Modulating Inhibitory Control Processes Using Individualized High Definition Theta Transcranial Alternating Current Stimulation (HD θ-tACS) of the Anterior Cingulate and Medial Prefrontal Cortex

. 2021 ; 15 () : 611507. [epub] 20210330

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33859554

Increased frontal midline theta activity generated by the anterior cingulate cortex (ACC) is induced by conflict processing in the medial frontal cortex (MFC). There is evidence that theta band transcranial alternating current stimulation (θ-tACS) modulates ACC function and alters inhibitory control performance during neuromodulation. Multi-electric (256 electrodes) high definition θ-tACS (HD θ-tACS) using computational modeling based on individual MRI allows precise neuromodulation targeting of the ACC via the medial prefrontal cortex (mPFC), and optimizes the required current density with a minimum impact on the rest of the brain. We therefore tested whether the individualized electrode montage of HD θ-tACS with the current flow targeted to the mPFC-ACC compared with a fixed montage (non-individualized) induces a higher post-modulatory effect on inhibitory control. Twenty healthy subjects were randomly assigned to a sequence of three HD θ-tACS conditions (individualized mPFC-ACC targeting; non-individualized MFC targeting; and a sham) in a double-blind cross-over study. Changes in the Visual Simon Task, Stop Signal Task, CPT III, and Stroop test were assessed before and after each session. Compared with non-individualized θ-tACS, the individualized HD θ-tACS significantly increased the number of interference words and the interference score in the Stroop test. The changes in the non-verbal cognitive tests did not induce a parallel effect. This is the first study to examine the influence of individualized HD θ-tACS targeted to the ACC on inhibitory control performance. The proposed algorithm represents a well-tolerated method that helps to improve the specificity of neuromodulation targeting of the ACC.

Zobrazit více v PubMed

Ahn S., Mellin J. M., Alagapan S., Alexander M. L., Gilmore J. H., Jarskog L. F., et al. (2019). Targeting reduced neural oscillations in patients with schizophrenia by transcranial alternating current stimulation. Neuroimage 186 126–136. 10.1016/j.neuroimage.2018.10.056 PubMed DOI PMC

Alam M., Truong D. Q., Khadka N., Bikson M. (2016). Spatial and polarity precision of concentric high-definition transcranial direct current stimulation (HD-tDCS). Phys. Med. Biol. 61 4506–4521. 10.1088/0031-9155/61/12/4506 PubMed DOI

Alfonso M. R., Miquel T. F., Xavier B., Blanca A. S. (2013). Resting parietal electroencephalogram asymmetries and self-reported attentional control. Clin. EEG Neurosci. 44 188–192. 10.1177/1550059412465871 PubMed DOI

Ali M. M., Sellers K. K., Fröhlich F. (2013). Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J. Neurosci. 33 11262–11275. 10.1523/jneurosci.5867-12.2013 PubMed DOI PMC

Antal A., Boros K., Poreisz C., Chaieb L., Terney D., Paulus W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul. 1 97–105. 10.1016/j.brs.2007.10.001 PubMed DOI

Antal A., Herrmann C. S. (2016). Transcranial alternating current and random noise stimulation: possible mechanisms. Neural Plast. 2016:3616807. 10.1155/2016/3616807 PubMed DOI PMC

Antal A., Paulus W. (2013). Transcranial alternating current stimulation (tACS). Front. Hum. Neurosci. 7:317. 10.3389/fnhum.2013.00317 PubMed DOI PMC

Berger A., Pixa N. H., Steinberg F., Doppelmayr M. (2018). Brain oscillatory and hemodynamic activity in a bimanual coordination task following transcranial alternating current stimulation (tACS): a combined EEG-fNIRS study. Front. Behav. Neurosci. 12:67. 10.3389/fnbeh.2018.00067 PubMed DOI PMC

Bergmann T. O., Karabanov A., Hartwigsen G., Thielscher A., Siebner H. R. (2016). Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: current approaches and future perspectives. Neuroimage 140 4–19. 10.1016/j.neuroimage.2016.02.012 PubMed DOI

Bialystok E., Craik F. I., Klein R., Viswanathan M. (2004). Bilingualism, aging, and cognitive control: evidence from the Simon task. Psychol. Aging 19:290. 10.1037/0882-7974.19.2.290 PubMed DOI

Bush G., Luu P., Posner M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4 215–222. 10.1016/S1364-6613(00)01483-2 PubMed DOI

Carter C. S., MacDonald A. W., III, Ross L. L., Stenger V. A. (2001). Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. Am. J. Psychiatry 158 1423–1428. 10.1176/appi.ajp.158.9.1423 PubMed DOI

