Impact of Electric Field Magnitude in the Left Dorsolateral Prefrontal Cortex on Changes in Intrinsic Functional Connectivity Using Transcranial Direct Current Stimulation: A Randomized Crossover Study.

Publisher: Wiley Interscience Country of Publication: United States NLM ID: 7600111 Publication Model: Print Cited Medium: Internet ISSN: 1097-4547 (Electronic) Linking ISSN: 03604012 NLM ISO Abbreviation: J Neurosci Res Subsets: MEDLINE

Publication: New York, NY : Wiley Interscience
Original Publication: New York, Liss.

Transcranial Direct Current Stimulation*/methods ; Cross-Over Studies* ; Magnetic Resonance Imaging* ; Dorsolateral Prefrontal Cortex*/physiology; Humans ; Male ; Female ; Adult ; Young Adult ; Neural Pathways/physiology ; Prefrontal Cortex/physiology ; Prefrontal Cortex/diagnostic imaging ; Brain Mapping

This study investigated whether the electric field magnitude (E-field) delivered to the left dorsolateral prefrontal cortex (L-DLPFC) changes resting-state brain activity and the L-DLPFC resting-state functional connectivity (rsFC), given the variability in tDCS response and lack of understanding of how rsFC changes. Twenty-one healthy participants received either 2 mA anodal or sham tDCS targeting the L-DLPFC for 10 min. Brain imaging was conducted before and after stimulation. The fractional amplitude of low-frequency fluctuation (fALFF), reflecting resting brain activity, and the L-DLPFC rsFC were analyzed to investigate the main effect of tDCS, main effect of time, and interaction effects. The E-field was estimated by modeling tDCS-induced individual electric fields and correlated with fALFF and L-DLPFC rsFC. Anodal tDCS increased fALFF in the left rostral middle frontal area and decreased fALFF in the midline frontal area (FWE p < 0.050), whereas sham induced no changes. Overall rsFC decreased after sham (positive and negative connectivity, p = 0.001 and 0.020, respectively), with modest and nonsignificant changes after anodal tDCS (p = 0.063 and 0.069, respectively). No significant differences in local rsFC were observed among the conditions. Correlations were observed between the E-field and rsFC changes in the L-DLPFC (r = 0.385, p = 0.115), left inferior parietal area (r = 0.495, p = 0.037), and right lateral visual area (r = 0.683, p = 0.002). Single-session tDCS induced resting brain activity changes and may help maintain overall rsFC. The E-field in the L-DLPFC is associated with rsFC changes in both proximal and distally connected brain regions to the L-DLPFC.
(© 2024 The Author(s). Journal of Neuroscience Research published by Wiley Periodicals LLC.)

