Application of fMRI in Transcranial Direct Current Stimulation Researches

doi:10.11938/cjmr20202805

Abstract

Abstract: Transcranial direct current stimulation (tDCS) noninvasively modulates the excitability of the brain, and is a promising method for treating diseases in the central nervous system. tDCS is safe, effective and affordable, and has been increasingly applied in neuroscience research. Functional magnetic resonance imaging (fMRI) is a widely-used tool to evaluate the therapeutic effects and the underlying neural mechanisms of tDCS. Herein we briefly reviewed the progresses of applications of fMRI in tDCS research. Both clinical trials and animal model experiments were discussed, as well as the perspectives of future applications.

Key words: transcranial direct current stimulation (tDCS), functional magnetic resonance imaging (fMRI), central nervous system

CLC Number:

O482.53

CHENG Li-wei, WANG Lu-lu, ZHONG Kai. Application of fMRI in Transcranial Direct Current Stimulation Researches[J]. Chinese Journal of Magnetic Resonance, 2020, 37(4): 533-546.

References

[1] LEFAUCHEUR J P, ANTAL A, AYACHE S, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS)[J]. Clin Neurophysiol, 2017, 128(1):56-92.
[2] LOLAS F. Brain polarization-behavioral and therapeutic effects[J]. Biol Psychiatry, 1977, 12(1):37-47.
[3] DYMOND A M, COGER R W, SERAFETINIDES E A. Intracerebral current levels in man during electrosleep therapy[J]. Biol Psychiatry, 1975, 10(1):101-104.
[4] OGAWA S, LEE T M, NAYAK A S, et al. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields[J]. Magn Reson Med, 1990, 14(1):68-78.
[5] BAUDEWIG J, NITSCHE M A, PAULUS W, et al. Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation[J]. Magn Reson Med, 2001, 45(2):196-201.
[6] CAVALIERE C, AIELLO M, DI PERRI C, et al. Functional connectivity substrates for tdcs response in minimally conscious state patients[J]. Front Cell Neurosci, 2016, 10:257.
[7] BINDMAN L J, LIPPOLD O C, REDFEARN J W. The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects[J]. J Physiol, 1964, 172(3):369-382.
[8] NITSCHE M A, PAULUS W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation[J]. J Physiol, 2000, 527(Pt 3):633-639.
[9] KASAHARA K, TANAKA S, HANAKAWA T, et al. Lateralization of activity in the parietal cortex predicts the effectiveness of bilateral transcranial direct current stimulation on performance of a mental calculation task[J]. Neurosci Lett, 2013, 545:86-90.
[10] KABAKOV A Y, MULLER P A, PASCUAL-LEONE A, et al. Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus[J]. J Neurophysiol, 2012, 107(7):1881-1889.
[11] BATSIKADZE G, MOLIADZE V, PAULUS W, et al. Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans[J]. J Physiol, 2013, 591(7):1987-2000.
[12] WAGNER T, FREGNI F, FECTEAU S, et al. Transcranial direct current stimulation:a computer-based human model study[J]. Neuroimage, 2007, 35(3):1113-1124.
[13] KWON O I, SAJIB S Z K, SERSA I, OH T I, et al. Current density imaging during transcranial direct current stimulation using DT-MRI and MREIT:Algorithm development and numerical simulations[J]. IEEE Trans Biomed Eng, 2016, 63(1):168-175.
[14] POLANIA R, PAULUS W, NITSCHE M A. Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation[J]. Hum Brain Mapp, 2012, 33(10):2499-2508.
[15] DYMOND A M, COGER R W, SERAFETINIDES E A. Intracerebral current levels in man during electrosleep therapy[J]. Biol Psychiatry, 1975, 10(1):101-104.
