High-definition transcranial direct current stimulation of the occipital cortices induces polarity dependent effects within the brain regions serving attentional reorientation

Abstract

Numerous brain stimulation studies have targeted the posterior parietal cortex, a key hub of the attention network, to manipulate attentional reorientation. However, the impact of stimulating brain regions earlier in the pathway, including early visual regions, is poorly understood. In this study, 28 healthy adults underwent three high-definition transcranial direct current stimulation (HD-tDCS) visits (i.e., anodal, cathodal, and sham). During each visit, they completed 20 min of occipital HD-tDCS and then a modified Posner task during magnetoencephalography (MEG). MEG data were transformed into the time-frequency domain and significant oscillatory events were imaged using a beamformer. Oscillatory response amplitude values were extracted from peak voxels in the whole-brain maps and were statistically compared. Behaviorally, we found that the participants responded slowly when attention reallocation was needed (i.e., the validity effect), irrespective of the stimulation condition. Our neural findings indicated that cathodal HD-tDCS was associated with significantly reduced theta validity effects in the occipital cortices, as well as reduced alpha validity effects in the left occipital and parietal cortices relative to anodal HD-tDCS. Additionally, anodal occipital stimulation significantly increased gamma amplitude in right occipital regions relative to cathodal and sham stimulation. Finally, we also found a negative correlation between the alpha validity effect and reaction time following anodal stimulation. Our findings suggest that HD-tDCS of the occipital cortices has a polarity dependent impact on the multispectral neural oscillations serving attentional reorientation in healthy adults, and that such effects may reflect altered local GABA concentrations in the neural circuitry serving attentional reorientation.

Keywords: Posner; alpha; gamma; magnetoencephalography; oscillations; validity.

FIGURE 1

Two‐dimensional montage showing placement of HD‐tDCS electrodes. The central electrode was placed on Oz, which corresponds to the calcarine fissure based on an extension of the Okamoto et al. transformations of the scalp‐based international 10/20 system into MNI space and was surrounded on the superior and lateral sides by electrodes of opposite polarity near the parieto‐occipital junction (i.e., PO₃, PO₄, PO_7, and PO₈)

FIGURE 2

Study setup and behavioral performance: Participants received 20 min of anodal, cathodal, and sham HD‐tDCS over the occipital region (Oz). Stimulation conditions were pseudorandomized across three visits, each separated by at least 1 week. (Left) Current distribution modeling using our HD‐tDCS montage revealed focal stimulation of the occipital region. (Middle) About 1 hr after HD‐tDCS, participants completed a modified Posner paradigm during MEG recording. Briefly a fixation cross was presented for 1,500 ms (±250 ms), followed by a cue (green bar‐enhanced in the figure for better visualization) presented in the left or right visual hemifield for 100 ms. The target stimulus (box with opening) appeared 200 ms after cue offset in either the left or right visual hemifield, for 1,200 ms. Participants responded as to whether the opening was on the top or bottom of the target. The cue was presented on the same side as the target (i.e., valid condition) in half of the trials. A delay period was incorporated between HD‐tDCS and MEG recording to optimize offline effects; thus, the total time (i.e., from the beginning of stimulation to the end of the MEG task) took approximately 94 min. (Right) Performance of the task showed significant validity effects across all stimulation montages, such that participants responded more slowly to invalid compared to valid trials (p < .001)

FIGURE 3

Neural responses to the modified Posner paradigm. (Left): Grand averaged time‐frequency spectrograms of MEG sensors exhibiting one or more significant responses, with gamma activity at the top, beta and alpha below, and theta at the bottom. In each spectrogram, time (ms) is denoted on the x‐axis and frequency (Hz) is shown on the y‐axis. All signal power data are expressed as percent difference from baseline, with color legends shown on the right of the spectrograms. Dashed rectangles indicate the time‐frequency windows that were subjected to beamforming. (Right): Grand‐averaged beamformer images (pseudo‐t) across all participants, conditions, and HD‐tDCS montages for each time‐frequency component, with theta at the bottom, alpha/beta in the middle, and gamma at the top. Separate color scale bars are shown for each

FIGURE 4

HD‐tDCS polarity dependent modulation of the theta validity effect during attentional reorientation. Response amplitude values (pseudo‐t) were extracted from peak voxels and subjected to a 2 × 3 ANOVA. A significant condition by montage interaction was found in the theta range in right occipital cortices, such that the theta validity effect was significantly weaker in this region following cathodal stimulation compared to both anodal and sham conditions. Box and whisker plot shows the right occipital theta validity in anodal, cathodal, and sham stimulation. Asterisk in the image to the upper right indicates the relevant region. *p < .05, ** p = .005

FIGURE 5

HD‐tDCS polarity dependent modulation of the alpha validity effect during attentional reorientation. Response amplitude values (pseudo‐t) were extracted from peak voxels and subjected to a 2 × 3 ANOVA. A significant stimulation montage by condition interaction was found in the alpha range and follow‐up testing indicated that the alpha validity effect was significantly weaker in the (a) left occipital and (b) left parietal following cathodal compared to anodal stimulation. Box and whisker plots show the individual data points, median (horizontal line), first and third quartile (box), and local minima and maxima (whiskers). Asterisks in the images above each plot indicate the relevant regions. *p < .05, ** p < .005

FIGURE 6

HD‐tDCS polarity dependent modulation of gamma oscillations during attentional reorientation. Response amplitude values (pseudo‐t) were extracted from peak voxels and subjected to a 2 × 3 ANOVA. A significant main effect of stimulation was found in the gamma range in the right occipital region, such that gamma oscillations were significantly stronger after anodal stimulation compared to the cathodal and sham conditions. Box and whisker plot shows right occipital gamma amplitude across both task conditions in anodal, cathodal, and sham conditions, and includes individual data points, median (horizontal line), first and third quartile (box), and local minima and maxima (whiskers). Asterisks in the image above each plot indicate the relevant region. *p < .05

FIGURE 7

Correlation of alpha validity effect with reaction time. Pearson correlational analysis between the alpha validity effect in left parietal regions (x‐axis; pseudo‐t) and reaction time (y‐axis) following anodal stimulation showed a negative association (p < .05). The respective line of best fit and the r value are overlaid on the plot