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, 2019, 7051079
eCollection

EEG Alpha Power Is Modulated by Attentional Changes During Cognitive Tasks and Virtual Reality Immersion

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EEG Alpha Power Is Modulated by Attentional Changes During Cognitive Tasks and Virtual Reality Immersion

Elisa Magosso et al. Comput Intell Neurosci.

Abstract

Variations in alpha rhythm have a significant role in perception and attention. Recently, alpha decrease has been associated with externally directed attention, especially in the visual domain, whereas alpha increase has been related to internal processing such as mental arithmetic. However, the role of alpha oscillations and how the different components of a task (processing of external stimuli, internal manipulation/representation, and task demand) interact to affect alpha power are still unclear. Here, we investigate how alpha power is differently modulated by attentional tasks depending both on task difficulty (less/more demanding task) and direction of attention (internal/external). To this aim, we designed two experiments that differently manipulated these aspects. Experiment 1, outside Virtual Reality (VR), involved two tasks both requiring internal and external attentional components (intake of visual items for their internal manipulation) but with different internal task demands (arithmetic vs. reading). Experiment 2 took advantage of the VR (mimicking an aircraft cabin interior) to manipulate attention direction: it included a condition of VR immersion only, characterized by visual external attention, and a condition of a purely mental arithmetic task during VR immersion, requiring neglect of sensory stimuli. Results show that: (1) In line with previous studies, visual external attention caused a significant alpha decrease, especially in parieto-occipital regions; (2) Alpha decrease was significantly larger during the more demanding arithmetic task, when the task was driven by external visual stimuli; (3) Alpha dramatically increased during the purely mental task in VR immersion, whereby the external stimuli had no relation with the task. Our results suggest that alpha power is crucial to isolate a subject from the environment, and move attention from external to internal cues. Moreover, they emphasize that the emerging use of VR associated with EEG may have important implications to study brain rhythms and support the design of artificial systems.

