Focal control of non-invasive deep brain stimulation using multipolar temporal interference
Status PubMed-not-MEDLINE Language English Country England, Great Britain Media electronic
Document type Journal Article
Grant support
101088623
European Research Council - International
101088623
European Research Council - International
101088623
European Research Council - International
101088623
European Research Council - International
MOP-93796
CIHR - Canada
MOP-93796
CIHR - Canada
MOP-93796
CIHR - Canada
MOP-93796
CIHR - Canada
PubMed
40140933
PubMed Central
PMC11948895
DOI
10.1186/s42234-025-00169-6
PII: 10.1186/s42234-025-00169-6
Knihovny.cz E-resources
- Keywords
- Focality, Multipolar, Non-Human Primate, Stimulation, Temporal Interference, Temporally Interfering Electric Fields,
- Publication type
- Journal Article MeSH
Temporal interference (TI) is a method of non-invasive brain stimulation using transcutaneous electrodes which allows the targeting and modulation of deeper brain structures, not normally associated with non-invasive simulation, while avoiding unwanted stimulation of shallower cortical structures. The properties of TI have been previously demonstrated, however, the problem of decoupling stimulation focality from stimulation intensity has not yet been well addressed. In this paper, we provide a possible novel solution, multipolar TI (mTI), which allows increased independent control over both the size of the stimulated region and the stimulation intensity. The mTI method uses multiple carrier frequencies to create multiple overlapping amplitude-modulated envelopes, rather than using one envelope as in standard TI. The study presents an explanation of the concept of mTI along with experimental data gathered from Rhesus macaques and mice. We improved the focality at depth in anesthetized mice and monkeys, and using the new focality in awake monkeys, evoked targeted activity at depth in the superior colliculus. The mTI method could be an interesting and potentially useful new tool alongside other forms of non-invasive brain stimulation. Teaser Multipolar Temporal Interference Stimulation can produce a more focal brain stimulation at depth compared to Temporal Interference.
Department of Mathematics Western University London ON N6A 5B7 Canada
Department of Physiology and Pharmacology Western University London ON N6A 5B7 Canada
Department of Psychology Western University London ON N6A 5B7 Canada
Graduate Program in Neuroscience Western University London ON N6A 5B7 Canada
Institut de Neurosciences Des Systèmes UMR_1106 INSERM Aix Marseille Université Marseille France
International Clinical Research Center St Anne'S University Hospital Brno Czech Republic
IT'IS Foundation for Research on Information Technologies in Society 8004 Zurich Switzerland
Robarts Research Institute Western University London ON N6A 5B7 Canada
See more in PubMed
Acerbo E, Jegou A, Luff C, et al. Focal non-invasive deep-brain stimulation with temporal interference for the suppression of epileptic biomarkers. Front Neurosci. 2022a;16:945221. 10.3389/fnins.2022.945221. PubMed PMC
Acerbo E, Jegou A, Luff C, et al. Focal non-invasive deep-brain stimulation with temporal interference for the suppression of epileptic biomarkers. Frontiers in Neuroscience. 2022;16. Accessed September 7, 2022. https://www.frontiersin.org/articles/10.3389/fnins.2022.945221 PubMed PMC
Acerbo, Missey et al. n.d., Non-invasive Temporal Interference Stimulation of the Hippocampus Suppresses Epileptic Biomarkers in Patients with Epilepsy: Biophysical Differences between Kilohertz and Amplitude Modulated Stimulation, preprint, https://www.medrxiv.org/content/10.1101/2024.12.05.24303799v1
