Research progress on transcranial electrical stimulation for deep brain stimulation_Journal of Biomedical Engineering

Authors：

MENG Weiyu ^1,2 , ZHANG Cheng ^1,2 , WU Changzhe ^1,2 , ZHANG Guanghao ^1,2 ,  HUO Xiaolin ^1,2

1. Beijing Key Laboratory of Bioelectromagnetism, Institute of Electrical Engineering, Chinese Academy of Sciences, Beijing 100190, P. R. China;
2. School of Electrical, Electronics and Communications Engineering, University of Chinese Academy of Sciences, Beijing 100149, P. R. China;

Corresponding author：

Keywords：

Transcranial electric stimulation; Strong current-transcranial alternating current stimulation; High-definition electrical stimulation; Temporal interference stimulation; Intersectional short pulse stimulation

DOI：

10.7507/1001-5515.202210012

Video：

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Transcranial electric stimulation (TES) is a non-invasive, economical, and well-tolerated neuromodulation technique. However, traditional TES is a whole-brain stimulation with a small current, which cannot satisfy the need for effectively focused stimulation of deep brain areas in clinical treatment. With the deepening of the clinical application of TES, researchers have constantly investigated new methods for deeper, more intense, and more focused stimulation, especially multi-electrode stimulation represented by high-precision TES and temporal interference stimulation. This paper reviews the stimulation optimization schemes of TES in recent years and further analyzes the characteristics and limitations of existing stimulation methods, aiming to provide a reference for related clinical applications and guide the following research on TES. In addition, this paper proposes the viewpoint of the development direction of TES, especially the direction of optimizing TES for deep brain stimulation, aiming to provide new ideas for subsequent research and application.

Citation： MENG Weiyu, ZHANG Cheng, WU Changzhe, ZHANG Guanghao, HUO Xiaolin. Research progress on transcranial electrical stimulation for deep brain stimulation. Journal of Biomedical Engineering, 2023, 40(5): 1005-1011. doi: 10.7507/1001-5515.202210012 Copy

