Transcranial direct current stimulation (tDCS) has emerged as a potentially effective intervention for improving consciousness levels in patients with disorders of consciousness (DoC). Most studies demonstrating benefits have targeted the left dorsolateral prefrontal cortex (DLPFC). However, inconsistent results have been reported across studies, and the brain effects of the stimulation remain unclear.
Objective
This work aimed to investigate the effects of a tDCS treatment on brain reactivity at rest in patients with DoC.
Methods
A 10-session tDCS treatment was administered over the left DLPFC in a group of patients with DoC. The effect of this stimulation was tested by combining the conventional behavioral assessment, conducted with the Coma Recovery Scale-Revised (CRS-R), with a quantitative analysis of the resting-state electrical brain activity, measured by electroencephalography (EEG).
Results
Following treatment, there was a slight improvement in CRS-R scores. More importantly, an increase in the ratio between alpha and theta power over posterior scalp regions was observed, even in patients who did not show changes in CRS-R scores.
Conclusions
These findings suggest that adding a simple quantitative EEG analysis alongside conventional clinical assessment post-tDCS could enhance the detection of changes in brain reactivity.
AmbrosiniE.VallesiA. (2016). Asymmetry in prefrontal resting-state EEG spectral power underlies individual differences in phasic and sustained cognitive control. Neuroimage, 124, 843–857. https://doi.org/10.1016/j.neuroimage.2015.09.035
2.
BaiY.XiaX.KangJ.YangY.HeJ.LiX. (2017). TDCS Modulates cortical excitability in patients with disorders of consciousness. NeuroImage: Clinical, 15, 702–709. https://doi.org/10.1016/j.nicl.2017.01.025
3.
BarraA.MontiM.ThibautA. (2022). Noninvasive brain stimulation therapies to promote recovery of consciousness: Where we are and where we should go. Seminars in Neurology, 42(03), 348–362. Thieme Medical Publishers, Inc. https://doi.org/10.1055/s-0042-1755562
CavaliereC.AielloM.Di PerriC.AmicoE.MartialC.ThibautA.LaureysS.SodduA. (2016). Functional connectivity substrates for tDCS response in minimally conscious state patients. Frontiers in Cellular Neuroscience, 10, 257. https://doi.org/10.3389/fncel.2016.00257
6.
CavinatoM.GennaC.FormaggioE.GregorioC.StortiS. F.ManganottiP.CasanovaE.PipernoR.PiccioneF. (2019). Behavioral and electrophysiological effects of tDCS to prefrontal cortex in patients with disorders of consciousness. Clinical Neurophysiology : Official Journal of the International Federation of Clinical Neurophysiology, 130(2), 231–238. https://doi.org/10.1016/j.clinph.2018.10.018
7.
ChennuS.AnnenJ.WannezS.ThibautA.ChatelleC.CassolH.MartensG.SchnakersC.GosseriesO.MenonD.LaureysS. (2017). Brain networks predict metabolism, diagnosis and prognosis at the bedside in disorders of consciousness. Brain : a Journal of Neurology, 140(8), 2120–2132. https://doi.org/10.1093/brain/awx163
8.
ChennuS.FinoiaP.KamauE.AllansonJ.WilliamsG. B.MontiM. M.NoreikaV.ArnatkeviciuteA.Canales-JohnsonA.OlivaresF.Cabezas-SotoD.MenonD. K.PickardJ. D.OwenA. M.BekinschteinT. A. (2014). Spectral signatures of reorganised brain networks in disorders of consciousness. PLoS Computational Biology, 10(10), e1003887. https://doi.org/10.1371/journal.pcbi.1003887
9.
DelormeA.MakeigS. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
10.
DongL.LiH.DangH.ZhangX.YueS.ZhangH. (2023). Efficacy of non-invasive brain stimulation for disorders of consciousness: A systematic review and meta-analysis. Frontiers in Neuroscience, 17, 1219043. https://doi.org/10.3389/fnins.2023.1219043
11.
EdlowB. L.ClaassenJ.SchiffN. D.GreerD. M. (2021). Recovery from disorders of consciousness: Mechanisms, prognosis and emerging therapies. Nature Reviews Neurology, 17(3), 135–156. https://doi.org/10.1038/s41582-020-00428-x
12.
EstraneoA.PascarellaA.MorettaP.MasottaO.FiorenzaS.ChiricoG.CrispinoE.LoretoV.TrojanoL. (2017). Repeated transcranial direct current stimulation in prolonged disorders of consciousness: A double-blind cross-over study. Journal of the Neurological Sciences, 375, 464–470. https://doi.org/10.1016/j.jns.2017.02.036
13.
