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Extent and Location of the Excitatory and Inhibitory Cortical Hand Representation Maps: A Navigated Transcranial Magnetic Stimulation Study

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An Author Correction to this article was published on 14 October 2017

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Abstract

Voluntary muscle action and control are modulated by the primary motor cortex, which is characterized by a well-defined somatotopy. Muscle action and control depend on a sensitive balance between excitatory and inhibitory mechanisms in the cortex and in the corticospinal tract. The cortical locations evoking excitatory and inhibitory responses in brain stimulation can be mapped, for example, as a pre-surgical procedure. The purpose of this study was to find the differences between excitatory and inhibitory motor representations mapped using navigated transcranial magnetic stimulation (nTMS). The representations of small hand muscles were mapped to determine the areas and the center of gravities (CoGs) in both hemispheres of healthy right-handed volunteers. The excitatory representations were obtained via resting motor evoked potential (MEP) mapping, with and without a stimulation grid. The inhibitory representations were mapped using the grid and measuring corticospinal silent periods (SPs) during voluntary muscle contraction. The excitatory representations were larger on the dominant hemisphere compared with the non-dominant (p < 0.05). The excitatory CoGs were more medial (p < 0.001) and anterior (p < 0.001) than the inhibitory CoGs. The use of the grid did not influence the areas or the CoGs. The results support the common hypothesis that the MEP and SP representations are located at adjacent sites. Furthermore, the dominant hemisphere seems to be better organized for controlling excitatory motor functions with respect to TMS. In addition, the inhibitory representations could provide further information about motor reorganization and aid in surgery planning when the functional cortical representations are located in abnormal cortical regions.

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Change history

  • 14 October 2017

    The original version of this article unfortunately contained an error. An error in the transformation between coordinate systems used to derive part of the results has been noticed.

References

  • Amunts K, Jäncke L, Mohlberg H, Steinmetz H, Zilles K (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychol 38:304–312

    Article  CAS  Google Scholar 

  • Awiszus F (2003) Chapter 2 TMS and threshold hunting. Suppl Clin Neurophysiol 56:13–23

    Article  PubMed  Google Scholar 

  • Awiszus F, Borckardt JJ (2012) TMS motor threshold assessment tool 2.0. http://clinicalresearcher.org/software.htm. Accessed 2 June 2014

  • Borghetti D, Sartucci F, Petacchi E, Guzzetta A, Piras MF, Murri L, Cioni G (2008) Transcranial magnetic stimulation mapping: a model based on spline interpolation. Brain Res Bull 77:143–148

    Article  CAS  PubMed  Google Scholar 

  • Büchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14:945–951

    Article  PubMed  Google Scholar 

  • Byrnes ML, Thickbroom GW, Wilson SA, Sacco P, Shipman JM, Stell R, Mastaglia FL (1998) The corticomotor representation of upper limb muscles in writer’s cramp and changes following botulinum toxin injection. Brain 121:977–988

    Article  PubMed  Google Scholar 

  • Byrnes ML, Thickbroom GW, Phillips BA, Wilson SA, Mastaglia FL (1999) Physiological studies of the corticomotor projection to the hand after subcortical stroke. Clin Neurophysiol 110:487–498

    Article  CAS  PubMed  Google Scholar 

  • Cantello R, Gianelli M, Civardi C, Mutani R (1992) Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 42:1951–1959

    Article  CAS  PubMed  Google Scholar 

  • Cicinelli P, Traversa R, Bassi A, Scivoletto G, Rossini PM (1997) Interhemispheric differences of hand muscle representation in human motor cortex. Muscle Nerv 20:535–542

    Article  CAS  Google Scholar 

  • Classen J, Knorr U, Werhahn KJ, Schlaug G, Kunesch E, Cohen LG, Seitz RJ, Benecke R (1998) Multimodal output mapping of human central motor representation on different spatial scales. J Physiol 512:163–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dassonville P, Zhu X-H, Uǧurbil K, Kim S-G, Ashe J (1997) Functional activation in motor cortex reflects the direction and the degree of handedness. Proc Natl Acad Sci USA 94:14015–14018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109:397–401