Abellaneda‐Perez, K., L. Vaqué‐Alcázar, R. Perellón‐Alfonso, et al. 2021. “Multifocal Transcranial Direct Current Stimulation Modulates Resting‐State Functional Connectivity in Older Adults Depending on the Induced Current Density.” Frontiers in Aging Neuroscience 13: 725013.
Andersson, J. L., S. Skare, and J. Ashburner. 2003. “How to Correct Susceptibility Distortions in Spin‐Echo Echo‐Planar Images: Application to Diffusion Tensor Imaging.” NeuroImage 20, no. 2: 870–888.
Antonenko, D., A. Thielscher, G. B. Saturnino, et al. 2019. “Towards Precise Brain Stimulation: Is Electric Field Simulation Related to Neuromodulation?” Brain Stimulation 12, no. 5: 1159–1168.
Barbey, A. K., R. Colom, J. Solomon, F. Krueger, C. Forbes, and J. Grafman. 2012. “An Integrative Architecture for General Intelligence and Executive Function Revealed by Lesion Mapping.” Brain 135, no. Pt 4: 1154–1164.
Bastani, A., and S. Jaberzadeh. 2013. “Differential Modulation of Corticospinal Excitability by Different Current Densities of Anodal Transcranial Direct Current Stimulation.” PLoS ONE 8, no. 8: e72254.
Berna, C., S. Leknes, E. A. Holmes, R. R. Edwards, G. M. Goodwin, and I. Tracey. 2010. “Induction of Depressed Mood Disrupts Emotion Regulation Neurocircuitry and Enhances Pain Unpleasantness.” Biological Psychiatry 67, no. 11: 1083–1090.
Berryhill, M. E., and D. Martin. 2018. “Cognitive Effects of Transcranial Direct Current Stimulation in Healthy and Clinical Populations: An Overview.” Journal of ECT 34, no. 3: e25–e35.
Biswal, B., F. Zerrin Yetkin, V. M. Haughton, and J. S. Hyde. 1995. “Functional Connectivity in the Motor Cortex of Resting Human Brain Using Echo‐Planar MRI.” Magnetic Resonance in Medicine 34, no. 4: 537–541.
Boggio, P. S., F. Bermpohl, A. O. Vergara, et al. 2007. “Go‐No‐Go Task Performance Improvement After Anodal Transcranial DC Stimulation of the Left Dorsolateral Prefrontal Cortex in Major Depression.” Journal of Affective Disorders 101, no. 1–3: 91–98.
Brunoni, A. R., M. A. Nitsche, N. Bolognini, et al. 2012. “Clinical Research With Transcranial Direct Current Stimulation (tDCS): Challenges and Future Directions.” Brain Stimulation 5, no. 3: 175–195.
Chan, M. M. Y., S. S. Y. Yau, and Y. M. Y. Han. 2021. “The Neurobiology of Prefrontal Transcranial Direct Current Stimulation (tDCS) in Promoting Brain Plasticity: A Systematic Review and Meta‐Analyses of Human and Rodent Studies.” Neuroscience and Biobehavioral Reviews 125: 392–416.
Chew, T., K.‐A. Ho, and C. K. Loo. 2015. “Inter‐and Intra‐Individual Variability in Response to Transcranial Direct Current Stimulation (tDCS) at Varying Current Intensities.” Brain Stimulation 8, no. 6: 1130–1137.
Corbetta, M., and G. Shulman. 2002. “Control of Goal‐Directed and Stimulus‐Driven Attention in the Brain.” Nature Reviews. Neuroscience 3, no. 3: 201–215.
Datta, A., M. Elwassif, F. Battaglia, and M. Bikson. 2008. “Transcranial Current Stimulation Focality Using Disc and Ring Electrode Configurations: FEM Analysis.” Journal of Neural Engineering 5, no. 2: 163–174.
Dedoncker, J., A. R. Brunoni, C. Baeken, and M. A. Vanderhasselt. 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 Stimulation 9, no. 4: 501–517.
Deng, S., C. G. Franklin, M. O'Boyle, et al. 2022. “Hemodynamic and Metabolic Correspondence of Resting‐State Voxel‐Based Physiological Metrics in Healthy Adults.” NeuroImage 250: 118923.
