Modulation of brain networks during MR-compatible transcranial direct current stimulation - PubMed (original) (raw)

Modulation of brain networks during MR-compatible transcranial direct current stimulation

Amber M Leaver et al. Neuroimage. 2022.

Abstract

Transcranial direct current stimulation (tDCS) can influence performance on behavioral tasks and improve symptoms of brain conditions. Yet, it remains unclear precisely how tDCS affects brain function and connectivity. Here, we measured changes in functional connectivity (FC) metrics in blood-oxygenation-level-dependent (BOLD) fMRI data acquired during MR-compatible tDCS in a whole-brain analysis with corrections for false discovery rate. Volunteers (n = 64) received active tDCS, sham tDCS, and rest (no stimulation), using one of three previously established electrode tDCS montages targeting left dorsolateral prefrontal cortex (DLPFC, n = 37), lateral temporoparietal area (LTA, n = 16), or superior temporal cortex (STC, n = 11). In brain networks where simulated E field was highest in each montage, connectivity with remote nodes decreased during active tDCS. During active DLPFC-tDCS, connectivity decreased between a fronto-parietal network and subgenual ACC, while during LTA-tDCS connectivity decreased between an auditory-somatomotor network and frontal operculum. Active DLPFC-tDCS was also associated with increased connectivity within an orbitofrontal network overlapping subgenual ACC. Irrespective of montage, FC metrics increased in sensorimotor and attention regions during both active and sham tDCS, which may reflect the cognitive-perceptual demands of tDCS. Taken together, these results indicate that tDCS may have both intended and unintended effects on ongoing brain activity, stressing the importance of including sham, stimulation-absent, and active comparators in basic science and clinical trials of tDCS.

Keywords: Functional connectivity; Transcranial direct current stimulation; fMRI.

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Conflict of interest statement

Declaration of Competing Interest All authors declare no conflicts of interest.

Figures

Fig. 1.

Electrode positions and resting state networks (RSNs) used in the current study. A. Electrode positions (“montages”) are displayed on the reconstructed surface of a template head, including DLPFC (dorsolateral prefrontal cortex), LTA (lateral temporoparietal area), and STC (superior temporal cortex). Anode is displayed in yellow and cathode in blue. 10–10 EEG positions are also displayed for each montage; green dots mark the visible 10–10 EEG grid. B. Resting state network (RSN) atlas is displayed, as derived from the 17-network template in Yeo et al. 2011. Each network is given a color as indicated by the key at bottom and is displayed on reconstructed cortical surfaces (from top to bottom: lateral, medial, dorsal, ventral). Gray outlines also indicate nodes used in the current analyses, derived from the 400-parcel template from Schaeffer et al. 2018.

Fig. 2.

Increased fALFF and ReHo during active and sham tDCS in sensory and motor regions. A. Significant main effects of tDCS condition (“Main Cond.”) were apparent in regional FC metrics fALFF and ReHo in nodes overlapping sensory and motor cortex (p(fdr)<0.05). B. In pairwise contrasts of tDCS conditions (active/sham/rest) in these nodes, regional fALFF and ReHo during both active and sham tDCS was greater than for the rest condition in most nodes (_p_<0.05). From left to right, the cortical surface views in A and B are: left and right lateral, superior temporal plane insets (left on top), left and right medial, and dorsal (left on bottom) surfaces. No significant effects were apparent for contrasts not shown (i.e., Rest > Active, Rest > Sham, Active > Sham). C. Mean fALFF is plotted for representative nodes marked with asterisks in A, including primary visual, auditory, and somatosensory cortex (PVC, PAC, PSC, respectively), as well as posterior cingulate cortex (PCC). Black whiskered error bars reflect standard error of the mean, and thick gray reflect 95% confidence intervals (within subjects). Individual datapoints are also plotted in color to reflect tDCS montage (red DLPFC, green LTA, blue STC). Double asterisks on plots mark p(fdr)<0.05 from the main analysis; single asterisks mark pairwise contrasts p<0.05; daggers mark pairwise contrasts p<0.10.

Fig. 3.

High E field nodes and networks. A. E field magnitude is plotted for each node on template cortical surfaces for each electrode montage. White asterisks mark the locations of the five nodes with greatest E field magnitude (i.e., ∣E∣ in V/m) for each montage, estimated using a single template head. B. Resting state networks (RSNs) that contain one or more of the top five nodes identified in A are displayed for each montage. **Note that the “Superior Temporal Sulcus” network was also a high E field network for the LTA (CP5/TP8) montage. Numbers given in the color keys at bottom match the RSN numbers displayed in Fig. 1B and Yeo et al. 2011 indices. In A and B, cortical surfaces are lateral, medial, and ventral displayed from top to bottom.

Fig. 4.

Active tDCS influences connectivity in high E field networks. A. Mean functional connectivity (Global FC) increased within a high E field network during active DLPFC-tDCS compared with sham. Cortical surface views are left and right medial (top row) and left and right ventral (bottom row). B. Mean global FC for the Orbitofrontal Network is plotted for each montage and condition; black whiskered error bars reflect standard error of the mean, and thick gray bars reflect 95% confidence intervals (within subjects). Individual datapoints are plotted in color to reflect tDCS montage (red DLPFC, green LTA, blue STC). Double asterisks on plots mark p(fdr)<0.05 from the main analysis; single asterisks mark pairwise contrasts p<0.05; daggers mark pairwise contrasts p<0.10. C. FC decreased between specific nodes and networks with high E field magnitude during active DLPFC-tDCS (red) and active LTA-tDCS (green). High E field networks are displayed in boxes, nodes are displayed in patches on cortical surfaces, and arrowed lines connect node-network pairs exhibiting significant differences in FC between active and sham conditions for a given montage of interest. D. FC is plotted for each node-network connection in C (numbered 1–4) using the same conventions as in B. RSN and Node numbers reflect indices from Yeo et al. 2011 and Schaeffer et al. 2017, respectively. RSN FC metrics plotted in B and D are beta (parameter) estimates from FSL dual regression.

Fig. 5.

Ratings of tDCS discomfort and intensity associate with functional connectivity (FC) metrics during active and sham conditions. A. Patches on cortical surfaces mark nodes where FC metrics showed linear relationships with participant ratings of tDCS-related discomfort (salmon) and intensity (yellow), respectively (10-pt scale). B. FC (y axis) is plotted for tDCS-related discomfort and intensity (x axes) for the nodes identified in A. Open circles reflect data for active and sham conditions in each participant with color indicating montage. Linear regression and fit lines are plotted in black and gray, respectively. RSN and Node numbers reflect indices from Yeo et al. 2011 and Schaeffer et al. 2017, respectively. RSN6 FC metrics plotted in B are beta (parameter) estimates from FSL dual regression.

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Modulation of brain networks during MR-compatible transcranial direct current stimulation - PubMed (original) (raw)