[16] RUOHONEN J, KARHU J. tDCS possibly stimulates glial cells[J]. Clin Neurophysiol, 2012, 123(10):2006-2009.
[17] BRAUN R, KLEIN R, WALTER H L, et al. Transcranial direct current stimulation accelerates recovery of function, induces neurogenesis and recruits oligodendrocyte precursors in a rat model of stroke[J]. Exp Neurol, 2016, 279:127-136.
[18] PELLETIER S J, LAGACE M, ST-AMOUR I, et al. The morphological and molecular changes of brain cells exposed to direct current electric field stimulation[J]. Int J Neuropsychopharmacol, 2015, 18(5):pyu090.
[19] TOSCHI F, LUGLI F, BISCARINI F, et al. Effects of electric field stress on a beta-amyloid peptide[J]. J Phys Chem B, 2009, 113(1):369-376.
[20] COFFMAN B A, CLARK V P, PARASURAMAN R. Battery powered thought:enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation[J]. Neuroimage, 2014, 85(3):895-908.
[21] ZHOU P, WEI J W, SUN C, et al. Research advancements in the regulation of transcranial direct current stimulation (tDCS) for cerebral cognitive function[J]. Chinese J Biomedical Engineering, 2018, 37(2):208-214. 周鹏, 魏晋文, 孙畅, 等. 经颅直流电刺激调控大脑认知功能的研究进展[J]. 中国生物医学工程学报, 2018, 37(2):208-214.
[22] FILIPPI M, AGOSTA F. Diffusion tensor imaging and functional MRI[M]//Neuroimaging Part II. Handb Clin Neurol, 2016, 136:1065-1087.
[23] CORDES D, TURSKI P A, SORENSON J A. Compensation of susceptibility-induced signal loss in echo-planar imaging for functional applications[J]. Magn Reson Imaging, 2000, 18(9):1055-1068.
[24] NIU M, LIU J L, ZHANG L. Modern Medicine & Health, 2008, 24(18):2754-2756. 牛猛, 刘嘉利, 张磊. FMRI脑功能磁共振成像的原理及应用进展[J]. 现代医药卫生, 2008, 24(18):2754-2756.
[25] FRISTON K. Causal modelling and brain connectivity in functional magnetic resonance imaging[J]. PLoS Biol, 2009, 7(2):e33.
[26] SMITHA K A, AKHIL RAJA K, ARUN K M, et al. Resting state fMRI:A review on methods in resting state connectivity analysis and resting state networks[J]. Neuroradiol J, 2017, 30(4):305-317.
[27] WOODS A J, HAMILTON R H, KRANJEC A, et al. Space, time, and causality in the human brain[J]. Neuroimage, 2014, 92:285-297.
[28] DEBENER S, BEAUDUCEL A, NESSLER D, et al. Is resting anterior EEG alpha asymmetry a trait marker for depression? Findings for healthy adults and clinically depressed patients[J]. Neuropsychobiology, 2000, 41(1):31-37.
[29] BULUBAS L, PADBERG F, BUENO P V, et al. Antidepressant effects of tDCS are associated with prefrontal gray matter volumes at baseline:Evidence from the ELECT-TDCS trial[J]. Brain Stimul, 2019, 12(5):1197-1204.
[30] PADBERG F, KUMPF U, MANSMANN U, et al. Prefrontal transcranial direct current stimulation (tDCS) as treatment for major depression:study design and methodology of a multicenter triple blind randomized placebo controlled trial (DepressionDC)[J]. Eur Arch Psychiatry Clin Neurosci, 2017, 267(8):751-766.
[31] CSIFCSAK G, BOAYUE N M, PUONTI O, et al. Effects of transcranial direct current stimulation for treating depression:A modeling study[J]. J Affect Disorders, 2018, 234:164-173.
[32] PALM U, HASAN A, STRUBE W, et al. tDCS for the treatment of depression:a comprehensive review[J]. Eur Arch Psychiatry Clin Neurosci, 2016, 266(8):681-694.
[33] KOENIGS M, GRAFMAN J. The functional neuroanatomy of depression:Distinct roles for ventromedial and dorsolateral prefrontal cortex[J]. Behav Brain Res, 2009, 201(2):239-243.
