Visual search performance in cerebral visual impairment is associated with altered alpha band oscillations

Abstract

Individuals with cerebral visual impairment (CVI) often present with deficits related to visuospatial processing. However, the neurophysiological basis underlying these higher order perceptual dysfunctions have not been clearly identified. We assessed visual search performance using a novel virtual reality based task paired with eye tracking to simulate the exploration of a naturalistic scene (a virtual toy box). This was combined with electroencephalography (EEG) recordings and an analysis pipeline focusing on time frequency decomposition of alpha oscillatory activity. We found that individuals with CVI showed an overall impairment in visual search performance (as indexed by decreased success rate, as well as increased reaction time, visual search area, and gaze error) compared to controls with neurotypical development. Analysis of captured EEG activity following stimulus onset revealed that in the CVI group, there was a distinct lack of strong and well defined posterior alpha desynchronization; an important signal involved in the coordination of neural activity related to visual processing. Finally, an exploratory analysis revealed that in CVI, the magnitude of alpha desynchronization was associated with impaired visual search performance as well as decreased volume of specific thalamic nuclei implicated in visual processing. These results suggest that impairments in visuospatial processing related to visual search in CVI are associated with alterations in alpha band oscillations as well as early neurological injury at the level of visual thalamic nuclei.

Figure 1.. Experimental Setup.

(A) The “virtual toy box” visual search task showing a screenshot of a sample trial. On each trail, the participant was instructed to search for the target (a blue truck) surrounded by distractor toys. (B) Visual search performance was recorded using a screen mounted eye tracker (Tobii 4C Eye Tracker system). EEG recordings associated with task performance were acquired using a wireless montage (Neuroelectrics Enobio 20 channel wireless EEG recording system).

Figure 2.. Visual Search Performance.

Heat maps generated from a representative (A) control and (B) CVI participant. Note the larger spatial extent of visual search area in the CVI participant. Group comparisons of (C) success rate, (D) reaction time, (E) visual search area, and (F) gaze error. Individuals with CVI showed an overall impairment in visual search performance compared to controls on all behavioral outcomes of interest (error bars: ± SD; * = p < 0.05).

Figure 3.. Time Frequency Plots of Alpha Oscillatory Activity.

(A) Relative power signal changes shown in time frequency representations with respect to baseline averaged across the occipital channels (O₁, O_z, and O₂). Data are shown across the frequency range of 3 to 40 Hz, and for a time window of 0.3 sec pre stimulus to 1.2 sec post stimulus. Data from each group (CVI and controls) are shown separately. Dotted black line represents stimulus onset. Group differences in alpha desynchronization reveal strong and consistent levels of alpha desynchronization signal in controls that are distinctly absent in the CVI group (see region within dotted line). (B) Scalp topographies of baseline corrected alpha oscillatory activity are shown for the time windows in which group comparisons revealed the highest statistical differences (0.5 to 0.7 sec post-stimulus). Data for each group (controls and CVI) are shown separately. Group differences can be observed at the whole scalp level and in particular, across the posterior electrode locations.

Figure 4.. Alpha Oscillatory Activity and Statistical Comparisons.

(A) Cluster-based permutation statistical comparison between groups (Controls > CVI). A statistical comparison was performed within a 0 to 1 sec post-stimulus time window across the frequency range of 3 to 40 Hz and all electrodes. Significant differences are observed between groups in the alpha range. (B) Scalp topographies of the cluster-based permutation results performed between groups (statistically significant channels highlighted with a white asterisk). (C) Time course plot showing change in alpha power over time for the occipital channel cluster (O1, O2, Oz). Both group means (solid lines) and one standard deviation (shaded areas) are shown. Note the separation between the curves for the control and CVI groups that is most evident around 0.3 sec post-stimulus onset. (D) Bar plot showing group differences with respect mean and individual alpha power data.