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Brain Topography

, Volume 30, Issue 6, pp 711–722 | Cite as

Minimum-Norm Estimation of Motor Representations in Navigated TMS Mappings

  • Minna Pitkänen
  • Elisa Kallioniemi
  • Petro Julkunen
  • Maria Nazarova
  • Jaakko O. Nieminen
  • Risto J. Ilmoniemi
Original Paper

Abstract

Navigated transcranial magnetic stimulation (nTMS) can be applied to locate and outline cortical motor representations. This may be important, e.g., when planning neurosurgery or focused nTMS therapy, or when assessing plastic changes during neurorehabilitation. Conventionally, a cortical location is considered to belong to the motor cortex if the maximum electric field (E-field) targeted there evokes a motor-evoked potential in a muscle. However, the cortex is affected by a broad E-field distribution, which tends to broaden estimates of representation areas by stimulating also the neighboring areas in addition to the maximum E-field location. Our aim was to improve the estimation of nTMS-based motor maps by taking into account the E-field distribution of the stimulation pulse. The effect of the E-field distribution was considered by calculating the minimum-norm estimate (MNE) of the motor representation area. We tested the method on simulated data and then applied it to recordings from six healthy volunteers and one stroke patient. We compared the motor representation areas obtained with the MNE method and a previously introduced interpolation method. The MNE hotspots and centers of gravity were close to those obtained with the interpolation method. The areas of the maps, however, depend on the thresholds used for outlining the areas. The MNE method may improve the definition of cortical motor areas, but its accuracy should be validated by comparing the results with maps obtained with direct cortical stimulation of the cortex where the E-field distribution can be better focused.

Keywords

Navigated transcranial magnetic stimulation Minimum-norm estimate Motor cortex Motor-evoked potential Motor representation Electric field 

Notes

Acknowledgements

The study was funded by the State Research Funding (Research Committee of the Kuopio University Hospital Catchment Area, projects 5041730 and 5041747, Kuopio, Finland); Finnish Cultural Foundation, Helsinki, Finland; Cancer Society of Finland, Helsinki, Finland; Päivikki and Sakari Sohlberg Foundation, Helsinki, Finland; Academy of Finland (Decisions Nos. 255347, 265680, and 294625), Helsinki, Finland; Russian Academic Excellence Project ‘5-100’, RFBR Grant (No. 16-04-01883) and Skolkovo personal grant “Umnik”. The funding sources had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the report, or in the decision to submit the article for publication.

Compliance with Ethical Standards

Conflict of interest

Petro Julkunen and Jaakko O. Nieminen have received unrelated consulting fees from Nexstim Plc, Elisa Kallioniemi has received unrelated travel support from Nexstim Plc, and Risto J. Ilmoniemi is an advisor and a minority shareholder of the company. The other authors declare 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 and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