1.	Zaghi S, Acar M, Hultgren B, et al. Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist, 2010, 16(3): 285-307.
2.	Helfrich R F, Schneider T R, Rach S, et al. Entrainment of brain oscillations by transcranial alternating current stimulation. Current Biology, 2014, 24(3): 333-339.
3.	Nasr K, Haslacher D, Dayan E, et al. Breaking the boundaries of interacting with the human brain using adaptive closed-loop stimulation. Progress in Neurobiology, 2022, 216: 102311.
4.	Krause M R, Zanos T P, Csorba B A, et al. Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain. Current Biology, 2017, 27(20): 3086-3096.
5.	Bradley C, Nydam A S, Dux P E, et al. State-dependent effects of neural stimulation on brain function and cognition. Nature Reviews Neuroscience, 2022, 23(8): 459-475.
6.	Voroslakos M, Takeuchi Y, Brinyiczki K, et al. Direct effects of transcranial electric stimulation on brain circuits in rats and humans. Nature Communications, 2018, 9(1): 483.
7.	Louviot S, Tyvaert L, Maillard L G, et al. Transcranial electrical stimulation generates electric fields in deep human brain structures. Brain Stimulation, 2022, 15(1): 1-12.
8.	White N E, Richards L M. Chapter 5-Nexalin and related forms of subcortical electrical stimulation. Rhythmic Stimulation Procedures in Neuromodulation. Academic Press, 2017: 131-157.
9.	Grover S, Wen W, Viswanathan V, et al. Long-lasting, dissociable improvements in working memory and long-term memory in older adults with repetitive neuromodulation. Nature Neuroscience, 2022, 25(9): 1237-1246.
10.	Grossman N, Bono D, Dedic N, et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell, 2017, 169(6): 1029-1041.
11.	Limoge A, Robert C, Stanley T H. Transcutaneous cranial electrical stimulation (TCES): a review 1998. Neuroscience and Biobehavioral Reviews, 1999, 23(4): 529-538.
12.	Lebedev V P, MalyginA V, KovalevskiA V, et al. Devices for noninvasive transcranial electrostimulation of the brain endorphinergic system: application for improvement of human psycho-physiological status. Artificial Organs, 2002, 26(3): 248-251.
13.	Katsnelson Y. Transcranial electrostimulation apparatus and method. US, 7769463B2. 2010-08-03.
14.	Shan Y, Wang H, Yang Y, et al. Evidence of a large current of transcranial alternating current stimulation directly to deep brain regions. Molecular Psychiatry, 2023. DOI: 10.1038/s41380-023-02150-8.
15.	Katsnelson Y. Transcranial electrostimulation device and method. US, 9186505B2. 2015-11-17.
16.	Katsnelson Y, Lapshin V, Claude J, et al. Transcranial electrotherapy stimulation device for temporary reduction of pain//Proceeding of the 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBS), Cancun, Mexico: IEEE, 2003, 25: 2285–2288.
17.	Wang H X, Wang K, Xue Q, et al. Transcranial alternating current stimulation for treating depression: a randomized controlled trial. Brain, 2022, 145(1): 83-91.
18.	Wang H X, Wang L, Zhang W R, et al. Effect of transcranial alternating current stimulation for the treatment of chronic insomnia: a randomized, double-blind, parallel-group, placebo-controlled clinical trial. Psychotherapy and Psychosomatics, 2020, 89(1): 38-47.
19.	Pellegrini M, Zoghi M, Jaberzadeh S. The effects of transcranial direct current stimulation on corticospinal and cortico-cortical excitability and response variability: conventional versus high-definition montages. Neuroscience Research, 2021, 166: 12-25.
20.	Chiang H S, Shakal S, Strain J F, et al. Reversal of unilateral hand movement dysfunction by high definition transcranial direct current stimulation in a patient with chronic traumatic brain injury. Brain Stimulation, 2022, 15(2): 283-285.
21.	Ghafoor U, Yang D, Hong K S. Neuromodulatory effects of HD-tACS/tDCS on the prefrontal cortex: a resting-state fNIRS-EEG study. IEEE Journal of Biomedical and Health Informatics, 2022, 26(5): 2192-2203.
22.	Iordan A D, Ryan S, Tyszkowski T, et al. High-definition transcranial direct current stimulation enhances network segregation during spatial navigation in mild cognitive impairment. Cerebral Cortex, 2022, 32(22): 5230-5241.
23.	Grover S, Nguyen J A, Viswanathan V, et al. High-frequency neuromodulation improves obsessive-compulsive behavior. Nature Medicine, 2021, 27(2): 232-238.
24.	Guo Z, Gong Y, Lu H, et al. Multitarget high-definition transcranial direct current stimulation improves response inhibition more than single-target high-definition transcranial direct current stimulation in healthy participants. Frontiers in Neuroscience, 2022, 16: 905247.
