A scalp-measurement based parameter space: Towards locating TMS coils in a clinically-friendly way

Abstract

The efficacy of TMS as a therapeutic intervention heavily depends on the TMS coil location [1Herbsman T. Avery D. Ramsey D. Holtzheimer P. Wadjik C. Hardaway F. et al.More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response.Biol Psychiatr. 2009; 66: 509-515https://doi.org/10.1016/j.biopsych.2009.04.034Abstract Full Text Full Text PDF PubMed Scopus (126) Google Scholar, 2Fox M.D. Buckner R.L. White M.P. Greicius M.D. Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate.Biol Psychiatr. 2012; 72: 595-603https://doi.org/10.1016/j.biopsych.2012.04.028Abstract Full Text Full Text PDF PubMed Scopus (557) Google Scholar, 3Cash R.F.H. Weigand A. Zalesky A. Siddiqi S.H. Downar J. Fitzgerald P.B. et al.Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression.Biol Psychiatr. 2020; https://doi.org/10.1016/j.biopsych.2020.05.033Abstract Full Text Full Text PDF Scopus (41) Google Scholar] [1Herbsman T. Avery D. Ramsey D. Holtzheimer P. Wadjik C. Hardaway F. et al.More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response.Biol Psychiatr. 2009; 66: 509-515https://doi.org/10.1016/j.biopsych.2009.04.034Abstract Full Text Full Text PDF PubMed Scopus (126) Google Scholar, 2Fox M.D. Buckner R.L. White M.P. Greicius M.D. Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate.Biol Psychiatr. 2012; 72: 595-603https://doi.org/10.1016/j.biopsych.2012.04.028Abstract Full Text Full Text PDF PubMed Scopus (557) Google Scholar, 3Cash R.F.H. Weigand A. Zalesky A. Siddiqi S.H. Downar J. Fitzgerald P.B. et al.Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression.Biol Psychiatr. 2020; https://doi.org/10.1016/j.biopsych.2020.05.033Abstract Full Text Full Text PDF Scopus (41) Google Scholar] [1Herbsman T. Avery D. Ramsey D. Holtzheimer P. Wadjik C. Hardaway F. et al.More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response.Biol Psychiatr. 2009; 66: 509-515https://doi.org/10.1016/j.biopsych.2009.04.034Abstract Full Text Full Text PDF PubMed Scopus (126) Google Scholar, 2Fox M.D. Buckner R.L. White M.P. Greicius M.D. Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate.Biol Psychiatr. 2012; 72: 595-603https://doi.org/10.1016/j.biopsych.2012.04.028Abstract Full Text Full Text PDF PubMed Scopus (557) Google Scholar, 3Cash R.F.H. Weigand A. Zalesky A. Siddiqi S.H. Downar J. Fitzgerald P.B. et al.Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression.Biol Psychiatr. 2020; https://doi.org/10.1016/j.biopsych.2020.05.033Abstract Full Text Full Text PDF Scopus (41) Google Scholar]. For clinical routine practice, various scalp measurement-based methods have been proposed to locate coils on patients’ scalps, using only tape measure [[4]Lefaucheur J.P. Aleman A. Baeken C. Benninger D.H. Brunelin J. di Lazzaro V. et al.Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014–2018).Clin Neurophysiol. 2020; 131: 474-528https://doi.org/10.1016/j.clinph.2019.11.002Crossref PubMed Scopus (483) Google Scholar]. For major depressive disorder as an example, the conventional “5-cm rule” defines the coil location to stimulate DLPFC as 5 cm anterior to the motor hotspot [[5]Pascual-Leone A. Rubio B. Pallardó F. Catalá M.D. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression.Lancet. 1996; 348: 233-237https://doi.org/10.1016/S0140-6736(96)01219-6Abstract Full Text Full Text PDF PubMed Scopus (989) Google Scholar]. The newer F3 method given by the International 10–20 system is also widely used [[6]Herwig U. Fallgatter A.J. Höppner J. Eschweiler G.W. Kron M. Hajak G. et al.Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial.Br J Psychiatry. 2007; 191: 441-448https://doi.org/10.1192/bjp.bp.106.034371Crossref PubMed Scopus (158) Google Scholar]. In general, the 10–20 based approaches and their extensions (e.g., 10–20 and 10-05 systems) advance the art by taking individual head size into account, but restrict the infinite number of possible coil locations to a limited number of scalp landmarks, while also lacking a clear definition for coil orientation. Moreover, the numerous measurements and calculations are time-consuming and result in low reliability, especially for operators with little experience [[7]Beam W. Borckardt J.J. Reeves S.T. George M.S. An efficient and accurate new method for locating the F3 position for prefrontal TMS applications.Brain Stimul. 