Transcranial Alternating Current Stimulation (tACS) Enhances Mental Rotation Performance during and after Stimulation

Florian H Kasten, Christoph S Herrmann, Florian H Kasten, Christoph S Herrmann

Abstract

Transcranial alternating current stimulation (tACS) has been repeatedly demonstrated to modulate endogenous brain oscillations in a frequency specific manner. Thus, it is a promising tool to uncover causal relationships between brain oscillations and behavior or perception. While tACS has been shown to elicit a physiological aftereffect for up to 70 min, it remains unclear whether the effect can still be elicited if subjects perform a complex task interacting with the stimulated frequency band. In addition, it has not yet been investigated whether the aftereffect is behaviorally relevant. In the current experiment, participants performed a Shepard-like mental rotation task for 80 min. After 10 min of baseline measurement, participants received either 20 min of tACS at their individual alpha frequency (IAF) or sham stimulation (30 s tACS in the beginning of the stimulation period). Afterwards another 50 min of post-stimulation EEG were recorded. Task performance and EEG were acquired during the whole experiment. While there were no effects of tACS on reaction times or event-related-potentials (ERPs), results revealed an increase in mental rotation performance in the stimulation group as compared to sham both during and after stimulation. This was accompanied by increased ongoing alpha power and coherence as well as event-related-desynchronization (ERD) in the alpha band in the stimulation group. The current study demonstrates a behavioral and physiological aftereffect of tACS in parallel. This indicates that it is possible to elicit aftereffects of tACS during tasks interacting with the alpha band. Therefore, the tACS aftereffect is suitable to achieve an experimental manipulation.

Keywords: EEG; aftereffect; alpha oscillations; event-related-desynchronization (ERD); mental rotation; transcranial alternating current stimulation (tACS); transcranial electrical stimulation (TES).

Figures

Figure 1
Figure 1
Experimental Design. (A) Time-course of the experiment. In the beginning, 90 s of eyes-closed EEG was recorded to determine participants individual alpha frequency (IAF). Afterwards, tACS intensity was adjusted to participants’ sensation threshold before the actual experiment started. First, 10 min of baseline measurement were acquired. During the whole experiment participants performed a mental rotation task intermitted by 1 min resting EEG every 24 trials (4 min, red box, blue indicates mental rotation period, gray resting EEG). During resting EEG, participants performed a visual vigilance task. Each block consisted of two mental rotation and two resting periods. The baseline measurement was followed by 20 min of tACS or sham stimulation and 50 min of post-stimulation EEG. (B) Electrode setup. tACS electrodes (black) were positioned centered above Cz and Oz. EEG was measured from 23 positions following the international 10–10 system with electrode sites above or close to tACS electrodes left blank. (C) Mental rotation task. Each trial started with the presentation of a white fixation cross at the center of the screen. After 3000 ms the mental rotation stimulus display (taken from Ganis and Kievit, 2015) appeared and remained on screen for another 7000 ms. During this time, participants were asked to judge whether the two presented figures were identical (but rotated) or different. The first display contains an example for a target differing from the cue, the second for a target similar to the cue.
Figure 2
Figure 2
Behavioral Results. Top row: overall performance increase of the mental rotation task for (A)stimulation and sham group and (B)male and female subjects. Asterisks depicts significant differences (*<0.05). Error bars depict SEM. (C) Time-course of the performance increase for stimulation and sham group. Gray background indicates blocks during which tACS or sham stimulation was applied. Bottom row: overall change in reaction times for (D)stimulation and sham group and (E) male and female subjects. (F) Time-course of reaction time changes for stimulation and sham group. Gray background indicates blocks during which tACS or sham stimulation was applied. Error bars depict SEM.
Figure 3
Figure 3
Ongoing alpha power. Top row: ongoing alpha power during mental rotation. Error bars and shaded areas depict SEM; asterisks code for significant differences (*<0.05, **<0.01, ***< 0.001). (A) Averaged relative alpha power after stimulation for stimulation and sham. (B) Averaged relative alpha power after stimulation for females and males. (C) Time-course of ongoing alpha power after stimulation for stimulation and sham group. Bottom row: ongoing alpha power during rest. (D) Averaged relative alpha power after stimulation for stimulation and sham. (E) Averaged relative alpha power after stimulation for females and males. (F) Time-course of ongoing alpha power after stimulation for stimulation and sham group.
Figure 4
Figure 4
Ongoing alpha coherence. Ongoing normalized alpha coherence during mental rotation. Top row: normalized coherence between electrode P3 and P4. Error bars and shaded areas depict SEM; asterisks code for significant differences (*<0.05). (A) Averaged normalized coherence after stimulation for stimulation and sham. (B) Averaged normalized coherence after stimulation for females and males. (C) Time-course of normalized coherence after stimulation for stimulation and sham group. Bottom row: normalized coherence between electrode P7 and P8. (D) Averaged normalized coherence after stimulation for stimulation and sham. (E) Averaged normalized coherence after stimulation for females and males. (F) Time-course of normalized coherence after stimulation for stimulation and sham group.
Figure 5
Figure 5
Event-related-desynchronization (ERD). Error bars and shaded areas depict SEM; asterisks code for significant differences (*<0.05), n.s. = not significant. (A) Overall relative ERD in the individual alpha band for stimulation and sham group. (B) Overall relative ERD in the individual alpha band for female and male subjects. (C) Time-course of relative ERD after stimulation. Bottom rows show relative alpha power 3 s before (reference period; middle row) and after stimulus onset (test period; bottom row). (D) Overall relative pre-stimulus alpha power (reference period) for stimulation and sham group. (E) Scatterplot depicting the correlation between relative pre-stimulus alpha power (test period) and relative ERD. (F) Time-course of relative pre-stimulus alpha power for stimulation and sham group. (G) Overall relative post-stimulus alpha power for stimulation and sham group. (H) Scatterplot depicting the correlation between relative post-stimulus alpha power and relative ERD. (I) Time-course of relative post-stimulus alpha power for stimulation and sham group.
Figure 6
Figure 6
Event-related relative power change. Time-frequency representations (TFRs) and topographies reflecting relative change in spectral power after onset of the mental rotation stimulus with respect to baseline (3000 ms prior to stimulus onset until stimulus onset). TFRs are averaged over subjects for each block on electrode Pz. Topographies illustrate relative change in alpha power (8–12 Hz) in the time window 0–3000 ms after stimulus onset. First column displays pre-stimulation baseline. Later columns illustrate post stimulation blocks. Please note that blocks 2 and 3 were performed during stimulation and were discarded from analysis. Top rows: TFRs and topographies of the stimulation group. Bottom rows: TFRs and topographies of the sham group.
Figure 7
Figure 7
Correlations between behavioral and physiological measures. Scatterplots depicting correlations between behavioral and physiological aftereffect measures. Asterisks indicate correlations significantly differing from zero. Black bars around the dots indicate their SEM. Top row: correlation between overall performance increase and (A) relative ongoing alpha power during mental rotation, (B) relative ongoing alpha power during rest, (C) relative ERD. Bottom row: correlation between overall change in reaction times and (D) relative alpha power during mental rotation, (E) relative alpha power during rest, (F) relative ERD.
Figure 8
Figure 8
Event-related-potentials (ERPs). Grand average ERPs before (black) and after stimulation (red). Shaded areas depict SEM. (A) Averaged ERPs before vs. after stimulation for stimulation group. (B) Averaged ERPs before vs. after stimulation for female subjects. (C) Averaged ERPs before vs. after stimulation for sham group. (D) Averaged ERPs before vs. after stimulation for male subjects.

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