Cavanagh J. F., Frank M. J. (2014). Frontal theta as a mechanism for cognitive control. Trends Cogn. Sci. 18 414–421. 10.1016/j.tics.2014.04.012 PubMed DOI PMC

Cavanagh J. F., Shackman A. J. (2015). Frontal midline theta reflects anxiety and cognitive control: meta-analytic evidence. J. Physiol. Paris 109 3–15. 10.1016/j.jphysparis.2014.04.003 PubMed DOI PMC

Chander B. S., Witkowski M., Braun C., Robinson S. E., Born J., Cohen L. G., et al. (2016). tACS phase locking of frontal midline theta oscillations disrupts working memory performance. Front. Cell Neurosci. 10:120. 10.3389/fncel.2016.00120 PubMed DOI PMC

Cipolotti L., Spanò B., Healy C., Tudor-Sfetea C., Chan E., White M., et al. (2016). Inhibition processes are dissociable and lateralized in human prefrontal cortex. Neuropsychologia 93 1–12. 10.1016/j.neuropsychologia.2016.09.018 PubMed DOI

Cohen M. X., Donner T. H. (2013). Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. J. Neurophysiol. 110 2752–2763. 10.1152/jn.00479.2013 PubMed DOI

Cohen M. X., Ridderinkhof K. R., Haupt S., Elger C. E., Fell J. (2008). Medial frontal cortex and response conflict: evidence from human intracranial EEG and medial frontal cortex lesion. Brain Res. 1238 127–142. 10.1016/j.brainres.2008.07.114 PubMed DOI

Conners C. (2014). Conners Continuous Performance Test, 3rd Edn. North Tonawanda, NY: Multi-Health Systems Inc.

Cunillera T., Brignani D., Cucurell D., Fuentemilla L., Miniussi C. (2016). The right inferior frontal cortex in response inhibition: a tDCS–ERP co-registration study. NeuroImage 140 66–75. 10.1016/j.neuroimage.2015.11.044 PubMed DOI

Dedoncker J., Brunoni A. R., Baeken C., Vanderhasselt M. A. (2016). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex in healthy and neuropsychiatric samples: influence of stimulation parameters. Brain Stimul. 9 501–517. 10.1016/j.brs.2016.04.006 PubMed DOI

Del Felice A., Castiglia L., Formaggio E., Cattelan M., Scarpa B., Manganotti P., et al. (2019). Personalized transcranial alternating current stimulation (tACS) and physical therapy to treat motor and cognitive symptoms in Parkinson’s disease: a randomized cross-over trial. NeuroImage Clin. 22:101768. 10.1016/j.nicl.2019.101768 PubMed DOI PMC

Dmochowski J. P., Datta A., Bikson M., Su Y., Parra L. C. (2011). Optimized multi-electrode stimulation increases focality and intensity at target. J. Neural Eng. 8:046011. 10.1088/1741-2560/8/4/046011 PubMed DOI

Dresler T., Mériau K., Heekeren H. R., van der Meer E. (2009). Emotional Stroop task: effect of word arousal and subject anxiety on emotional interference. Psychol. Res. 73 364–371. 10.1007/s00426-008-0154-6 PubMed DOI

Egner T. (2008). Multiple conflict-driven control mechanisms in the human brain. Trends Cogn. Sci. 12 374–380. 10.1016/j.tics.2008.07.001 PubMed DOI

Egner T., Delano M., Hirsch J. (2007). Separate conflict-specific cognitive control mechanisms in the human brain. NeuroImage 35 940–948. 10.1016/j.neuroimage.2006.11.061 PubMed DOI

Egner T., Hirsch J. (2005). Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat. Neurosci. 8:1784. 10.1038/nn1594 PubMed DOI

Fernández-Corazza M., Turovets S., Luu P., Anderson E., Tucker D. (2016). Transcranial electrical neuromodulation based on the reciprocity principle. Front. Psychiatry 7:87. 10.3389/fpsyt.2016.00087 PubMed DOI PMC

Fitzgerald K. D., Welsh R. C., Gehring W. J., Abelson J. L., Himle J. A., Liberzon I., et al. (2005). Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder. Biol. Psychiatry 57 287–294. 10.1016/j.biopsych.2004.10.038 PubMed DOI

Fusco G., Fusaro M., Aglioti S. (2020). Midfrontal-occipital θ-tACS modulates cognitive conflicts related to bodily stimuli. Soc. Cogn. Affect. Neurosci. nsaa125. 10.1093/scan/nsaa125 PubMed DOI PMC