Faul, F., E. Erdfelder, A. Buchner, and A.‐G. Lang. 2009. “Statistical Power Analyses Using G*Power 3.1: Tests for Correlation and Regression Analyses.” Behavior Research Methods 41, no. 4: 1149–1160.
Faul, F., E. Erdfelder, A.‐G. Lang, and A. Buchner. 2007. “G*Power 3: A Flexible Statistical Power Analysis Program for the Social, Behavioral, and Biomedical Sciences.” Behavior Research Methods 39, no. 2: 175–191.
Fox, M. D., and M. E. Raichle. 2007. “Spontaneous Fluctuations in Brain Activity Observed With Functional Magnetic Resonance Imaging.” Nature Reviews Neuroscience 8, no. 9: 700–711.
Fox, M. D., A. Z. Snyder, J. L. Vincent, M. Corbetta, D. C. Van Essen, and M. E. Raichle. 2005. “The Human Brain Is Intrinsically Organized Into Dynamic, Anticorrelated Functional Networks.” Proceedings of the National Academy of Sciences of the United States of America 102, no. 27: 9673–9678.
Gordon, E. M., A. L. Breeden, S. E. Bean, and C. J. Vaidya. 2014. “Working Memory‐Related Changes in Functional Connectivity Persist Beyond Task Disengagement.” Human Brain Mapping 35, no. 3: 1004–1017.
Halko, M., A. Datta, E. B. Plow, J. Scaturro, M. Bikson, and L. B. Merabet. 2011. “Neuroplastic Changes Following Rehabilitative Training Correlate With Regional Electrical Field Induced With tDCS.” NeuroImage 57, no. 3: 885–891.
Harmelech, T., S. Preminger, E. Wertman, and R. Malach. 2013. “The Day‐After Effect: Long Term, Hebbian‐Like Restructuring of Resting‐State fMRI Patterns Induced by a Single Epoch of Cortical Activation.” Journal of Neuroscience 33, no. 22: 9488–9497.
Indahlastari, A., A. Albizu, J. N. Kraft, et al. 2021. “Individualized tDCS Modeling Predicts Functional Connectivity Changes Within the Working Memory Network in Older Adults.” Brain Stimulation 14, no. 5: 1205–1215.
Jamil, A., G. Batsikadze, H. I. Kuo, et al. 2020. “Current Intensity‐ and Polarity‐Specific Online and Aftereffects of Transcranial Direct Current Stimulation: An fMRI Study.” Human Brain Mapping 41, no. 6: 1644–1666.
Kar, K., T. Ito, M. W. Cole, and B. Krekelberg. 2020. “Transcranial Alternating Current Stimulation Attenuates BOLD Adaptation and Increases Functional Connectivity.” Journal of Neurophysiology 123, no. 1: 428–438.
Keeser, D., T. Meindl, J. Bor, et al. 2011. “Prefrontal Transcranial Direct Current Stimulation Changes Connectivity of Resting‐State Networks During fMRI.” Journal of Neuroscience 31, no. 43: 15284–15293.
Kelly, A. C., L. Q. Uddin, B. B. Biswal, F. X. Castellanos, and M. P. Milham. 2008. “Competition Between Functional Brain Networks Mediates Behavioral Variability.” NeuroImage 39, no. 1: 527–537.
Kim, T., J. C. Salazar Fajardo, H. Jang, et al. 2023. “Effect of Optimized Transcranial Direct Current Stimulation on Motor Cortex Activation in Patients With sub‐Acute or Chronic Stroke: A Study Protocol for a Single‐Blinded Cross‐Over Randomized Control Trial.” Frontiers in Neuroscience 17: 1328727.
Laakso, I., M. Mikkonen, S. Koyama, A. Hirata, and S. Tanaka. 2019. “Can Electric Fields Explain Inter‐Individual Variability in Transcranial Direct Current Stimulation of the Motor Cortex?” Scientific Reports 9, no. 1: 626.
Laakso, I., S. Tanaka, M. Mikkonen, S. Koyama, N. Sadato, and A. Hirata. 2016. “Electric Fields of Motor and Frontal tDCS in a Standard Brain Space: A Computer Simulation Study.” NeuroImage 137: 140–151.