    Article  PubMed  Google Scholar 

  • Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E (1995) Increased cortical representation of the fingers of the left hand in string players. Science 270:305–307

    Article  CAS  PubMed  Google Scholar 

  • Fandino J, Kollias SS, Wieser HG, Valavanis A, Yonekawa Y (1999) Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 91:238–250

    Article  CAS  PubMed  Google Scholar 

  • Freund P, Rothwell J, Craggs M, Thompson AJ, Bestmann S (2011) Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury. Eur J Neurosci 34:1839–1846

    Article  PubMed  Google Scholar 

  • Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262

    Article  CAS  PubMed  Google Scholar 

  • Guye M, Parker GJM, Symms M, Boulby P, Wheeler-Kingshott CAM, Salek-Haddadi A, Barker GJ, Duncan JS (2003) Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 19:1349–1360

    Article  PubMed  Google Scholar 

  • Hervé P-Y, Crivello F, Perchey G, Mazoyer B, Tzourio-Mazoyer N (2006) Handedness and cerebral anatomical asymmetries in young adult males. Neuroimage 29:1066–1079

    Article  PubMed  Google Scholar 

  • Herwig U, Kölbel K, Wunderlich AP, Thielscher A, von Tiesenhausen C, Spitzer M, Schönfeldt-Lecuona C (2002) Spatial congruence of neuronavigated transcranial magnetic stimulation and functional neuroimaging. Clin Neurophysiol 113:462–468

    Article  PubMed  Google Scholar 

  • Ho KH, Nithi K, Mills KR (1998) Covariation between human intrinsic hand muscles of the silent periods and compound muscle action potentials evoked by magnetic brain stimulation: evidence for common inhibitory connections. Exp Brain Res 122:433–440

    Article  CAS  PubMed  Google Scholar 

  • Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534

    CAS  PubMed  PubMed Central  Google Scholar 

  • Julkunen P (2014) Methods for estimating cortical motor representation size and location in navigated transcranial magnetic stimulation. J Neurosci Methods 232:125–133

    Article  PubMed  Google Scholar 

  • Julkunen P, Säisänen L, Danner N, Niskanen E, Hukkanen T, Mervaala E, Könönen M (2009) Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 44:790–795

    Article  PubMed  Google Scholar 

  • Kagerer FA, Summers JJ, Byblow WD, Taylor B (2003) Altered corticomotor representation in patients with Parkinson’s disease. Mov Disord 18:919–927

    Article  PubMed  Google Scholar 

  • Kallioniemi E, Säisänen L, Könönen M, Awiszus F, Julkunen P (2014) On the estimation of silent period thresholds in transcranial magnetic stimulation. Clin Neurophysiol 125:2247–2252

    Article  PubMed  Google Scholar 

  • Krings T, Buchbinder BR, Butler WE, Chiappa KH, Jiang HJ, Cosgrove GR, Rosen BR (1997) Functional magnetic resonance imaging and transcranial magnetic stimulation: complementary approaches in the evaluation of cortical motor function. Neurology 48:1406–1416

    Article  CAS  PubMed  Google Scholar 

  • Lewko JP, Stokić DS, Tarkka IM (1996) Dissociation of cortical areas responsible for evoking excitatory and inhibitory responses in the small hand muscles. Brain Topogr 8:397–405

    Article  CAS  PubMed  Google Scholar 

  • Mäkelä JP, Vitikainen A-M, Lioumis P, Paetau R, Ahtola E, Kuusela L, Valanne L, Blomstedt G, Gaily E (2013) Functional plasticity of the motor cortical structures demonstrated by navigated TMS in two patients with epilepsy. Brain Stimul 6:286–291

    Article  PubMed  Google Scholar 

  • Menon P, Kiernan MC, Vucic S (2014) Cortical excitability differences in hand muscles follow a split-hand pattern in healthy controls. Muscle Nerv 49:836–844

