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. 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.

Spatial specificity of alpha oscillations in the human visual system

“…Maintenance of a cued position in the left visual hemifield was associated with a sustained contralateral posterior alpha band power decrease (Figure , right, p < .05 cluster‐based permutation test) accompanied by ipsilateral power increase ( p < .05, Figure , middle) over posterior occipital sensors. Previous analyses of this effect demonstrated that the sources were confined to early visual brain areas (Popov et al, ). These results confirm the well‐known hemispheric lateralization of alpha‐band activity and were taken as a starting point to investigate the sources of alpha‐band activity associated with the 16 different directions.…”

“…Incongruent flankers are associated with a reaction time increase and accuracy decrease (Popov et al, ). This effect can be quantified as the RT difference between incongruent and congruent conditions resulting in one behavioral measure per subject.…”

“…We suggest that decreases of alpha activity that are specific to spatial attention potentially lengthen the oscillatory duty cycle, thereby preparing the corresponding task‐relevant neural circuit for faster and accurate performance of an upcoming target. In contrast, frontal eye fields were tuned, at least to some extent, to visual field locations along the horizontal meridian (Figure ) reflecting a rather sparse representation “overseeing” the principal direction of attention potentially regulating activity in early visual areas in a top‐down fashion (Bressler, Tang, Sylvester, Shulman, & Corbetta, ; Ekstrom, Roelfsema, Arsenault, Bonmassar, & Vanduffel, ; Ekstrom, Roelfsema, Arsenault, Kolster, & Vanduffel, ; Marshall, O'Shea, Jensen, & Bergmann, ; Moore & Armstrong, ; Popov et al, ). However, it should be noted that the spatial resolution of the MEG at that area is lower as compared to visual areas such that this interpretation should be taken with caution.…”

“…Participants covertly attended a location indicated by a cue at which a subsequent target appeared in a circular array. During the delay period, attentional allocation has been shown to modulate alpha‐band activity in both human and nonhuman primates (Popov et al, ; Saalmann et al, ). In the present report, we asked to what extent the modulations of alpha‐band activity were distributed retinotopically.…”

Humans strategically shift decision bias by flexibly adjusting sensory evidence accumulation

“…Specifically, bottom-up processing of visual information has previously been linked to increased highfrequency (> 40 Hz, i.e. gamma) electrophysiological activity over visual cortex [14][15][16][17] . peer-reviewed) is the author/funder.…”