25.	Mikkonen M, Laakso I, Tanaka S, et al. Cost of focality in TDCS: interindividual variability in electric fields. Brain Stimulation, 2020, 13(1): 117-124.
26.	Huang Y, Parra L C. Can transcranial electric stimulation with multiple electrodes reach deep targets. Brain Stimulation, 2019, 12(1): 30-40.
27.	Wessel M J, Beanato E, Popa T, et al. Evidence for temporal interference (TI) stimulation effects on motor striatum. Brain Stimulation, 2021, 14(6): 1684.
28.	Sunshine M D, Cassarà A M, Neufeld E, et al. Restoration of breathing after opioid overdose and spinal cord injury using temporal interference stimulation. Communications Biology, 2021, 4(1): 107.
29.	Wang B, Aberra A, Grill W, et al. Comparing temporal interference stimulation and other kilohertz stimulation modalities using computational models. Brain Stimulation, 2021, 14(6): 1679.
30.	Mirzakhalili E, Barra B, Capogrosso M, et al. Biophysics of temporal interference stimulation. Cell System, 2020, 11(6): 557-572.
31.	Missey F, Rusina E, Acerbo E, et al. Orientation of temporal interference for non-invasive deep brain stimulation in epilepsy. Frontiers in Neuroscience, 2021, 15: 633988.
32.	Gomez-Tames J, Asai A, Hirata A. Multiscale computational model reveals nerve response in a mouse model for temporal interference brain stimulation. Frontiers in Neuroscience, 2021, 15: 684465.
33.	Terasawa Y, Tashiro H, Ueno T, et al. Precise temporal control of interferential neural stimulation via phase modulation. IEEE Transactions on Biomedical Engineering, 2022, 69(1): 220-228.
34.	Huang Y, Datta A, Parra L C. Optimization of interferential stimulation of the human brain with electrode arrays. Journal of Neural Engineering, 2020, 17(3): 036023.
35.	Rampersad S, Roig-Solvas B, Yarossi M, et al. Prospects for transcranial temporal interference stimulation in humans: a computational study. Neuroimage, 2019, 202: 116124.
36.	von Conta J, Kasten F H, Curcic-Blake B, et al. Interindividual variability of electric fields during transcranial temporal interference stimulation (tTIS). Scientific Reports, 2021, 11(1): 20357.
37.	Sorkhabi M M, Wendt K, Denison T. Temporally interfering TMS: focal and dynamic stimulation location//Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Montreal, Canada: IEEE Engn Med & Biol Soc. 2020: 3537-3543.
38.	Xin Z, Kuwahata A, Liu S, et al. Magnetically induced temporal interference for focal and deep-brain stimulation. Frontiers in Human Neuroscience, 2021, 15: 693207.
39.	Liu R, Ma R, Liu X, et al. A noninvasive deep brain stimulation method via temporal-spatial interference magneto-acoustic effect: simulation and experimental validation. IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control, 2022, 69(8): 2474-2483.
40.	Howell B, Mcintyre C C. Feasibility of interferential and pulsed transcranial electrical stimulation for neuromodulation at the human scale. Neuromodulation, 2021, 24(5): 843-853.
41.	Balzan P, Tattersall C, Palmer R. Non-invasive brain stimulation for treating neurogenic dysarthria: a systematic review. Annals of Physical and Rehabilitation Medicine, 2022, 65(5): 101580.
42.	Goswami C, Grover P. HingePlace: focused transcranial electrical current stimulation that allows subthreshold fields outside the stimulation target//Annual International Conference of The IEEE Engineering in Medicine and Biology Society, Mexico: IEEE Engn Med & Biol Soc, 2021: 1577-1583.
43.	Haslacher D, Nasr K, Robinson S E, et al. Stimulation artifact source separation (SASS) for assessing electric brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage, 2021, 228: 117571.
44.	Witkowski M, Garcia-Cossio E, Chander B S, et al. Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage, 2016, 140: 89-98.
45.	Hosseinian T, Yavari F, Biagi M C, et al. External induction and stabilization of brain oscillations in the human. Brain Stimulation, 2021, 14(3): 579-587.
46.	Parker T, Raghu A L B, Fitzgerald J J, et al. Multitarget deep brain stimulation for clinically complex movement disorders. Journal of Neurosurgery, 2020, 134(2): 351-356.
47.	Saturnino G B, Madsen K H, Thielscher A. Optimizing the electric field strength in multiple targets for multichannel transcranial electric stimulation. Journal of Neural Engineering, 2021, 18: 014001.