Figures

Figure 1
Figure 1
(a) Timeline of Experiment 1. The experiment included two sessions, i.e., an arithmetic session and a reading numbers session, separated by a 10 min break, performed by all participants. Each session lasted fifteen minutes and included an initial (r1) 5-minute relaxation phase, a final (r2) 5-minute relaxation phase, and a central 5-minute task phase (T) consisting in an arithmetic task (arithmetic session) or a reading numbers task (reading numbers session). The order of the tasks was counterbalanced across the participants. (b) Design of each session. In both sessions, the relaxation phases (r1 and r2) consisted in the presentation of a gray screen with the world “relax.” In the arithmetic session, during the task phase, the participant had to provide the response to the arithmetic operation (by selecting one of the black button-items with the mouse); after the response selection, a new screen with a new operation appeared. In the reading numbers session, during the task phase, the participant had just to mentally read the numbers appearing on the screen (e.g., 300, 0, 3, 8,…), and the screen updated every 5 seconds.
Figure 2
Figure 2
(a) CAD model processed in IC.IDO (Industrial Grade Immersive VR Solutions) Software creating the digital mock-up of the entire cabin with the proper color, material, and finishing properties of each surface. (b, c) The two different configurations of the cabin interior, namely, configuration B1 (b) and B2 (c), characterized by different color, material, and finishing properties, when projected on the CAVE screens. (d) Example of the avatar within the cabin virtual environment. (e) Timeline of Experiment 2. The experiment included two sessions corresponding to the cabin configurations B1 and B2. The order of the presentation of the two configurations was counterbalanced across participants. All participants executed the phases r1 (relaxation without VR), r1VR (first static immersion in the VR), intVR (interactive exploration of VR), and r2VR (second static immersion in the VR) in both sessions. Only a subset of participants (24 out of 41) executed an additional phase in the second session (phase maVR), consisting in performing a mental arithmetic task (mental serial subtractions) while immersed in the VR.
Figure 3
Figure 3
Scalp maps of alpha power (μV2) averaged across all participants in Experiment 1, as a function of the experimental session (arithmetic session: first row; reading numbers session: second row) and of the phase within the session (relaxation pretask r1: first column; task T: second column; relaxation posttask r2: third column). Each scalp map was obtained via the EEGLAB Matlab Toolbox, by color coding the average alpha power value at each electrode position in a 2D circular view (top view of the head, nose at the top) and using interpolation on a fine 67 × 67 grid. (a) Arithmetic session (r1 phase). (b) Arithmetic session (T phase). (c) Arithmetic session (r2 phase). (d) Reading numbers session (r1 phase). (e) Reading numbers session (T phase). (f) Reading numbers session (r2 phase).
Figure 4
Figure 4
Normalized alpha power, averaged across participants (mean ± sem), at each single electrode in Experiment 1, distinguishing between session (arithmetic session: red lines; reading numbers session: blue lines) and phase (phase T: continuous lines; phase r2: dotted lines). Value 1 represents the pretask reference value (at phase r1) for each electrode; thus, values below 1 indicate alpha power decrease (desynchronization) while values above 1 indicate alpha power increase (synchronization) compared to the pretask phase, at single-channel level.
Figure 5
Figure 5
Normalized alpha power, averaged across participants (mean ± sem), over the two scalp regions (front-central-temporal FCT (a); parietal-occipital PO (b)) at each of the three phases (r1, T, and r2) of the arithmetic session and of the reading numbers session. Asterisks denote the results of multiple one-sample t-tests comparing the normalized alpha power in the phases T and r2 of each session with the reference value (1), separately within each region (significance cut-off = 0.05/4 = 0.0125). In both regions, significant deviation from the reference value was found during the task phases T (p < 0.0001 for both arithmetic and reading numbers) but not during the r2 phases (FCT: p=0.082 arithmetic; p=0.195 reading numbers; PO: p=0.07 arithmetic; p=0.25 reading numbers) (a) Normalized alpha power-FCT. (b) Normalized alpha power-PO.
Figure 6
Figure 6
Normalized alpha power, averaged across participants (mean ± sem) and aggregated across the two sessions, at each single electrode in Experiment 2, during the two examined phases of purely VR immersion (r1VR and r2VR).
Figure 7
Figure 7
Power Spectrum Density (PSD) over each scalp region (front-central-temporal FCT (a); parietal-occipital PO (b)) computed separately for each phase r1, r1Vr, and r2VR, averaged across participants and across the two sessions (a) PSD-FCT. (b) PSD-PO.
Figure 8
Figure 8
Normalized alpha power, averaged across participants (mean ± sem), over the two scalp regions (front-central-temporal FCT (a); parietal-occipital PO (b)) at each of the three phases (r1, r1VR, and r2VR) of the VR sessions. Asterisks denote the results of multiple one-sample t-tests comparing the normalized α powers in the phases r1VR and r2VR with the reference value (1), separately within each regions (significance cut-off = 0.05/2 = 0.025). In both regions, significant deviation from the reference value was found both in r1VR and r2VR (∗∗∗p < 0.0001; p=0.0096). (a) Normalized alpha power-FCT. (b) Normalized alpha power-PO.
Figure 9
Figure 9
Temporal pattern, at 1-minute resolution, of the normalized alpha power (mean ± sem across participants) throughout the first ten minutes of the VR sessions, plotted separately for each scalp region (front-central-temporal FCT (a); parietal-occipital PO (b)). The examined ten minutes included the r1 phase from minute 1 to minute 5 and the r1VR phase from minute 6 to minute 10. For each region, the α power at each minute was normalized with respect to the value obtained at minute 1 (i.e., the first minute of phase r1). Symbols above each point denote the results of multiple one-sample t-tests comparing the normalized α power at each minute (from 2 to 10) with the reference value (1), separately within each region (significance cut-off = 0.05/9 = 0.0056). Symbols ∗ denote points that satisfied the uncorrected significance threshold (0.05), while symbols § denote points that survived the severe Bonferroni correction (0.05/9). Uncorrected p values at each point (subscript indicate the minute at which the p value refer to) are p2=0.015, p3=0.01, p4=0.159, p5=0.089, p6=1.5 · 10−6, p7=0.004, p8=0.003; p9=0.136, p10=0.006 for the FCT region; p2=0.021, p3=0.032, p4=0.036, p5=0.019, p6=4 · 10−7, p7=5 · 10−5, p8=0.004; p9=6 · 10−4, p10=0.011 for the PO region. (a) Normalized alpha power-FCT. (b) Normalized alpha power-PO.
Figure 10
Figure 10
Normalized alpha power, averaged across the subset of 24 participants (mean ± sem), over the two scalp regions (front-central-temporal FCT (a); parietal-occipital PO (b)) in the four phases of the second session (r1, r1VR, r2VR, and maVR). Asterisks denote the results of multiple one-sample t-tests comparing the normalized α power in the phases r1VR, r2VR, and maVR with the reference value (1), separately within each region (significance threshold = 0.05/3 = 0.0167). In both regions, significant deviation from the reference value was found in r1VR and r2VR (FCT: ∗∗p=0.0004 in r1VR, ∗∗p=0.001 in r2VR; PO: ∗∗∗p < 0.0001 in r1VR and r2VR), but not in maVR (FCT: p=0.71; PO: p=0.9). (a) Normalized alpha power-FCT. (b) Normalized alpha power-PO.

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