Frontal theta phase modulates asymmetric posterior neural mechanisms of spatial attention

Abstract

Selective attention enables prioritization of behaviorally relevant information through coordinated control of neural excitability. Although theta-band (3-7 Hz) rhythms are implicated in top-down attentional sampling in non-human primates, how intrinsic theta phase organizes sensory gain and behavior in humans, and whether this control operates symmetrically across hemispheres, remains unknown. We recorded electroencephalography (EEG) and pupillometry in typically developing human participants (n = 21; 14.7 {+/-} 3.8 YO) performing a covert spatial attention task. Behaviorally, participants responded faster during leftward relative to rightward attention. This behavioral asymmetry was paralleled in the neural data: anticipatory modulation of parieto-occipital alpha and beta power emerged selectively during leftward attention, whereas rightward attention did not recruit comparable posterior oscillatory processes. Mechanistically, ipsilateral fronto-central theta phase emerged as a potential driver of this asymmetry. Intrinsic theta phase predicted trial-by-trial reaction time (RT) in a cue-direction-specific manner. During leftward attention, 3-Hz theta-phase over left fronto-central cortex modulated behavior and was significantly coupled to coordinated posterior alpha-band activity. In contrast, 6-7-Hz theta-phase over right fronto-central cortex modulated behavior during rightward attention but showed no relationship with alpha or beta modulation; instead, it modulated early sensory gain, indexed by P1 amplitude. Consistent with these distinct architectures, RT was jointly predicted by lower pre-stimulus alpha power and higher P1 amplitude over the attended hemisphere during leftward attention, whereas only P1 amplitude predicted performance during rightward attention. Resting-state alpha power did not differ across hemispheres, indicating that these effects were task-evoked rather than baseline spectral differences. Critically, older participants, who demonstrated enhanced behavioral performance, also exhibited a larger hemispheric asymmetry. Together, these findings reveal developmentally emerging, direction-specific neural control dynamics underlying human spatial attention. Significance StatementSpatial attention is often assumed to rely on symmetric neural mechanisms across left and right space. Using EEG in typically developing children and adolescents, we show that intrinsic theta rhythms organize attention through direction-specific control architectures. Leftward attention engages slower frontal theta (3-Hz) that coordinates posterior alpha and beta activity, consistent with oscillatory sensory gating. Rightward attention instead relies on faster theta (6-7-Hz) that modulates early sensory responses without coordinated alpha dynamics. These asymmetric mechanisms occur despite lack of hemispheric differences in resting alpha activity, indicating that they emerge during active control rather than reflecting baseline biases. These findings reveal that human attentional sampling is rhythmically organized but fundamentally asymmetric across space.