1. Zaghi S, Acar M, Hultgren B, et al. Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist, 2010, 16(3): 285-307.
2. Helfrich R F, Schneider T R, Rach S, et al. Entrainment of brain oscillations by transcranial alternating current stimulation. Current Biology, 2014, 24(3): 333-339.
3. Nasr K, Haslacher D, Dayan E, et al. Breaking the boundaries of interacting with the human brain using adaptive closed-loop stimulation. Progress in Neurobiology, 2022, 216: 102311.
4. Krause M R, Zanos T P, Csorba B A, et al. Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain. Current Biology, 2017, 27(20): 3086-3096.
5. Bradley C, Nydam A S, Dux P E, et al. State-dependent effects of neural stimulation on brain function and cognition. Nature Reviews Neuroscience, 2022, 23(8): 459-475.
6. Voroslakos M, Takeuchi Y, Brinyiczki K, et al. Direct effects of transcranial electric stimulation on brain circuits in rats and humans. Nature Communications, 2018, 9(1): 483.
7. Louviot S, Tyvaert L, Maillard L G, et al. Transcranial electrical stimulation generates electric fields in deep human brain structures. Brain Stimulation, 2022, 15(1): 1-12.
8. White N E, Richards L M. Chapter 5-Nexalin and related forms of subcortical electrical stimulation. Rhythmic Stimulation Procedures in Neuromodulation. Academic Press, 2017: 131-157.
9. Grover S, Wen W, Viswanathan V, et al. Long-lasting, dissociable improvements in working memory and long-term memory in older adults with repetitive neuromodulation. Nature Neuroscience, 2022, 25(9): 1237-1246.
10. Grossman N, Bono D, Dedic N, et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell, 2017, 169(6): 1029-1041.
11. Limoge A, Robert C, Stanley T H. Transcutaneous cranial electrical stimulation (TCES): a review 1998. Neuroscience and Biobehavioral Reviews, 1999, 23(4): 529-538.
12. Lebedev V P, MalyginA V, KovalevskiA V, et al. Devices for noninvasive transcranial electrostimulation of the brain endorphinergic system: application for improvement of human psycho-physiological status. Artificial Organs, 2002, 26(3): 248-251.
13. Katsnelson Y. Transcranial electrostimulation apparatus and method. US, 7769463B2. 2010-08-03.
14. Shan Y, Wang H, Yang Y, et al. Evidence of a large current of transcranial alternating current stimulation directly to deep brain regions. Molecular Psychiatry, 2023. DOI: 10.1038/s41380-023-02150-8.
15. Katsnelson Y. Transcranial electrostimulation device and method. US, 9186505B2. 2015-11-17.
16. Katsnelson Y, Lapshin V, Claude J, et al. Transcranial electrotherapy stimulation device for temporary reduction of pain//Proceeding of the 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBS), Cancun, Mexico: IEEE, 2003, 25: 2285–2288.
17. Wang H X, Wang K, Xue Q, et al. Transcranial alternating current stimulation for treating depression: a randomized controlled trial. Brain, 2022, 145(1): 83-91.
18. Wang H X, Wang L, Zhang W R, et al. Effect of transcranial alternating current stimulation for the treatment of chronic insomnia: a randomized, double-blind, parallel-group, placebo-controlled clinical trial. Psychotherapy and Psychosomatics, 2020, 89(1): 38-47.
19. Pellegrini M, Zoghi M, Jaberzadeh S. The effects of transcranial direct current stimulation on corticospinal and cortico-cortical excitability and response variability: conventional versus high-definition montages. Neuroscience Research, 2021, 166: 12-25.
20. Chiang H S, Shakal S, Strain J F, et al. Reversal of unilateral hand movement dysfunction by high definition transcranial direct current stimulation in a patient with chronic traumatic brain injury. Brain Stimulation, 2022, 15(2): 283-285.
21. Ghafoor U, Yang D, Hong K S. Neuromodulatory effects of HD-tACS/tDCS on the prefrontal cortex: a resting-state fNIRS-EEG study. IEEE Journal of Biomedical and Health Informatics, 2022, 26(5): 2192-2203.
22. Iordan A D, Ryan S, Tyszkowski T, et al. High-definition transcranial direct current stimulation enhances network segregation during spatial navigation in mild cognitive impairment. Cerebral Cortex, 2022, 32(22): 5230-5241.
23. Grover S, Nguyen J A, Viswanathan V, et al. High-frequency neuromodulation improves obsessive-compulsive behavior. Nature Medicine, 2021, 27(2): 232-238.
24. Guo Z, Gong Y, Lu H, et al. Multitarget high-definition transcranial direct current stimulation improves response inhibition more than single-target high-definition transcranial direct current stimulation in healthy participants. Frontiers in Neuroscience, 2022, 16: 905247.