Fusco G., Scandola M., Feurra M., Pavone E. F., Rossi S., Aglioti S. M. (2018). Midfrontal theta transcranial alternating current stimulation modulates behavioural adjustment after error execution. Eur. J. Neurosci. 48 3159–3170. 10.1111/ejn.14174 PubMed DOI

Gasquoine P. G. (2013). Localization of function in anterior cingulate cortex: from psychosurgery to functional neuroimaging. Neurosci. Biobehav. Rev. 37 340–348. 10.1016/j.neubiorev.2013.01.002 PubMed DOI

Gehring W. J., Coles M. G., Meyer D. E., Donchin E. (1995). A brain potential manifestation of error-related processing. Electroencephalogr. Clin. Neurophysiol. Suppl. 44 261–272. PubMed

Gratton G., Coles M. G. H., Sirevaag E. J., Eriksen C. W., Donchin E. (1988). Pre- and poststimulus activation of response channels: a psychophysiological analysis. J. Exp. Psychol. Hum. Percept. Perform. 14 331–344. 10.1037/0096-1523.14.3.331 PubMed DOI

Herrmann C., Rach S., Neuling T., Strüber D. (2013). Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front. Hum. Neurosci. 7:279. 10.3389/fnhum.2013.00279 PubMed DOI PMC

Hill A. T., Fitzgerald P. B., Hoy K. E. (2016). Effects of anodal transcranial direct current stimulation on working memory: a systematic review and meta-analysis of findings from healthy and neuropsychiatric populations. Brain Stimul. 9 197–208. 10.1016/j.brs.2015.10.006 PubMed DOI

Hoy K. E., Bailey N., Arnold S., Windsor K., John J., Daskalakis Z. J., et al. (2015). The effect of γ-tACS on working memory performance in healthy controls. Brain Cogn. 101 51–56. 10.1016/j.bandc.2015.11.002 PubMed DOI

Huster R. J., Enriquez-Geppert S., Lavallee C. F., Falkenstein M., Herrmann C. S. (2013). Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. Int. J. Psychophysiol. 87 217–233. 10.1016/j.ijpsycho.2012.08.001 PubMed DOI

Inquisit M. (2007). 3.0 [Computer Software]. Seattle, WA: Millisecond Software.

Kanai R., Paulus W., Walsh V. (2010). Transcranial alternating current stimulation (tACS) modulates cortical excitability as assessed by TMS-induced phosphene thresholds. Clin. Neurophysiol. 121 1551–1554. 10.1016/j.clinph.2010.03.022 PubMed DOI

Kaneda M., Osaka N. (2008). Role of anterior cingulate cortex during semantic coding in verbal working memory. Neurosci. Lett. 436 57–61. 10.1016/j.neulet.2008.02.069 PubMed DOI

Kopp B., Mattler U., Goertz R., Rist F. (1996a). N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming. Electroencephalogr. Clin. Neurophysiol. 99 19–27. 10.1016/0921-884X(96)95617-9 PubMed DOI

Kopp B., Rist F., Mattler U. (1996b). N200 in the flanker task as a neurobehavioral tool for investigating executive control. Psychophysiology 33 282–294. 10.1111/j.1469-8986.1996.tb00425.x PubMed DOI

Lamm C., Zelazo P. D., Lewis M. D. (2006). Neural correlates of cognitive control in childhood and adolescence: disentangling the contributions of age and executive function. Neuropsychologia 44 2139–2148. 10.1016/j.neuropsychologia.2005.10.013 PubMed DOI

Lang S., Gan L., Alrazi T., Monchi O. (2019). High definition transcranial alternating current stimulation of the right fusiform cortex improves visual associative memory. Brain Stimul. 12:429. 10.1016/j.brs.2018.12.389 PubMed DOI PMC

Lavric A., Pizzagalli D. A., Forstmeier S. (2004). When ‘go’and ‘nogo’are equally frequent: ERP components and cortical tomography. Eur. J. Neurosci. 20 2483–2488. 10.1111/j.1460-9568.2004.03683.x PubMed DOI

Lefaucheur J. P., Antal A., Ayache S. S., Benninger D. H., Brunelin J., Cogiamanian F., et al. (2017). Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin. Neurophysiol. 128 56–92. 10.1016/j.clinph.2016.10.087 PubMed DOI

Lehr A., Henneberg N., Nigam T., Paulus W., Antal A. (2019). Modulation of conflict processing by theta-range tACS over the Dorsolateral prefrontal cortex. Neural Plast. 2019:6747049. 10.1155/2019/6747049 PubMed DOI PMC

Lezak M. D., Howieson D. B., Loring D. W., Fischer J. S. (2004). Neuropsychological Assessment. New York, NY: Oxford University Press.