[34] THIBAUT A, CARVALHO S, MORSE L R, et al. Delayed pain decrease following M1 tDCS in spinal cord injury:A randomized controlled clinical trial[J]. Neurosci Lett, 2017, 658:19-26.
[35] NAEGEL S, BIERMANN J, THEYSOHN N, et al. Polarity-specific modulation of pain processing by transcranial direct current stimulation-a blinded longitudinal fMRI study[J]. J Headache Pain, 2018, 19(1):99.
[36] NGUYEN J P, NIZARD J, KERAVEL Y, et al. Invasive brain stimulation for the treatment of neuropathic pain[J]. Nat Rev Neurol, 2011, 7(12):699-709.
[37] NEEB L, BAYER A, BAYER K E, et al. Transcranial direct current stimulation in inflammatory bowel disease patients modifies resting-state functional connectivity:A RCT[J]. Brain Stimul, 2019, 12(4):978-980.
[38] LIN R L, DOUAUD G, FILIPPINI N, et al. Tracey I. Structural connectivity variances underlie functional and behavioral changes during pain relief induced by neuromodulation[J]. Sci Rep, 2017, 7:41603.
[39] ANTAL A, KRIENER N, LANG N, et al. Cathodal transcranial direct current stimulation of the visual cortex in the prophylactic treatment of migraine[J]. Cephalalgia, 2011, 31(7):820-828.
[40] MANOLA L, ROELOFSEN B H, HOLSHEIMER J, et al. Modelling motor cortex stimulation for chronic pain control:electrical potential field, activating functions and responses of simple nerve fibre models[J]. Med Biol Eng Comput, 2005, 43(3):335-43.
[41] CASTILLO-SAAVEDRA L, GEBODH N, BIKSON M, et al. Clinically effective treatment of fibromyalgia pain with high-definition transcranial direct current stimulation:phase II open-label dose optimization[J]. J Pain, 2016, 17(1):14-26.
[42] CUMMIFORD C M, NASCIMENTO T D, FOERSTER B R, et al. Changes in resting state functional connectivity after repetitive transcranial direct current stimulation applied to motor cortex in fibromyalgia patients[J]. Arthritis Res Ther, 2016, 18:40.
[43] KANI A S, SHINN A K, LEWANDOWSKI K E, et al. Converging effects of diverse treatment modalities on frontal cortex in schizophrenia:A review of longitudinal functional magnetic resonance imaging studies[J]. Psychiatr Res, 2017, 84:256-276.
[44] MONDINO M, HAESEBAERT F, POULET E, et al. Fronto-temporal transcranial Direct Current Stimulation (tDCS) reduces source-monitoring deficits and auditory hallucinations in patients with schizophrenia[J]. Schizophr Res, 2015, 161(2,3):515-516.
[45] MONDINO M, JARDRI R, SUAUD-CHAGNY M F, et al. Effects of Fronto-temporal transcranial direct current stimulation on auditory verbal hallucinations and resting-state functional connectivity of the left temporo-parietal junction in patients with schizophrenia[J]. Schizophr Bull, 2016, 42(2):318-326.
[46] PALM U, KEESER D, BLAUTZIK J, et al. Prefrontal transcranial direct current stimulation (tDCS) changes negative symptoms and functional connectivity MRI (fcMRI) in a single case of treatment-resistant schizophrenia[J]. Schizophr Res, 2013, 150(2-3):583-585.
[47] LANG N, SIEBNER H R, WARD N S, et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain?[J]. Eur J Neurosci, 2005, 22(2):495-504
[48] DI PINO G, PELLEGRINO G, ASSENZA G, et al. Modulation of brain plasticity in stroke:a novel model for neurorehabilitation[J]. Nat Rev Neurol, 2014, 10(10):597-608.
[49] NOWAK M, HINSON E, VAN EDE F, et al. Driving human motor cortical oscillations leads to behaviorally relevant changes in local GABA(A) inhibition:A tACS-TMS study[J]. J Neurosci, 2017, 37(17):4481-4492.
