FEF-Controlled Alpha Delay Activity Precedes Stimulus-Induced Gamma-Band Activity in Visual Cortex

Abstract

Recent findings in the visual system of nonhuman primates have demonstrated an important role of gamma-band activity (40-100 Hz) in the feedforward flow of sensory information, whereas feedback control appears to be established dynamically by oscillations in the alpha (8-13 Hz) and beta (13-18 Hz) bands (van Kerkoerle et al., 2014; Bastos et al., 2015). It is not clear, however, how alpha oscillations are controlled and how they interact with the flow of visual information mediated by gamma-band activity. Using noninvasive human MEG recordings in subjects performing a visuospatial attention task, we show that fluctuations in alpha power during a delay period in a spatial attention task preceded subsequent stimulus-driven gamma-band activity. Importantly, these interactions correlated with behavioral performance. Using Granger analysis, we further show that the right frontal-eye field (rFEF) exerted feedback control of the visual alpha oscillations. Our findings suggest that alpha oscillations controlled by the FEF route cortical information flow by modulating gamma-band activity.SIGNIFICANCE STATEMENT Visual perception relies on a feedforward flow of information from sensory regions, which is modulated by a feedback drive. We have identified the neuronal dynamics supporting integration of the feedforward and feedback information. Alpha oscillations in early visual regions reflect feedback control when spatial attention is allocated and this control is exercised by the right frontal eye field. Importantly, the alpha-band activity predicted both performance and activity in the gamma band. In particular, gamma activity was modulated by the phase of the alpha oscillations. These findings provide novel insight into how the brain operates as a network and suggest that the integration of feedforward and feedback information is implemented by cross-frequency interactions between slow and fast neuronal oscillations.