FengY.ZhangJ.ZhouY.BaiZ.YinY. (2020). Noninvasive brain stimulation for patients with a disorder of consciousness: A systematic review and meta-analysis. Reviews in the Neurosciences, 31(8), 905–914. https://doi.org/10.1515/revneuro-2020-0033
14.
GiacinoJ. T.AshwalS.ChildsN.CranfordR.JennettB.KatzD. I.KellyJ. P.RosenbergJ. H.WhyteJ.ZafonteR. D.ZaslerN. D. (2002). The minimally conscious state: Definition and diagnostic criteria. Neurology, 58(3), 349–353. https://doi.org/10.1212/wnl.58.3.349
15.
GiacinoJ. T.FinsJ. J.LaureysS.SchiffN. D. (2014). Disorders of consciousness after acquired brain injury: The state of the science. Nature Reviews Neurology, 10(2), 99–114. https://doi.org/10.1038/nrneurol.2013.279
16.
GiacinoJ. T.KalmarK.WhyteJ. (2004). The JFK coma recovery scale-revised: Measurement characteristics and diagnostic utility. Archives of Physical Medicine and Rehabilitation, 85(12), 2020–2029. https://doi.org/10.1016/j.apmr.2004.02.033
17.
HanJ.ChenC.ZhengS.YanX.WangC.WangK.HuY. (2022). High-definition transcranial direct current stimulation of the dorsolateral prefrontal cortex modulates the electroencephalography rhythmic activity of parietal occipital lobe in patients with chronic disorders of consciousness. Frontiers in Human Neuroscience, 16, 889023. https://doi.org/10.3389/fnhum.2022.889023
18.
HermannB.RaimondoF.HirschL.HuangY.Denis-ValenteM.PérezP.EngemannD.FaugerasF.WeissN.DemeretS.RohautB.ParraL. C.SittJ. D.NaccacheL. (2020). Combined behavioral and electrophysiological evidence for a direct cortical effect of prefrontal tDCS on disorders of consciousness. Scientific Reports, 10(1), 4323. https://doi.org/10.1038/s41598-020-61180-2
19.
HuY.HuL.WangY.LuoX.ZhaoX.HeL. (2023). The effects of non-invasive brain stimulation on disorder of consciousness in patients with brain injury: A systematic review and meta-analysis of randomized controlled trial. Brain Research, 1822, 148633. https://doi.org/10.1016/j.brainres.2023.148633
20.
KeeserD.MeindlT.BorJ.PalmU.PogarellO.MulertC.BrunelinJ.MöllerH. J.ReiserM.PadbergF. (2011a). Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 31(43), 15284–15293. https://doi.org/10.1523/JNEUROSCI.0542-11.2011
21.
KeeserD.PadbergF.ReisingerE.PogarellO.KirschV.PalmU.KarchS.MöllerH. J.NitscheM. A.MulertC. (2011b). Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: A standardized low resolution tomography (sLORETA) study. NeuroImage, 55(2), 644–657. https://doi.org/10.1016/j.neuroimage.2010.12.004
22.
KingJ. R.SittJ. D.FaugerasF.RohautB.El KarouiI.CohenL.NaccacheL.DehaeneS. (2013). Information sharing in the brain indexes consciousness in noncommunicative patients. Current Biology : CB, 23(19), 1914–1919. https://doi.org/10.1016/j.cub.2013.07.075
23.
KulkarniV. P.LinK.BenbadisS. R. (2007). EEG Findings in the persistent vegetative state. Journal of Clinical Neurophysiology, 24(6), 433–437. https://doi.org/10.1097/WNP.0b013e31815c2810
24.
LefaucheurJ. P.AntalA.AyacheS. S.BenningerD. H.BrunelinJ.CogiamanianF.CotelliM.De RidderD.FerrucciR.LangguthB.MarangoloP.MyliusV.NitscheM. A.PadbergF.PalmU.PouletE.PrioriA.RossiS.SchecklmannM.VannesteS., …, PaulusW. (2017). Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clinical Neurophysiology : Official Journal of the International Federation of Clinical Neurophysiology, 128(1), 56–92. https://doi.org/10.1016/j.clinph.2016.10.087
25.
LlinásR. R.RibaryU.JeanmonodD.KronbergE.MitraP. P. (1999). Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proceedings of the National Academy of Sciences, 96(26), 15222–15227. https://doi.org/10.1073/pnas.96.26.15222
26.
MaH.ZhaoK.JiaC.YouJ.ZhouM.WangT.HuangC. (2023). Effect of transcranial direct current stimulation for patients with disorders of consciousness: A systematic review and meta-analysis. Frontiers in Neuroscience, 16, 1081278. https://doi.org/10.3389/fnins.2022.1081278
27.