    Article  Google Scholar 

  • Ngomo S, Leonard G, Moffet H, Mercier C (2012) Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J Neurosci Methods 205:65–71

    Article  PubMed  Google Scholar 

  • Paiva WS, Fonoff ET, Marcolin MA, Cabrera HN, Teixeira MJ (2012) Cortical mapping with navigated transcranial magnetic stimulation in low-grade glioma surgery. Neuropsychiatr Dis Treat 8:197–201

    Article  PubMed  PubMed Central  Google Scholar 

  • Pascual-Leone A, Dang N, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045

    CAS  PubMed  Google Scholar 

  • Pentland A (1980) Maximum likelihood estimation: the best PEST. Percept Psychophys 28:377–379

    Article  CAS  PubMed  Google Scholar 

  • Picht T, Schmidt S, Brandt S, Frey D, Hannula H, Neuvonen T, Karhu J, Vajkoczy P, Suess O (2011) Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurg 69:581–588

    Article  Google Scholar 

  • Portney LG, Watkins MP (2000) Foundations of clinical research: applications to practice. Prentice Hall Inc, New Jersey

    Google Scholar 

  • Rose S, Rowland T, Pannek K, Baumann F, Coulthard A, McCombe P, Henderson R (2012) Structural hemispheric asymmetries in the human precentral gyrus hand representation. Neuroscience 210:211–221

    Article  CAS  PubMed  Google Scholar 

  • Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, Di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S 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 126:1071–1107

    Article  CAS  PubMed  Google Scholar 

  • Ruohonen J, Karhu J (2010) Navigated transcranial magnetic stimulation. Clin Neurophysiol 40:7–17

    Article  CAS  Google Scholar 

  • Säisänen L, Könönen M, Julkunen P, Määttä S, Vanninen R, Immonen A, Jutila L, Kälviäinen R, Jääskeläinen JE, Mervaala E (2010) Non-invasive preoperative localization of primary motor cortex in epilepsy surgery by navigated transcranial magnetic stimulation. Epilepsy Res 92:134–144

    Article  PubMed  Google Scholar 

  • Schabrun SM, Stinear CM, Byblow WD, Ridding MC (2009) Normalizing motor cortex representations in focal hand dystonia. Cereb Cortex 19:1968–1977

    Article  PubMed  Google Scholar 

  • Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16

    Article  PubMed  Google Scholar 

  • Siebner HR, Dressnandt J, Auer C, Conrad B (1998) Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerv 21:1209–1212

    Article  CAS  Google Scholar 

  • Thickbroom GW, Byrnes ML, Mastaglia FL (1999) A model of the effect of MEP amplitude variation on the accuracy of TMS mapping. Clin Neurophysiol 110:941–943

    Article  CAS  PubMed  Google Scholar 

  • Triggs WJ, Subramanium B, Rossi F (1999) Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation. Brain Res 835:324–329

    Article  CAS  PubMed  Google Scholar 

  • Uy J, Ridding MC, Miles TS (2002) Stability of maps of human motor cortex made with transcranial magnetic stimulation. Brain Topogr 14:293–297

    Article  PubMed  Google Scholar 

  • Vaalto S, Julkunen P, Säisänen L, Könönen M, Määttä S, Karhu J (2013) Long-term plasticity may be manifested as reduction or expansion of cortical representations of actively used muscles in motor skill specialists. NeuroReport 24:596–600

    Article  PubMed  Google Scholar 

  • Vitikainen A-M, Salli E, Lioumis P, Mäkelä JP, Metsähonkala L (2013) Applicability of nTMS in locating the motor cortical representation areas in patients with epilepsy. Acta Neurochir 155:507–518

    Article  PubMed  Google Scholar 

  • Volkmann J, Schnitzler A, Witte OW, Freund H-J (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79:2149–2154

    CAS  PubMed  Google Scholar 

  • Wassermann EM, McShane LM, Hallett M, Cohen LG (1992) Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol 85:1–8

