Distinct and complementary mechanisms of oscillatory and aperiodic alpha activity in visuospatial attention

Alpha oscillations are thought to play a key role in visuospatial attention, particularly through lateralisation mechanisms. However, whether this function is driven purely by oscillatory activity or also involves aperiodic neural components remains unclear, making it difficult to develop precise theoretical models of alpha function and attention. Using EEG and concurrent TMS-EEG, this study aimed to (1) disentangle the contributions of oscillatory and aperiodic alpha activity to visuospatial attention and (2) examine their causal roles by differentially modulating aperiodic and oscillatory components. First, across four independent EEG datasets, we found that both aperiodic and oscillatory alpha activity contribute to spatial attention encoding and univariate lateralisation effects. The two signals were uncorrelated across electrodes and their combination yielded stronger lateralisation effects than either signal separately, suggesting that they may play complementary roles. Then, we used concurrent TMS-EEG to modulate the two signals. Compared to arrhythmic TMS (ar-TMS), rhythmic TMS (rh-TMS), enhanced oscillatory alpha power, especially at the stimulated area, while decreasing aperiodic alpha power across the scalp. Despite these opposing effects, rh-TMS improved visuospatial attention representation carried by both oscillatory and aperiodic alpha signals, suggesting that both signals may reflect attentional processing. Moreover, TMS-induced changes in oscillatory and aperiodic alpha decoding differentially predicted behavioural performance, with TMS-induced changes in oscillatory alpha decoding correlating with response errors and changes in aperiodic alpha decoding correlating with response speed. Together these findings reveal a functional dissociation between oscillatory and aperiodic activity in the alpha band. We suggest a dual mechanism for alpha band activity in supporting visuospatial attention, where the two components have distinct but complementary roles. Oscillatory components may primarily support attentional filtering and target prioritization, while aperiodic components may reflect overall neural excitability and cognitive efficiency. Both of these mechanisms contribute to successful visuospatial attention.