25. Mikkonen M, Laakso I, Tanaka S, et al. Cost of focality in TDCS: interindividual variability in electric fields. Brain Stimulation, 2020, 13(1): 117-124.
26. Huang Y, Parra L C. Can transcranial electric stimulation with multiple electrodes reach deep targets. Brain Stimulation, 2019, 12(1): 30-40.
27. Wessel M J, Beanato E, Popa T, et al. Evidence for temporal interference (TI) stimulation effects on motor striatum. Brain Stimulation, 2021, 14(6): 1684.
28. Sunshine M D, Cassarà A M, Neufeld E, et al. Restoration of breathing after opioid overdose and spinal cord injury using temporal interference stimulation. Communications Biology, 2021, 4(1): 107.
29. Wang B, Aberra A, Grill W, et al. Comparing temporal interference stimulation and other kilohertz stimulation modalities using computational models. Brain Stimulation, 2021, 14(6): 1679.
30. Mirzakhalili E, Barra B, Capogrosso M, et al. Biophysics of temporal interference stimulation. Cell System, 2020, 11(6): 557-572.
31. Missey F, Rusina E, Acerbo E, et al. Orientation of temporal interference for non-invasive deep brain stimulation in epilepsy. Frontiers in Neuroscience, 2021, 15: 633988.
32. Gomez-Tames J, Asai A, Hirata A. Multiscale computational model reveals nerve response in a mouse model for temporal interference brain stimulation. Frontiers in Neuroscience, 2021, 15: 684465.
33. Terasawa Y, Tashiro H, Ueno T, et al. Precise temporal control of interferential neural stimulation via phase modulation. IEEE Transactions on Biomedical Engineering, 2022, 69(1): 220-228.
34. Huang Y, Datta A, Parra L C. Optimization of interferential stimulation of the human brain with electrode arrays. Journal of Neural Engineering, 2020, 17(3): 036023.
35. Rampersad S, Roig-Solvas B, Yarossi M, et al. Prospects for transcranial temporal interference stimulation in humans: a computational study. Neuroimage, 2019, 202: 116124.
36. von Conta J, Kasten F H, Curcic-Blake B, et al. Interindividual variability of electric fields during transcranial temporal interference stimulation (tTIS). Scientific Reports, 2021, 11(1): 20357.
37. Sorkhabi M M, Wendt K, Denison T. Temporally interfering TMS: focal and dynamic stimulation location//Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Montreal, Canada: IEEE Engn Med & Biol Soc. 2020: 3537-3543.
38. Xin Z, Kuwahata A, Liu S, et al. Magnetically induced temporal interference for focal and deep-brain stimulation. Frontiers in Human Neuroscience, 2021, 15: 693207.
39. Liu R, Ma R, Liu X, et al. A noninvasive deep brain stimulation method via temporal-spatial interference magneto-acoustic effect: simulation and experimental validation. IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control, 2022, 69(8): 2474-2483.
40. Howell B, Mcintyre C C. Feasibility of interferential and pulsed transcranial electrical stimulation for neuromodulation at the human scale. Neuromodulation, 2021, 24(5): 843-853.
41. Balzan P, Tattersall C, Palmer R. Non-invasive brain stimulation for treating neurogenic dysarthria: a systematic review. Annals of Physical and Rehabilitation Medicine, 2022, 65(5): 101580.
42. Goswami C, Grover P. HingePlace: focused transcranial electrical current stimulation that allows subthreshold fields outside the stimulation target//Annual International Conference of The IEEE Engineering in Medicine and Biology Society, Mexico: IEEE Engn Med & Biol Soc, 2021: 1577-1583.
43. Haslacher D, Nasr K, Robinson S E, et al. Stimulation artifact source separation (SASS) for assessing electric brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage, 2021, 228: 117571.
44. Witkowski M, Garcia-Cossio E, Chander B S, et al. Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage, 2016, 140: 89-98.
45. Hosseinian T, Yavari F, Biagi M C, et al. External induction and stabilization of brain oscillations in the human. Brain Stimulation, 2021, 14(3): 579-587.
46. Parker T, Raghu A L B, Fitzgerald J J, et al. Multitarget deep brain stimulation for clinically complex movement disorders. Journal of Neurosurgery, 2020, 134(2): 351-356.
47. Saturnino G B, Madsen K H, Thielscher A. Optimizing the electric field strength in multiple targets for multichannel transcranial electric stimulation. Journal of Neural Engineering, 2021, 18: 014001.

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