Spatiotemporal Dynamics of High-Gamma Activities during a 3-Stimulus Visual Oddball Task

Akimoto, Yoritaka; Kanno, Akitake; Kambara, Toshimune; Nozawa, Takayuki; Sugiura, Motoaki; Okumura, Eiichi; Kawashima, Ryuta · 2013 · OpenAlex-citations

DOI: 10.1371/journal.pone.0059969

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Summary

This study investigates the spatiotemporal dynamics of high-gamma (52–100 Hz) neural activities to refine the understanding of top-down and bottom-up visual attention. While functional magnetic resonance imaging (fMRI) offers high spatial resolution and event-related potentials (ERPs) provide temporal data, neither fully captures the rapid, localized neural processing underlying attentional shifts. The authors aimed to bridge this gap by using magnetoencephalography (MEG) to map high-gamma event-related synchronization (ERS) and functional connectivity during a 3-stimulus visual oddball task, which distinguishes between target stimuli requiring response and infrequent non-target stimuli that are salient but irrelevant. Fourteen healthy participants performed the task while MEG data were recorded. The experimental design involved presenting frequent standard stimuli, infrequent target stimuli, and infrequent non-target stimuli. Data were processed using dual-state adaptive spatial filtering to enhance high-frequency source reconstruction and imaginary coherence analysis to assess functional connectivity while minimizing volume conduction artifacts. Regions of interest were identified in the left middle frontal gyrus (MFG), left intraparietal sulcus (IPS), left thalamus, and visual areas. The analysis focused on high-gamma power changes and coherence between these regions across specific time windows relative to stimulus onset. The results revealed distinct spatiotemporal patterns for target and non-target processing. High-gamma ERS was observed in the left MFG, left IPS, left thalamus, and visual areas, with different timing for each condition. Specifically, bottom-up attention to non-targets elicited early high-gamma activity in visual areas and the left MFG (100–200 ms), whereas top-down attention to targets showed significant activity in the left MFG and thalamus starting at 200–300 ms. Functional connectivity analysis showed elevated high-gamma imaginary coherence between the left IPS and right MFG (300–400 ms) during target processing, and theta-band coherence between the left thalamus and left MFG (150–450 ms) during non-target processing. Crucially, the strength of high-gamma coherence within the attention network and high-gamma power in the left thalamus negatively correlated with individual reaction times, indicating that stronger connectivity predicted faster target detection. These findings provide source-level electrophysiological evidence that clarifies the temporal sequence of attentional processes. The study demonstrates that bottom-up attention involves rapid, transient high-gamma synchronization in visual and frontal areas, while top-down attention is characterized by sustained synchronization and specific frontoparietal connectivity. Furthermore, the link between functional connectivity strength and behavioral performance suggests that the efficiency of communication within the dorsal and ventral attention networks directly influences cognitive processing speed. This work extends previous fMRI and ERP studies by offering a refined temporal map of how the brain allocates resources for stimulus evaluation and orientation.

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• attention selective divided