[50] BACHTIAR V, JOHNSTONE A, BERRINGTON A, et al. Modulating regional motor cortical excitability with noninvasive brain stimulation results in neurochemical changes in bilateral motor cortices[J]. Neurosci, 2018, 38(33):7327-7336.
[51] FIGLEWSKI K, BLICHER J U, MORTENSEN J, et al. Transcranial direct current stimulation potentiates improvements in functional ability in patients with chronic stroke receiving constraint-induced movement therapy[J]. Stroke, 2017, 48(1):229-232.
[52] WARD N S. Non-invasive brain stimulation for stroke recovery:ready for the big time?[J]. J Neurol Neurosur Ps, 2016, 87(4):343-344.
[53] KLOMJAI W, LACKMY-VALLEE A, ROCHE N, et al. Repetitive transcranial magnetic stimulation and transcranial direct current stimulation in motor rehabilitation after stroke:an update[J]. Ann Phys Rehabil Med, 2015, 58(4):220-224.
[54] ALLMAN C, AMADI U, WINKLER A M, et al. Ipsilesional anodal tDCS enhances the functional benefits of rehabilitation in patients after stroke[J]. Sci Transl Med, 2016, 8(330):330re1.
[55] BENNINGER D H, LOMAREV M, LOPEZ G, et al. Transcranial direct current stimulation for the treatment of Parkinson's disease[J]. J Neurol Neurosur Ps, 2010, 81(10):1105-1111.
[56] GALEA J M, JAYARAM G, AJAGBE L, et al. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation[J]. Neurosci, 2009, 29(28):9115-9122.
[57] D'MELLO A M, TURKELTAUB P E, STOODLEY C J. Cerebellar tDCS modulates neural circuits during semantic prediction:A combined tDCS-fMRI Study[J]. Neurosci, 2017, 37(6):1604-1613.
[58] FERRUCCI R, CORTESE F, BIANCHI M, et al. Cerebellar and motor cortical transcranial stimulation decrease levodopa-induced dyskinesias in Parkinson's disease[J]. Cerebellum, 2016, 15(1):43-47.
[59] FRESNOZA S, PAULUS W, NITSCHE M A, et al. Nonlinear dose-dependent impact of D1 receptor activation on motor cortex plasticity in humans[J]. Neurosci, 2014, 34(7):2744-2753.
[60] VALENTINO F, COSENTINO G, BRIGHINA F, et al. Transcranial direct current stimulation for treatment of freezing of gait:a cross-over study[J]. Mov Disord, 2014, 29(8):1064-1069.
[61] SCHOELLMANN A, SCHOLTEN M, WASSERKA B, et al. Anodal tDCS modulates cortical activity and synchronization in Parkinson's disease depending on motor processing[J]. Neuroimage Clin, 2019, 22:101689.
[62] CESPON J, RODELLA C, MINIUSSI C, et al. Behavioural and electrophysiological modulations induced by transcranial direct current stimulation in healthy elderly and Alzheimer's disease patients:A pilot study[J]. Clin Neurophysiol, 2019, 130(11):2038-2052.
[63] MEINZER M, LINDENBERG R, PHAN M T, et al. Transcranial direct current stimulation in mild cognitive impairment:Behavioral effects and neural mechanisms[J]. Alzheimers Dement, 2015, 11(9):1032-1140.
[64] BYSTAD M, GRONLI O, RASMUSSEN I D, et al. Transcranial direct current stimulation as a memory enhancer in patients with Alzheimer's disease:a randomized, placebo-controlled trial[J]. Alzheimers Res Ther, 2016, 8(1):13.
[65] FICEK B N, WANG Z, ZHAO Y, et al. The effect of tDCS on functional connectivity in primary progressive aphasia[J]. Neuroimage Clin, 2018, 19:703-715.
[66] FIORI V, KUNZ L, KUHNKE P, et al. Transcranial direct current stimulation (tDCS) facilitates verb learning by altering effective connectivity in the healthy brain[J]. Neuroimage, 2018, 181:550-559.