2009; 2: 50-54https://doi.org/10.1016/j.brs.2008.09.006Abstract Full Text Full Text PDF PubMed Scopus (271) Google Scholar,[8]Xiao X. Zhu H. Liu W.-J. Yu X.-T. Duan L. Li Z. et al.Semi-automatic 10/20 identification method for MRI-free probe placement in transcranial brain mapping techniques.Front Neurosci. 2017; 11: 105-111Crossref PubMed Scopus (14) Google Scholar]. In this letter, we introduce a Scalp Geometry-based Parameter (SGP) space to the TMS society. Instead of a limited number of scalp landmarks, SGP can describe any conventional coil placement (coil placed tangent to the scalp, with coil center contacting the scalp to ensure minimal energy attenuation and easy operation) [[9]Valero-Cabré A. Amengual J.L. Stengel C. Pascual-Leone A. Coubard O.A. Transcranial magnetic stimulation in basic and clinical neuroscience: a comprehensive review of fundamental principles and novel insights.Neurosci Biobehav Rev. 2017; 83: 381-404https://doi.org/10.1016/j.neubiorev.2017.10.006Crossref PubMed Scopus (157) Google Scholar]. Detailed definition of SGP is shown in Fig. 1A. A 2D normalized coordinate (pNZ, pAL) originally proposed for fNIRS brain imaging [[10]Xiao X. Yu X. Zhang Z. Zhao Y. Jiang Y. Li Z. et al.Transcranial brain atlas.Sci Adv. 2018; 4eaar6904https://doi.org/10.1126/sciadv.aar6904Crossref Scopus (13) Google Scholar] is used here to describe coil location s. The first coordinate, 0<pNZ<1, indicates the coil location along the anterior-posterior direction; the smaller the value of pNZ, the more anterior. The second coordinate, 0<pAL < 1, indicates position in the left-right direction; the smaller the value of pAL, the more leftward. The coil orientation θ is defined as the angle between the coil handle direction and a predefined zero orientation vector in the tangent plane of s. Considering convenience of clinical practice, the zero-orientation vector is defined in a parasagittal and posterior-anterior direction. A competitive advantage of SGP is that any conventionally placed coil can be manually recorded with a triplet of values (pNZ, pAL, θ) and conversely, a coil can be manually placed according to a given (pNZ, pAL, θ), both in a fast and reliable way. The procedures for manual measurement are demonstrated in Fig. 1B. (Tutorial video can be found at https://www.youtube.com/watch?v=8nMs_IaWwUg.) An investigation of manual measurement performance was conducted by three technicians on five participants at two time points (at least 24 hours apart). Nine uniformly distributed scalp positions ((PNZ, PAL): (0.27,0.26), (0.53,0.25), (0.79,0.24), (0.22,0.47), (0.52,0.50), (0.78,0.53), (0.24,0.72), (0.50,0.77), (0.75,0.75)) were set as the targets. The time-cost for each target was 4.4 minutes on average, much quicker compared to time required by the 10–20 method (16 minutes as reported in Ref. [[8]Xiao X. Zhu H. Liu W.-J. Yu X.-T. Duan L. Li Z. et al.Semi-automatic 10/20 identification method for MRI-free probe placement in transcranial brain mapping techniques.Front Neurosci. 2017; 11: 105-111Crossref PubMed Scopus (14) Google Scholar]). The overall location error was 4.1 ± 2.51mm on average, as recorded by a commercial 3D digitizer (Fastrak™, Polhemus). Among them, 73% of measurements’ errors were less than 5mm. The intra- and inter-technician reliabilities were 3.53 ± 1.86 and 4.72 ± 2.2mm respectively, outperforming the 5.5cm method (11.7 ± 6.8 and 12.2 ± 6.6 mm) reported in Ref. [[11]Trapp N.T. Bruss J. King Johnson M. Uitermarkt B.D. Garrett L. Heinzerling A. et al.Reliability of targeting methods in TMS for depression: beam F3 vs. 5.5 cm.Brain Stimul. 2020; 13: 578-581https://doi.org/10.1016/j.brs.2020.01.010Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar]. Four orientations (0°, 45°, 90°, 135°) were additionally measured at three target locations, taking an extra 0.63 minutes and having 4.24 ± 2.24° angle error on average. It is important to translate advances in neuropathology findings from neuroimaging studies [[2]Fox M.D. Buckner R.L. White M.P. Greicius M.D. Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate.Biol Psychiatr. 2012; 72: 595-603https://doi.org/10.1016/j.biopsych.2012.04.028Abstract Full Text Full Text PDF PubMed Scopus (557) Google Scholar,12Weigand A. Horn A. Caballero R. Cooke D. Stern A.P. Taylor S.F. et al.Prospective validation that subgenual connectivity predicts antidepressant efficacy of transcranial magnetic stimulation sites.Biol Psychiatr. 2017; : 1-10https://doi.org/10.1016/j.biopsych.2017.10.028Abstract Full Text Full Text PDF Scopus (178) Google Scholar, 13Cash R.F.H. Cocchi L. Lv J. Fitzgerald P.B. Zalesky A. Functional magnetic resonance imaging–guided personalization of transcranial magnetic stimulation treatment for depression.JAMA Psychiatr. 2021; 78: 337https://doi.org/10.1001/JAMAPSYCHIATRY.2020.3794Crossref PubMed Scopus (0) Google Scholar, 14Siddiqi S.H. Schaper F.L.W.V.J. Horn A. Hsu J. Padmanabhan J.L. Brodtmann A. et al.Brain stimulation and brain lesions converge on common causal circuits in neuropsychiatric disease.Nat Human Behav. 2021; 5: 1707https://doi.org/10.1038/S41562-021-01161-1Crossref PubMed Scopus (0) Google Scholar] into TMS clinical practice [15Mir-Moghtadaei A. Siddiqi S.H. Mir-Moghtadaei K. Blumberger D.M. Vila-Rodriguez F. Daskalakis Z.J. et al.Updated scalp heuristics for localizing the dorsolateral prefrontal cortex based on convergent evidence of lesion and brain stimulation studies in depression.Brain Stimul. 2022; 15: 291-295https://doi.org/10.1016/j.brs.2022.01.013Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar, 16Andoh J. Riviere D. Mangin J.F. Artiges E. Cointepas Y. Grevent D. et al.A triangulation-based magnetic resonance image-guided method for transcranial magnetic stimulation coil positioning.Brain Stimul. 2009; 2: 123-131https://doi.org/10.1016/j.brs.2008.10.002Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 17Mir-Moghtadaei A. Dunlop K. Mansouri F. Giacobbe P. Kennedy S.H. Lam R.H. et al.Scalp-based heuristics for locating the nodes of the salience network for use in neurostimulation.Brain Stimul: Basic Translat Clinical Res Neuromodulat. 2017; 10: 479https://doi.org/10.1016/J.BRS.2017.01.404Abstract Full Text Full Text PDF Google Scholar]. The SGP provides a general approach to manually targeting individualized cortical targets without navigation systems. Specifically, the coil location can be computationally determined by the scalp point (pNZ, pAL) nearest to the cortical target in an individual's MRI and then manually located on the individual's scalp. Based on our previously established probabilistic transcranial mapping that relates each scalp point (pNZ, pAL) to a cortical position in MNI space [[10]Xiao X. Yu X. Zhang Z. Zhao Y. Jiang Y. Li Z. et al.Transcranial brain atlas.Sci Adv. 2018; 4eaar6904https://doi.org/10.1126/sciadv.aar6904Crossref Scopus (13) Google Scholar], the SGP thus gives an avenue to manually targeting cortical targets in MNI space, even without individual MRI data (Fig. 1C). Another competitive advantage of SGP is the inter-individual scalp comparability due to the common scalp landmarks and normalized curve length. This allows the SGP to act as a standard space to synthesize TMS therapeutic efficacy. In the future, the actual administered coil location and orientation can be manually recorded using a triplet of values (pNZ, pAL, θ) for each patient in daily clinical treatments. The accumulation of values with clinical improvement from different patients and centers can be organized into treatment atlases, which can guide clinical coil placement to maximize modulation efficacy. The potential applications of the SGP suggested above, however, should be methodologically and clinically validated in further studies. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. This work was supported by the National Natural Science Foundation of China (grant no. 82071999 and 61431002 ). The authors declare no competing financial interests. We thank Ye Xin for the assistance in conducting the experiments.

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