Luu P., Essaki Arumugam E. M., Anderson E., Gunn A., Rech D., Turovets S., et al. (2016). Slow-Frequency pulsed transcranial electrical stimulation for modulation of cortical plasticity based on reciprocity targeting with precision electrical head modeling. Front. Hum. Neurosci. 10:377. 10.3389/fnhum.2016.00377 PubMed DOI PMC

Luu P., Flaisch T., Tucker D. M. (2000). Medial frontal cortex in action monitoring. J. Neurosci. 20 464–469. 10.1523/JNEUROSCI.20-01-00464.2000 PubMed DOI PMC

Luu P., Tucker D. M., Makeig S. (2004). Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin. Neurophysiol. 115 1821–1835. 10.1016/j.clinph.2004.03.031 PubMed DOI

Moliadze V., Sierau L., Lyzhko E., Stenner T., Werchowski M., Siniatchkin M., et al. (2019). After-effects of 10 Hz tACS over the prefrontal cortex on phonological word decisions. Brain Stimul. 12 1464–1474. 10.1016/j.brs.2019.06.021 PubMed DOI

Neuling T., Ruhnau P., Weisz N., Herrmann C. S., Demarchi G. (2017). Faith and oscillations recovered: on analyzing EEG/MEG signals during tACS. NeuroImage 147 960–963. 10.1016/j.neuroimage.2016.11.022 PubMed DOI

Nigbur R., Cohen M. X., Ridderinkhof K. R., Stürmer B. (2012). Theta dynamics reveal domain-specific control over stimulus and response conflict. J. Cogn. Neurosci. 24 1264–1274. 10.1162/jocn_a_00128 PubMed DOI

Nikolin S., Loo C. K., Bai S., Dokos S., Martin D. M. (2015). Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning. NeuroImage 117 11–19. 10.1016/j.neuroimage.2015.05.019 PubMed DOI

Onoda K., Kawagoe T., Zheng H., Yamaguchi S. (2017). Theta band transcranial alternating current stimulations modulates network behavior of dorsal anterior cingulate cortex. Sci. Rep. 7:3607. 10.1038/s41598-017-03859-7 PubMed DOI PMC

Pahor A., Jaušovec N. (2018). The effects of theta and gamma tACS on working memory and electrophysiology. Front. Hum. Neurosci. 11:651. 10.3389/fnhum.2017.00651 PubMed DOI PMC

Paulus W. (2011). Transcranial electrical stimulation (tES – tDCS; tRNS, tACS) methods. Neuropsychol. Rehabil. 21 602–617. 10.1080/09602011.2011.557292 PubMed DOI

Peterson B. S., Kane M. J., Alexander G. M., Lacadie C., Skudlarski P., Leung H. C., et al. (2002). An event-related functional MRI study comparing interference effects in the Simon and Stroop tasks. Cogn. Brain Res. 13 427–440. 10.1016/S0926-6410(02)00054-X PubMed DOI

Poreisz C., Boros K., Antal A., Paulus W. (2007). Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res. Bull. 72 208–214. 10.1016/j.brainresbull.2007.01.004 PubMed DOI

Pratte M. S., Rouder J. N., Morey R. D., Feng C. (2010). Exploring the differences in distributional properties between Stroop and Simon effects using delta plots. Atten. Percept. Psychophys. 72 2013–2025. 10.3758/APP.72.7.2013 PubMed DOI

Reverberi C., Kuhlen A., Abutalebi J., Greulich R. S., Costa A., Seyed-Allaei S., et al. (2015). Language control in bilinguals: intention to speak vs. execution of speech. Brain Lang. 144 1–9. 10.1016/j.bandl.2015.03.004 PubMed DOI

Ruchsow M., Grön G., Reuter K., Spitzer M., Hermle L., Kiefer M. (2005). Error-related brain activity in patients with obsessive-compulsive disorder and in healthy controls. J. Psychophysiol. 19 298–304. 10.1027/0269-8803.19.4.298 DOI

Sela T., Kilim A., Lavidor M. (2012). Transcranial alternating current stimulation increases risk-taking behavior in the balloon analog risk task. Front. Neurosci. 6:22. 10.3389/fnins.2012.00022 PubMed DOI PMC

Soutschek A., Müller H. J., Schubert T. (2013). Conflict-specific effects of accessory stimuli on cognitive control in the Stroop task and the Simon task. Exp. Psychol. 60 140–148. 10.1027/1618-3169/a000181 PubMed DOI

Spielberg J. M., Miller G. A., Heller W., Banich M. T. (2015). Flexible brain network reconfiguration supporting inhibitory control. Proc. Natl. Acad. Sci. U.S.A. 112 10020–10025. 10.1073/pnas.1500048112 PubMed DOI PMC

StataCorp (2017). Stata Statistical Software: Release 15. College Station, TX: StataCorp LLC.

