Frontal theta phase modulates asymmetric posterior neural mechanisms of spatial attention

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.