Lang, S., L. S. Gan, C. McLennan, A. Kirton, O. Monchi, and J. J. P. Kelly. 2020. “Preoperative Transcranial Direct Current Stimulation in Glioma Patients: A Proof of Concept Pilot Study.” Frontiers in Neurology 11: 593950.
Lefaucheur, J. P., A. Antal, S. S. Ayache, et al. 2017. “Evidence‐Based Guidelines on the Therapeutic Use of Transcranial Direct Current Stimulation (tDCS).” Clinical Neurophysiology 128, no. 1: 56–92.
Liang, B., D. Zhang, X. Wen, et al. 2014. “Brain Spontaneous Fluctuations in Sensorimotor Regions Were Directly Related to Eyes Open and Eyes Closed: Evidences From a Machine Learning Approach.” Frontiers in Human Neuroscience 8: 645.
Liu, D., Z. Dong, X. Zuo, J. Wang, and Y. Zang. 2013. “Eyes‐Open/Eyes‐Closed Dataset Sharing for Reproducibility Evaluation of Resting State fMRI Data Analysis Methods.” Neuroinformatics 11, no. 4: 469–476.
Lopez‐Alonso, V., B. Cheeran, D. Río‐Rodríguez, and M. Fernández‐del‐Olmo. 2014. “Inter‐Individual Variability in Response to Non‐invasive Brain Stimulation Paradigms.” Brain Stimulation 7, no. 3: 372–380.
MacDonald, A. W., 3rd, J. D. Cohen, V. A. Stenger, and C. S. Carter. 2000. “Dissociating the Role of the Dorsolateral Prefrontal and Anterior Cingulate Cortex in Cognitive Control.” Science 288, no. 5472: 1835–1838.
Madhavan, R., S. E. Joel, R. Mullick, et al. 2019. “Longitudinal Resting State Functional Connectivity Predicts Clinical Outcome in Mild Traumatic Brain Injury.” Journal of Neurotrauma 36, no. 5: 650–660.
Marchitelli, R., M. Aiello, A. Cachia, et al. 2018. “Simultaneous Resting‐State FDG‐PET/fMRI in Alzheimer Disease: Relationship Between Glucose Metabolism and Intrinsic Activity.” NeuroImage 176: 246–258.
Mosayebi‐Samani, M., A. Jamil, R. Salvador, G. Ruffini, J. Haueisen, and M. A. Nitsche. 2021. “The Impact of Individual Electrical Fields and Anatomical Factors on the Neurophysiological Outcomes of tDCS: A TMS‐MEP and MRI Study.” Brain Stimulation 14, no. 2: 316–326.
Mueller, S., D. Wang, M. D. Fox, et al. 2013. “Individual Variability in Functional Connectivity Architecture of the Human Brain.” Neuron 77, no. 3: 586–595.
Mylius, V., S. S. Ayache, R. Ahdab, et al. 2013. “Definition of DLPFC and M1 According to Anatomical Landmarks for Navigated Brain Stimulation: Inter‐Rater Reliability, Accuracy, and Influence of Gender and Age.” NeuroImage 78: 224–232.
Nitsche, M. A., and W. Paulus. 2000. “Excitability Changes Induced in the Human Motor Cortex by Weak Transcranial Direct Current Stimulation.” Journal of Physiology 527, no. Pt 3: 633–639.
Oldfield, R. C. 1971. “The Assessment and Analysis of Handedness: The Edinburgh Inventory.” Neuropsychologia 9, no. 1: 97–113.
Opitz, A., W. Paulus, S. Will, A. Antunes, and A. Thielscher. 2015. “Determinants of the Electric Field During Transcranial Direct Current Stimulation.” NeuroImage 109: 140–150.
Polania, R., M. A. Nitsche, and W. Paulus. 2011. “Modulating Functional Connectivity Patterns and Topological Functional Organization of the Human Brain With Transcranial Direct Current Stimulation.” Human Brain Mapping 32, no. 8: 1236–1249.
Power, J. D., K. A. Barnes, A. Z. Snyder, B. L. Schlaggar, and S. E. Petersen. 2012. “Spurious but Systematic Correlations in Functional Connectivity MRI Networks Arise From Subject Motion.” NeuroImage 59, no. 3: 2142–2154.