    Article  CAS  PubMed  Google Scholar 

  • Wassermann EM, Pascual-Leone A, Valls-Solé J, Toro C, Cohen LG, Hallett M (1993) Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. Electroencephalogr Clin Neurophysiol 89:424–433

    Article  CAS  PubMed  Google Scholar 

  • Weiss C, Nettekoven C, Rehme AK, Neuschmelting V, Eisenbeis A, Goldbrunner R, Grefkes C (2013) Mapping the hand, foot and face representations in the primary motor cortex—retest reliability of neuronavigated TMS versus functional MRI. Neuroimage 66:531–542

    Article  PubMed  Google Scholar 

  • Wilson SA, Thickbroom GW, Mastaglia FL (1993a) Topography of excitatory and inhibitory muscle responses evoked by transcranial magnetic stimulation in the human motor cortex. Neurosci Lett 154:52–56

    Article  CAS  PubMed  Google Scholar 

  • Wilson SA, Thickbroom GW, Mastaglia FL (1993b) Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. The representation of two intrinsic hand muscles. J Neurol Sci 118:134–144

    Article  CAS  PubMed  Google Scholar 

  • Wilson SA, Thickbroom GW, Mastaglia FL (1995) Comparison of the magnetically mapped corticomotor representation of a muscle at rest and during low-level voluntary contraction. Electroencephalogr Clin Neurophysiol 97:246–250

    CAS  PubMed  Google Scholar 

  • Wolf SL, Butler AJ, Campana GI, Parris TA, Struys DM, Weinstein SR, Weiss P (2004) Intra-subject reliability of parameters contributing to maps generated by transcranial magnetic stimulation in able-bodied adults. Clin Neurophysiol 115:1740–1747

    Article  PubMed  Google Scholar 

  • Zdunczyk A, Fleischmann R, Schulz J, Vajkoczy P, Picht T (2013) The reliability of topographic measurements from navigated transcranial magnetic stimulation in healthy volunteers and tumor patients. Acta Neurochir 155:1309–1317

    Article  PubMed  Google Scholar 

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Acknowledgments

The study was funded by the State Research Funding (Project 5041730, Kuopio, Finland). In addition, Minna Pitkänen was supported by the Research Foundation of Helsinki University of Technology, Espoo, Finland, and Elisa Kallioniemi was supported by the Kaute Foundation, Helsinki, Finland, The Finnish Brain Research and Rehabilitation Center Neuron, Kuopio, Finland, The Finnish Concordia Fund, Helsinki, Finland, The Paulo Foundation, Helsinki, Finland. The funding sources had no involvement in the study design, in the collection, analysis and interpretation of data; in the writing of the report, and in the decision to submit the article for publication.

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Authors and Affiliations

  1. Department of Clinical Neurophysiology, Kuopio University Hospital, POB 100, 70029, KYS, Finland

    Minna Pitkänen, Elisa Kallioniemi & Petro Julkunen

  2. Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, POB 12200, 00076, Aalto, Finland

    Minna Pitkänen

  3. Department of Applied Physics, University of Eastern Finland, POB 1627, 70211, Kuopio, Finland

    Elisa Kallioniemi & Petro Julkunen

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  1. Minna Pitkänen
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  2. Elisa Kallioniemi
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Correspondence to Minna Pitkänen.

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Conflicts of interest

Petro Julkunen has received unrelated consulting pay from Nexstim Plc, manufacturer of the nTMS devices. The rest of the authors declared that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (ethical permission 1/2014) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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A correction to this article is available online at https://doi.org/10.1007/s10548-017-0600-0.

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Pitkänen, M., Kallioniemi, E. & Julkunen, P. Extent and Location of the Excitatory and Inhibitory Cortical Hand Representation Maps: A Navigated Transcranial Magnetic Stimulation Study. Brain Topogr 28, 657–665 (2015). https://doi.org/10.1007/s10548-015-0442-6

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