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

References

  1. Awiszus F (2003) TMS and threshold hunting. Suppl to Clin Neurophysioly 56:13–23CrossRefGoogle Scholar
  2. Awiszus F, Borckardt JJ (2012) TMS Motor Threshold Assessment Tool 2.0 http://clinicalresearcher.org/software.htm. Accessed 2 June 2014
  3. Bohning DE, He L, George MS, Epstein CM (2001) Deconvolution of transcranial magnetic stimulation (TMS) maps. J Neural Transm 108:35–52CrossRefPubMedGoogle Scholar
  4. 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 77:143–148CrossRefPubMedGoogle Scholar
  5. Bungert A, Antunes A, Espenhahn S, Thielscher A (2016) Where does TMS stimulate the motor cortex? Combining electrophysiological measurements and realistic field estimates to reveal the affected cortex position. Cereb Cortex 1–12Google Scholar
  6. 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
  7. Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338CrossRefPubMedGoogle Scholar
  8. Fox PT, Narayana S, Tandon N, Sandoval H, Fox SP, Kochunov P, Lancaster JL (2004) Column-based model of electric field excitation of cerebral cortex. Hum Brain Mapp 22:1–14CrossRefPubMedGoogle Scholar
  9. Goetz SM, Luber B, Lisanby SH, Peterchev AV (2014) A novel model incorporating two variability sources for describing motor evoked potentials. Brain Stimul 7:541–552CrossRefPubMedPubMedCentralGoogle Scholar
  10. Hämäläinen MS, Ilmoniemi RJ (1994) Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Comput 32:35–42CrossRefPubMedGoogle Scholar
  11. Heald A, Bates D, Cartlidge NEF, French JM, Miller S (1993) Longitudinal study of central motor conduction time following stroke: 2. Central motor conduction measured within 72 h after stroke as a predictor of functional outcome at 12 months. Brain 116:1371–1385CrossRefPubMedGoogle Scholar
  12. Ilmoniemi RJ (2009) The triangle phantom in magnetoencephalography. J Jpn Biomagn Bioelectromagn Soc 22:44–45Google Scholar
  13. Ilmoniemi RJ, Ruohonen J, Karhu J (1999) Transcranial magnetic stimulation—a new tool for functional imaging of the brain. Crit Rev Biomed Eng 27:241–284PubMedGoogle Scholar
  14. Jang SH, Ahn SH, Sakong J, Byun WM, Choi BY, Chang CH, Bai D, Son SM (2010) Comparison of TMS and DTT for predicting motor outcome in intracerebral hemorrhage. J Neurol Sci 290:107–111CrossRefPubMedGoogle Scholar
  15. Julkunen P (2014) Methods for estimating cortical motor representation size and location in navigated transcranial magnetic stimulation. J Neurosci Methods 232:125–133CrossRefPubMedGoogle Scholar
  16. Julkunen P, Säisänen L, Danner N, Awiszus F, Könönen M (2012) Within-subject effect of coil-to-cortex distance on cortical electric field threshold and motor evoked potentials in transcranial magnetic stimulation. J Neurosci Methods 206:158–164CrossRefPubMedGoogle Scholar
  17. Jussen D, Zdunczyk A, Schmidt S, Rösler J, Buchert R, Julkunen P, Karhu J, Brandt S, Picht T, Vajkoczy P (2016) Motor plasticity after extra-intracranial bypass surgery in occlusive cerebrovascular disease. Neurology 87:27–35CrossRefPubMedGoogle Scholar
  18. Kallioniemi E, Julkunen P (2016) Alternative stimulation intensities for mapping cortical motor area with navigated TMS. Brain Topogr 29:395–404CrossRefPubMedGoogle Scholar
  19. Kallioniemi E, Pitkänen M, Säisänen L, Julkunen P (2015) Onset latency of motor evoked potentials in motor cortical mapping with neuronavigated transcranial magnetic stimulation. Open Neurol J 9:62–69CrossRefPubMedPubMedCentralGoogle Scholar
  20. Liepert J, Bauder H, Miltner WHR, Taub E, Weiller C (2000) Treatment-induced cortical reorganization after stroke in humans. Stroke 31:1210–1216CrossRefPubMedGoogle Scholar
  21. Malcolm MP, Triggs WJ, Light KE, Shechtman O, Khandekar G, Gonzalez Rothi LJ (2006) Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol 117:1037–1046CrossRefPubMedGoogle Scholar
  22. Matthäus L, Trillenberg P, Fadini T, Finke M, Schweikard A (2008) Brain mapping with transcranial magnetic stimulation using a refined correlation ratio and Kendall’s τ. Stat Med 27:5252–5270CrossRefPubMedGoogle Scholar
  23. Nieminen JO, Koponen LM, Ilmoniemi RJ (2015) Experimental characterization of the electric field distribution induced by TMS devices. Brain Stimul 8:582–589CrossRefPubMedGoogle Scholar
