Shimazu H, Maier MA, Cerri G et al (2004) Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J Neurosci 24:1200–1211CrossRefPubMedGoogle Scholar
  43. Sparing R, Buelte D, Meister IG et al (2008) Transcranial magnetic stimulation and the challenge of coil placement: a comparison of conventional and stereotaxic neuronavigational strategies. Hum Brain Mapp 29:82–96CrossRefPubMedGoogle Scholar
  44. Tarapore PE, Tate MC, Findlay AM et al (2012) Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 117:354–362CrossRefPubMedPubMedCentralGoogle Scholar
  45. Teitti S, Määttä S, Säisänen L et al (2008) Non-primary motor areas in the human frontal lobe are connected directly to hand muscles. Neuroimage 40:1243–1250CrossRefPubMedGoogle Scholar
  46. Terao Y, Ugawa Y, Sakai K et al (1998) Localizing the site of magnetic brain stimulation by functional MRI. Exp Brain Res 121:145–152CrossRefPubMedGoogle Scholar
  47. Thielscher A, Kammer T (2004) Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency. Clin Neurophysiol 115:1697–1708CrossRefPubMedGoogle Scholar
  48. Tokuno H, Nambu A (2000) Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb Cortex 10:58–68CrossRefPubMedGoogle Scholar
  49. Uematsu S, Lesser R, Fisher RS et al (1992) Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. Neurosurgery 31:59–71CrossRefPubMedGoogle Scholar
  50. Wassermann EM, Wang B, Zeffiro TA et al (1996) Locating the motor cortex on the MRI with transcranial magnetic stimulation and PET. Neuroimage 3:1–9CrossRefPubMedGoogle Scholar
  51. Yousry TA, Schmid UD, Jassoy AG et al (1995) Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. Radiology 195:23–29CrossRefPubMedGoogle Scholar
  52. Yousry TA, Schmid UD, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus: a new landmark. Brain 120:141–157CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Rechdi Ahdab
    • 1
    • 2
    • 3
  • Samar S. Ayache
    • 1
    • 2
    • 3
  • Pierre Brugières
    • 4
  • Wassim H. Farhat
    • 1
    • 2
  • Jean-Pascal Lefaucheur
    • 1
    • 2
  1. 1.EA 4391, Excitabilité Nerveuse et ThérapeutiqueUniversité Paris-Est-CréteilCréteilFrance
  2. 2.Service de Physiologie – Explorations FonctionnellesHôpital Henri Mondor, Assistance Publique – Hôpitaux de ParisCréteilFrance
  3. 3.Neurology DivisionUniversity Medical Center Rizk HospitalBeirutLebanon
  4. 4.Service de NeuroradiologieHôpital Henri Mondor, Assistance Publique – Hôpitaux de ParisCréteilFrance

Personalised recommendations