Frontal theta phase modulates asymmetric posterior neural mechanisms of spatial attention

Darrell, Megan; Vanneau, Theo; Brittenham, Chloe; Foxe, John J.; Molholm, Sophie · 2026 · Crossref

DOI: 10.64898/2026.03.25.714015

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Summary

This study investigates how intrinsic frontal theta rhythms organize spatial attention in humans, specifically addressing whether these neural control mechanisms operate symmetrically across left and right visual fields. While the rhythmic theory of attention posits that theta-band oscillations (3–7 Hz) govern top-down sampling and gating, prior research has largely relied on non-human primate data or external perturbations, leaving the role of intrinsic, ongoing theta dynamics in humans poorly understood. Furthermore, despite behavioral evidence for a leftward attentional bias (pseudoneglect), it remains unclear if the underlying oscillatory architectures differ by direction. The authors aimed to characterize these direction-specific control dynamics and their developmental emergence in typically developing children and adolescents. The researchers recorded electroencephalography (EEG) and pupillometry from 21 participants (mean age 14.7 years) performing a covert spatial attention task. Participants attended to either the left or right visual hemifield while detecting targets amidst social (faces) and non-social (houses) distractors. The experimental design included pure social, pure non-social, and inter-mixed stimulus contexts to assess top-down and bottom-up influences. Resting-state EEG was also collected to establish baseline oscillatory profiles. Analyses focused on trial-by-trial relationships between pre-stimulus frontal theta phase, posterior alpha/beta power, early sensory gain (indexed by P1 amplitude), and behavioral reaction times. The results revealed a fundamental asymmetry in the neural mechanisms supporting spatial attention. Behaviorally, participants responded faster during leftward attention than rightward attention. Neural data mirrored this asymmetry: leftward attention recruited anticipatory modulation of parieto-occipital alpha and beta power, whereas rightward attention did not. Mechanistically, ipsilateral fronto-central theta phase drove these effects in a direction-specific manner. During leftward attention, slower 3-Hz theta phase over the left fronto-central cortex modulated reaction times and coupled with coordinated posterior alpha activity, consistent with oscillatory sensory gating. In contrast, rightward attention relied on faster 6–7-Hz theta phase over the right fronto-central cortex, which modulated behavior by enhancing early sensory gain (P1 amplitude) without engaging coordinated alpha dynamics. Resting-state alpha power showed no hemispheric differences, indicating these effects were task-evoked rather than baseline biases. Additionally, older participants exhibited enhanced performance and larger hemispheric asymmetries, suggesting these control dynamics mature with age. These findings challenge the assumption that spatial attention relies on symmetric neural mechanisms across hemispheres. Instead, the study demonstrates that human attentional sampling is rhythmically organized but fundamentally asymmetric, with leftward and rightward attention engaging distinct theta-frequency bands and downstream oscillatory processes. This work provides the first developmental characterization of intrinsic theta-phase control in humans, highlighting that leftward attention utilizes slower theta rhythms to coordinate posterior inhibition, while rightward attention employs faster theta rhythms to modulate early sensory amplification. These insights refine models of top-down attentional control and underscore the importance of considering directional asymmetries in neurophysiological studies of spatial attention.

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