  24. Nummenmaa A, Stenroos M, Ilmoniemi RJ, Okada YC, Hämäläinen MS, Raij T (2013) Comparison of spherical and realistically shaped boundary element head models for transcranial magnetic stimulation navigation. Clin Neurophysiol 124:1995–2007CrossRefPubMedPubMedCentralGoogle Scholar
  25. Numminen J, Ahlfors S, Ilmoniemi R, Montonen J, Nenonen J (1995) Transformation of multichannel magnetocardiographic signals to standard grid form. IEEE Trans Biomed Eng 42:72–78CrossRefPubMedGoogle Scholar
  26. Opitz A, Legon W, Rowlands A, Bickel WK, Paulus W, Tyler WJ (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
  27. Opitz A, Zafar N, Bockermann V, Rohde V, Paulus W (2014) Validating computationally predicted TMS stimulation areas using direct electrical stimulation in patients with brain tumors near precentral regions. NeuroImage 4:500–507CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 8:197–201CrossRefPubMedPubMedCentralGoogle Scholar
  29. Parker RL (1977) Understanding inverse theory. Annu Rev Earth Planet Sci 5:35–64CrossRefGoogle Scholar
  30. 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. Neurosurgery 69:581–589CrossRefPubMedGoogle Scholar
  31. Picht T, Krieg SM, Sollmann N, Rösler J, Niraula B, Neuvonen T, Savolainen P, Lioumis P, Mäkelä JP, Deletis V, Meyer B, Vajkoczy P, Ringel F (2013) A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 72:808–819CrossRefPubMedGoogle Scholar
  32. Pitkänen M, Kallioniemi E, Julkunen P (2015) Extent and location of the excitatory and inhibitory cortical hand representation maps: a navigated transcranial magnetic stimulation study. Brain Topogr 28:657–665CrossRefPubMedGoogle Scholar
  33. Raffin E, Pellegrino G, Di Lazzaro V, Thielscher A, Siebner HR (2015) Bringing transcranial mapping into shape: sulcus-aligned mapping captures motor somatotopy in human primary motor hand area. NeuroImage 120:164–175CrossRefPubMedGoogle Scholar
  34. 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 126:1071–1107CrossRefPubMedGoogle Scholar
  35. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. Electroencephalogr Clin Neurophysiol Suppl 52:97–103PubMedGoogle Scholar
  36. Säisänen L, Julkunen P, Niskanen E, Danner N, Hukkanen T, Lohioja T, Nurkkala J, Mervaala E, Karhu J, Könönen M (2008) Motor potentials evoked by navigated transcranial magnetic stimulation in healthy subjects. J Clin Neurophysiol 25:367–372CrossRefPubMedGoogle Scholar
  37. Sarvas J (1987) Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. Phys Med Biol 32:11–22CrossRefPubMedGoogle Scholar
  38. Thickbroom GW, Sammut R, Mastaglia FL (1998) Magnetic stimulation mapping of motor cortex: factors contributing to map area. Electroencephalogr Clin Neurophysiol 109:79–84CrossRefPubMedGoogle Scholar
  39. Thielscher A, Kammer T (2002) Linking physics with physiology in TMS: a sphere field model to determine the cortical stimulation site in TMS. NeuroImage 17:1117–1130CrossRefPubMedGoogle Scholar
  40. Thielscher A, Wichmann FA (2009) Determining the cortical target of transcranial magnetic stimulation. NeuroImage 47:1319–1330CrossRefPubMedGoogle Scholar
  41. Traversa R, Cicinelli P, Bassi A, Rossini PM, Bernardi G (1997) Mapping of motor cortical reorganization after stroke: a brain simulation study with focal magnetic pulses. Stroke 28:110–117CrossRefPubMedGoogle Scholar
  42. 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 155:507–518CrossRefPubMedGoogle Scholar
  43. Wassermann EM, McShane LM, Hallett M, Cohen LG (1992) Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol 85:1–8CrossRefPubMedGoogle Scholar
  44. 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 89:424–433CrossRefPubMedGoogle Scholar
  45. Wilson SA, Thickbroom GW, Mastaglia FL (1993) Topography of excitatory and inhibitory muscle responses evoked by transcranial magnetic stimulation in the human motor cortex. Neurosci Lett 154:52–56CrossRefPubMedGoogle Scholar
  46. 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 115:1740–1747CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of Neuroscience and Biomedical EngineeringAalto University School of ScienceAalto, EspooFinland
  2. 2.Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
  3. 3.Department of Clinical RadiologyKuopio University HospitalKuopioFinland
  4. 4.Department of Applied PhysicsUniversity of Eastern FinlandKuopioFinland
  5. 5.Centre for Cognition and Decision MakingNational Research University Higher School of EconomicsMoscowRussian Federation

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