Taylor S. F., Stern E. R., Gehring W. J. (2007). Neural systems for error monitoring: recent findings and theoretical perspectives. Neuroscientist 13 160–172. 10.1177/1073858406298184 PubMed DOI

Ursu S., Stenger V. A., Shear M. K., Jones M. R., Carter C. S. (2003). Overactive action monitoring in obsessive-compulsive disorder: evidence from functional magnetic resonance imaging. Psychol. Sci. 14 347–353. 10.1111/1467-9280.24411 PubMed DOI

van Driel J., Sligte I. G., Linders J., Elport D., Cohen M. X. (2015). Frequency band-specific electrical brain stimulation modulates cognitive control processes. PLoS One 10:e0138984. 10.1371/journal.pone.0138984 PubMed DOI PMC

van Gaal S., Ridderinkhof K. R., van den Wildenberg W. P., Lamme V. A. (2009). Dissociating consciousness from inhibitory control: evidence for unconsciously triggered response inhibition in the stop-signal task. J. Exp. Psychol. Hum. Percept. Perform. 35:1129. 10.1037/a0013551 PubMed DOI

Van Noordt S. J. R., Campopiano A., Segalowitz S. J. (2016). A functional classification of medial frontal negativity ERPs: theta oscillations and single subject effects. Psychophysiology 53 1317–1334. 10.1111/psyp.12689 PubMed DOI

van Veen V., Carter C. S. (2002). The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiol. Behav. 77 477–482. 10.1016/S0031-9384(02)00930-7 PubMed DOI

Veniero D., Brignani D., Thut G., Miniussi C. (2011). Alpha-generation as basic response-signature to transcranial magnetic stimulation (TMS) targeting the human resting motor cortex: a TMS/EEG co-registration study. Psychophysiology 48 1381–1389. 10.1111/j.1469-8986.2011.01218.x PubMed DOI

Vossen A., Gross J., Thut G. (2015). Alpha power increase after transcranial alternating current stimulation at alpha frequency (α-tACS) reflects plastic changes rather than entrainment. Brain Stimul. 8 499–508. 10.1016/j.brs.2014.12.004 PubMed DOI PMC

Vosskuhl J., Huster R. J., Herrmann C. S. (2015). Increase in short-term memory capacity induced by down-regulating individual theta frequency via transcranial alternating current stimulation. Front. Hum. Neurosci. 9:257. 10.3389/fnhum.2015.00257 PubMed DOI PMC

Vosskuhl J., Huster R. J., Herrmann C. S. (2016). BOLD signal effects of transcranial alternating current stimulation (tACS) in the alpha range: a concurrent tACS–fMRI study. NeuroImage 140 118–125. 10.1016/j.neuroimage.2015.10.003 PubMed DOI

Williams E. J. (1949). Experimental designs balanced for the estimation of residual effects of treatments. Aust. J. Chem. 2 149–168. 10.1071/ch9490149 DOI

Wischnewski M., Zerr P., Schutter D. J. (2016). Effects of theta transcranial alternating current stimulation over the frontal cortex on reversal learning. Brain Stimul. 9 705–711. 10.1016/j.brs.2016.04.011 PubMed DOI

Witkowski M., Garcia-Cossio E., Chander B. S., Braun C., Birbaumer N., Robinson S. E., et al. (2016). Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). NeuroImage 140 89–98. 10.1016/j.neuroimage.2015.10.024 PubMed DOI

Yeung N., Botvinick M. M., Cohen J. D. (2004). The neural basis of error detection: conflict monitoring and the error-related negativity. Psychol. Rev. 111:931. 10.1037/0033-295X.111.4.931 PubMed DOI

Zaehle T., Rach S., Herrmann C. S. (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One 5:e13766. 10.1371/journal.pone.0013766 PubMed DOI PMC

Zaghi S., de Freitas Rezende L., de Oliveira L. M., El-Nazer R., Menning S., Tadini L., et al. (2010). Inhibition of motor cortex excitability with 15 Hz transcranial alternating current stimulation (tACS). Neurosci. Lett. 479 211–214. 10.1016/j.neulet.2010.05.060 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...