[67] ALEKSEICHUK I, DIERS K, PAULUS W, et al. Transcranial electrical stimulation of the occipital cortex during visual perception modifies the magnitude of BOLD activity:A combined tES-fMRI approach[J]. Neuroimage, 2016, 140:110-117.
[68] ROSSI S, ROSSINI P M. TMS in cognitive plasticity and the potential for rehabilitation[J]. Trends Cogn Sci, 2004, 8(6):273-279.
[69] FLÖEL A. tDCS-enhanced motor and cognitive function in neurological diseases[J]. Neuroimage, 2014, 85:934-947.
[70] KRAUSE M R, VIEIRA P G, CSORBA B A, et al. Transcranial alternating current stimulation entrains single-neuron activity in the primate brain[J]. Proc Natl Acad Sci U S A, 2019, 116(12):5747-5755.
[71] EDEMANN-CALLESEN H, HABELT B, WIESKE F, et al. Non-invasive modulation reduces repetitive behavior in a rat model through the sensorimotor cortico-striatal circuit[J]. Transl Psychiatry, 2018, 8(1):11.
[72] KIM H J, HAN S J. Anodal Transcranial direct current stimulation provokes neuroplasticity in repetitive mild traumatic brain injury in rats[J]. Neural Plast, 2017:1372946.
[73] TAKANO Y, YOKAWA T, MASUDA A, et al. A rat model for measuring the effectiveness of transcranial direct current stimulation using Fmri[J]. Neurosci Lett, 2011, 491(1):40-43.
[74] BEWERNICK B H, HURLEMANN R, MATUSCH A, et al. Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression[J]. Biol Psychiatry, 2010, 67(2):110-116.
[75] ANTONENKO D, THIELSCHER A, SATURNINO G B, et al. Towards precise brain stimulation:Is electric field simulation related to neuromodulation?[J]. Brain Stimul, 2019, 12(5):1159-1168.
[76] CIOBANU L, SOLOMON E, PYATIGORSKAYA N, et al. fMRI contrast at high and ultrahigh magnetic fields:insight from complementary methods[J]. Neuroimage, 2015, 113:37-43.
[77] SALLET J, MARS R B, NOONAN M P, et al. The organization of dorsal frontal cortex in humans and macaques[J]. J Neurosci, 2013, 33(30):12255-12274.
[78] MINKINA I, ROSENBERG S, KALINYAK-FLISZAR M, et al. Short-term memory and aphasia:from theory to treatment[J]. Semin Speech Lang, 2017, 38(1):17-28.
[79] CLARK M, STEGER-HARTMANN T. A big data approach to the concordance of the toxicity of pharmaceuticals in animals and humans[J]. Regul Toxicol Pharmacol, 2018, 96:94-105.
[80] TYSNES OB, STORSTEIN A. Epidemiology of Parkinson's disease[J]. J Neural Transm-supp, 2017, 124(8):901-905.
[81] OLSON H, BETTON G, ROBINSON D, et al. Concordance of the toxicity of pharmaceuticals in humans and in animals[J]. Regul Toxicol Pharmacal, 2000, 32(1):56-67.
[82] DUNLOP K, HANLON CA, DOWNAR J. Noninvasive brain stimulation treatments for addiction and major depression[J]. Ann N Y Acad Sci, 2017, 1394(1):31-54.
[83] WORSCHING J, PADBERG F, HELBICH K, et al. Test-retest reliability of prefrontal transcranial direct current stimulation (tDCS) effects on functional MRI connectivity in healthy subjects[J]. Neuroimage, 2017, 155:187-201.
[84] TREMBLAY S, LEPAGE J F, LATULIPE-LOISELLE A, et al. The uncertain outcome of prefrontal tDCS[J]. Brain Stimul, 2014, 7(6):773-783.
[85] SPORNS O. Contributions and challenges for network models in cognitive neuroscience[J]. Nat Neurosci, 2014, 17(5):652-660.
[86] SANDRINI M, XU B, VOLOCHAYEV R, et al. Transcranial direct current stimulation facilitates response inhibition through dynamic modulation of the fronto-basal ganglia network[J]. Brain Stimul, 2020, 13(1):96-104.
[87] ESMAEILPOUR Z, SHEREEN A D, GHOBADI-AZBARI P, et al. Methodology for tDCS integration with fMRI[J]. Hum Brain Mapp, 2019, 41(4):1950-1967.