Botzanowski B, Donahue MJ, Ejneby MS, et al. Noninvasive Stimulation of Peripheral Nerves using Temporally-Interfering Electrical Fields. Adv Healthcare Mater. 2022;11(17):2200075. 10.1002/adhm.202200075. PubMed PMC
Cao J, Grover P. STIMULUS: Noninvasive Dynamic Patterns of Neurostimulation Using Spatio-Temporal Interference. IEEE Trans Biomed Eng. 2020;67(3):726–37. 10.1109/TBME.2019.2919912. PubMed
Corneil BD, Olivier E, Munoz DP. Neck muscle responses to stimulation of monkey superior colliculus. I. Topography and manipulation of stimulation parameters. J Neurophysiol. 2002;88(4):1980–1999. 10.1152/jn.2002.88.4.1980 PubMed
Deng ZD, Lisanby SH, Peterchev AV. Electric field depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs. Brain Stimul. 2013;6(1):1–13. 10.1016/j.brs.2012.02.005. PubMed PMC
Florian M, Rusina E, Acerbo E, et al. Orientation of Temporal Interference for Non-invasive Deep Brain Stimulation in Epilepsy. Front Neurosci. 2021;15:633988. 10.3389/fnins.2021.633988. PubMed PMC
Gandhi NJ, Katnani HA. Motor functions of the superior colliculus. Annu Rev Neurosci. 2011;34:205–31. 10.1146/annurev-neuro-061010-113728. PubMed PMC
George DD, Ojemann SG, Drees C, Thompson JA. Stimulation Mapping Using Stereoelectroencephalography: Current and Future Directions. Front Neurol. 2020;11:320. 10.3389/fneur.2020.00320. PubMed PMC
Grossman N, Bono D, Dedic N, et al. Noninvasive Deep Brain Stimulation via Temporally Interfering Electric Fields. Cell. 2017;169(6):1029-1041.e16. 10.1016/j.cell.2017.05.024. PubMed PMC
Goldberg ME, Wurtz RH. Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. J Neurophysiol. 1972;35(4):542–559. 10.1152/jn.1972.35.4.542 PubMed
Huang Y, Parra LC. Can transcranial electric stimulation with multiple electrodes reach deep targets? Brain Stimul. 2019;12(1):30–40. 10.1016/j.brs.2018.09.010. PubMed PMC
Hwang J, Mitz AR, Murray EA. NIMH MonkeyLogic: Behavioral control and data acquisition in MATLAB. J Neurosci Methods. 2019;323:13–21. 10.1016/j.jneumeth.2019.05.002. PubMed PMC
IT’IS Database for Thermal and Electromagnetic Parameters of Biological Tissues – ScienceOpen. Accessed August 20, 2024. https://www.scienceopen.com/document?vid=a95fbaa4-efd8-429a-a59e-5e208fea2e45
Klomjai W, Katz R, Lackmy-Vallée A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med. 2015;58(4):208–13. 10.1016/j.rehab.2015.05.005. PubMed
Lehmann SJ, Corneil BD. Transient Pupil Dilation after Subsaccadic Microstimulation of Primate Frontal Eye Fields. J Neurosci. 2016;36(13):3765–76. 10.1523/JNEUROSCI.4264-15.2016. PubMed PMC
Lee S, Park J, Choi DS, Lee C, Im CH. Multipair transcranial temporal interference stimulation for improved focalized stimulation of deep brain regions: A simulation study. Comput Biol Med. 2022;143:105337. 10.1016/j.compbiomed.2022.105337. PubMed
Lehmann SJ, Corneil BD. Completing the puzzle: Why studies in non-human primates are needed to better understand the effects of non-invasive brain stimulation. Neurosci Biobehav Rev. 2022;132:1074–85. 10.1016/j.neubiorev.2021.10.040. PubMed
Mikkonen M, Laakso I, Tanaka S, Hirata A. Cost of focality in TDCS: Interindividual variability in electric fields. Brain Stimul. 2020;13(1):117–24. 10.1016/j.brs.2019.09.017. PubMed
Missey et al., “Laser-driven wireless temporal interference using organic electrolytic photocapacitors for chronic deep brain stimulation of the mouse hippocampus”, Advanced Functional Materials, 2200691 (2022)
Missey F, Ejneby MS, Ngom I, et al. Obstructive sleep apnea improves with non-invasive hypoglossal nerve stimulation using temporal interference. Bioelectron Med. 2023;9(1):18. 10.1186/s42234-023-00120-7. PubMed PMC
Morel P. Gramm: grammar of graphics plotting in Matlab. Journal of Open Source Software. 2018;3(23):568. 10.21105/joss.00568.