MartensG.LejeuneN.O'BrienA. T.FregniF.MartialC.WannezS.LaureysS.ThibautA. (2018). Randomized controlled trial of home-based 4-week tDCS in chronic minimally conscious state. Brain Stimulation, 11(5), 982–990. https://doi.org/10.1016/j.brs.2018.04.021
28.
Romero LauroL. J.RosanovaM.MattavelliG.ConventoS.PisoniA.OpitzA.BologniniN.VallarG. (2014). TDCS Increases cortical excitability: Direct evidence from TMS-EEG. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 58, 99–111. https://doi.org/10.1016/j.cortex.2014.05.003
29.
SchiffN. D.NauvelT.VictorJ. D. (2014). Large-scale brain dynamics in disorders of consciousness. Current Opinion in Neurobiology, 25, 7–14. https://doi.org/10.1016/j.conb.2013.10.007
StaffordC. A.OwenA. M.Fernández-EspejoD. (2019). The neural basis of external responsiveness in prolonged disorders of consciousness. Neuroimage: Clinical, 22, 101791. https://doi.org/10.1016/j.nicl.2019.101791
32.
ThibautA.ChennuS.ChatelleC.MartensG.AnnenJ.CassolH.LaureysS. (2018). Theta network centrality correlates with tDCS response in disorders of consciousness. Brain Stimulation, 11(6), 1407–1409. https://doi.org/10.1016/j.brs.2018.09.002
33.
ThibautA.FregniF.EstraneoA.FiorenzaS.NoeE.LlorensR.FerriJ.FormisanoR.MoroneG.BenderA.RosenfelderM.LambertiG.KodratyevaE.KondratyevS.LegostaevaL.SuponevaN.KrewerC.MüllerF.DardenneN.JedidiH., …, IBIA DOC-SIG (2023). Sham-controlled randomized multicentre trial of transcranial direct current stimulation for prolonged disorders of consciousness. European Journal of Neurology, 30(10), 3016–3031. https://doi.org/10.1111/ene.15974
34.
ThibautA.SchiffN.GiacinoJ.LaureysS.GosseriesO. (2019). Therapeutic interventions in patients with prolonged disorders of consciousness. The Lancet Neurology, 18(6), 600–614. https://doi.org/10.1016/S1474-4422(19)30031-6
35.
UlamF.SheltonC.RichardsL.DavisL.HunterB.FregniF.HigginsK. (2015). Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury. Clinical Neurophysiology, 126(3), 486–496. https://doi.org/10.1016/j.clinph.2014.05.015
36.
VanhaudenhuyseA.DemertziA.SchabusM.NoirhommeQ.BredartS.BolyM.PhillipsC.SodduA.LuxenA.MoonenG.LaureysS. (2011). Two distinct neuronal networks mediate the awareness of environment and of self. Journal of Cognitive Neuroscience, 23(3), 570–578. https://doi.org/10.1162/jocn.2010.21488
37.
WadeD. T. (2018). How many patients in a prolonged disorder of consciousness might need a best interests meeting about starting or continuing gastrostomy feeding?Clinical Rehabilitation, 32(11), 1551–1564. https://doi.org/10.1177/0269215518777285
38.
WidmannA.SchrögerE.MaessB. (2015). Digital filter design for electrophysiological data–a practical approach. Journal of Neuroscience Methods, 250, 34–46. https://doi.org/10.1016/j.jneumeth.2014.08.002
39.
WuX.ZouQ.HuJ.TangW.MaoY.GaoL.ZhuJ.JinY.WuX.LuL.ZhangY.ZhangY.DaiZ.GaoJ. H.WengX.ZhouL.NorthoffG.GiacinoJ. T.HeY.YangY. (2015). Intrinsic functional connectivity patterns predict consciousness level and recovery outcome in acquired brain injury. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 35(37), 12932–12946. https://doi.org/10.1523/JNEUROSCI.0415-15.2015
40.
ZaehleT.SandmannP.ThorneJ. D.JänckeL.HerrmannC. S. (2011). Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: Combined behavioral and electrophysiological evidence. BMC Neuroscience, 12, 1–11. https://doi.org/10.1186/1471-2202-12-2
41.
ZhangC.HanS.LiZ.WangX.LvC.ZouX.ZhuF.ZhangK.LuS.BieL.LvG.GuoY. (2022). Multidimensional assessment of electroencephalography in the neuromodulation of disorders of consciousness. Frontiers in Neuroscience, 16, 903703. https://doi.org/10.3389/fnins.2022.903703
42.
ZhangY.SongW. (2018). Transcranial direct current stimulation in disorders of consciousness: A review. International Journal of Neuroscience, 128(3), 255–261. https://doi.org/10.1080/00207454.2017.1381094
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