Pruim, R. H. R., M. Mennes, D. van Rooij, A. Llera, J. K. Buitelaar, and C. F. Beckmann. 2015. “ICA‐AROMA: A Robust ICA‐Based Strategy for Removing Motion Artifacts From fMRI Data.” NeuroImage 112: 267–277.
Rudie, J. D., J. A. Brown, D. Beck‐Pancer, et al. 2012. “Altered Functional and Structural Brain Network Organization in Autism.” Neuroimage Clinical 2: 79–94.
Seeley, W. W., V. Menon, A. F. Schatzberg, et al. 2007. “Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control.” Journal of Neuroscience 27, no. 9: 2349–2356.
Soleimani, G., R. Kupliki, M. Paulus, and H. Ekhtiari. 2023. “Dose‐Response in Modulating Brain Function With Transcranial Direct Current Stimulation: From Local to Network Levels.” PLoS Computational Biology 19, no. 10: e1011572.
Steinmann, I., K. A. Williams, M. Wilke, and A. Antal. 2022. “Detection of Transcranial Alternating Current Stimulation Aftereffects Is Improved by Considering the Individual Electric Field Strength and Self‐Rated Sleepiness.” Frontiers in Neuroscience 16: 870758.
Tailby, C., R. A. J. Masterton, J. Y. Huang, G. D. Jackson, and D. F. Abbott. 2015. “Resting State Functional Connectivity Changes Induced by Prior Brain State Are Not Network Specific.” NeuroImage 106: 428–440.
Vergallito, A., S. Feroldi, A. Pisoni, and L. J. Romero Lauro. 2022. “Inter‐Individual Variability in tDCS Effects: A Narrative Review on the Contribution of Stable, Variable, and Contextual Factors.” Brain Sciences 12, no. 5: 522.
Wang, L., W. Dai, Y. Su, et al. 2012. “Amplitude of Low‐Frequency Oscillations in First‐Episode, Treatment‐Naive Patients With Major Depressive Disorder: A Resting‐State Functional MRI Study.” PLoS One 7, no. 10: e48658.
Wei, J., T. Chen, C. Li, G. Liu, J. Qiu, and D. Wei. 2018. “Eyes‐Open and Eyes‐Closed Resting States With Opposite Brain Activity in Sensorimotor and Occipital Regions: Multidimensional Evidences From Machine Learning Perspective.” Frontiers in Human Neuroscience 12: 422.
Xu, Y., C. Zhuo, W. Qin, J. Zhu, and C. Yu. 2015. “Altered Spontaneous Brain Activity in Schizophrenia: A Meta‐Analysis and a Large‐Sample Study.” BioMed Research International 2015: 1–11.
Yoo, Y. J., H. J. Park, T. Y. Kim, et al. 2022. “MRI‐Based Personalized Transcranial Direct Current Stimulation to Enhance the Upper Limb Function in Patients With Stroke: Study Protocol for a Double‐Blind Randomized Controlled Trial.” Brain Sciences 12, no. 12: 1673.
Yuan, K., C. H. E. Ti, X. Wang, et al. 2023. “Individual Electric Field Predicts Functional Connectivity Changes After Anodal Transcranial Direct‐Current Stimulation in Chronic Stroke.” Neuroscience Research 186: 21–32.
Zhou, M., X. Hu, L. Lu, et al. 2017. “Intrinsic Cerebral Activity at Resting State in Adults With Major Depressive Disorder: A Meta‐Analysis.” Progress in Neuro‐Psychopharmacology and Biological Psychiatry 75: 157–164.
Zou, Q. H., C. Z. Zhu, Y. Yang, et al. 2008. “An Improved Approach to Detection of Amplitude of Low‐Frequency Fluctuation (ALFF) for Resting‐State fMRI: Fractional ALFF.” Journal of Neuroscience Methods 172, no. 1: 137–141.

Keywords: electric field magnitude; fractional amplitude of low‐frequency fluctuations; functional magnetic resonance imaging; inter‐individual variability; modeling; transcranial direct current stimulation

Date Created: 20240903 Date Completed: 20240903 Latest Revision: 20240903

20240903

10.1002/jnr.25378

39225477