Mueller JK, Grigsby EM, Prevosto V, et al. Simultaneous transcranial magnetic stimulation and single-neuron recording in alert non-human primates. Nat Neurosci. 2014;17(8):1130–6. 10.1038/nn.3751. PubMed PMC
Munoz DP, Fecteau JH. Vying for dominance: dynamic interactions control visual fixation and saccadic initiation in the superior colliculus. Prog Brain Res. 2002;140:3–19. 10.1016/S0079-6123(02)40039-8. PubMed
Paxinos G, Huang XF, Toga A. The Rhesus Monkey Brain in Stereotaxic Coordinates. Faculty of Health and Behavioural Sciences - Papers (Archive). Published online January 1, 2000. https://ro.uow.edu.au/hbspapers/3613
Peel TR, Dash S, Lomber SG, Corneil BD. Frontal Eye Field Inactivation Diminishes Superior Colliculus Activity, But Delayed Saccadic Accumulation Governs Reaction Time Increases. J Neurosci. 2017;37(48):11715–30. 10.1523/JNEUROSCI.2664-17.2017. PubMed PMC
Rezvani S, Corneil Bd. Recruitment of a head-turning synergy by low-frequency activity in the primate superior colliculus. Journal of neurophysiology. 2008;100(1). 10.1152/jn.90223.2008 PubMed
Ritter P, Schirner M, McIntosh AR, Jirsa VK. The virtual brain integrates computational modeling and multimodal neuroimaging. Brain Connect. 2013;3(2):121–45. 10.1089/brain.2012.0120. PubMed PMC
Rossini PM, Burke D, Chen R, et al. 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. 2015;126(6):1071–1107. 10.1016/j.clinph.2015.02.001 PubMed PMC
Roy AV, Camchong J, Lim KO. Principles and Applications of Transcranial Electrical Stimulation. In: Engineering in Medicine. Elsevier; 2019:319–334. 10.1016/B978-0-12-813068-1.00012-9
Romero MC, Davare M, Armendariz M, Janssen P. Neural effects of transcranial magnetic stimulation at the single-cell level. Nat Commun. 2019;10(1):2642. 10.1038/s41467-019-10638-7. PubMed PMC
Stanford TR, Freedman EG, Sparks DL. Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J Neurophysiol. 1996;76(5):3360–81. 10.1152/jn.1996.76.5.3360. PubMed
Thompson KG, Hanes DP, Bichot NP, Schall JD. Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J Neurophysiol. 1996;76(6):4040–55. 10.1152/jn.1996.76.6.4040. PubMed
Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9:527–65. 10.1146/annurev.bioeng.9.061206.133100. PubMed
Wang CA, Munoz DP. Coordination of Pupil and Saccade Responses by the Superior Colliculus. J Cogn Neurosci. 2021;33(5):919–32. 10.1162/jocn_a_01688. PubMed
Wang CA, Boehnke SE, White BJ, Munoz DP. Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. J Neurosci. 2012;32(11):3629–36. 10.1523/JNEUROSCI.5512-11.2012. PubMed PMC
Wurtz RH, Goldberg ME. Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. J Neurophysiol. 1972;35(4):575–586. 10.1152/jn.1972.35.4.575 PubMed
Zhu X, Li Y, Zheng L, et al. Multi-Point Temporal Interference Stimulation by Using Each Electrode to Carry Different Frequency Currents. IEEE Access. 2019;7:168839–48. 10.1109/ACCESS.2019.2947857.