Top-Down Control of Visual Alpha Oscillations: Sources of Control Signals and Their Mechanisms of Action

Abstract

Alpha oscillations (8-12 Hz) are thought to inversely correlate with cortical excitability. Goal-oriented modulation of alpha has been studied extensively. In visual spatial attention, alpha over the region of visual cortex corresponding to the attended location decreases, signifying increased excitability to facilitate the processing of impending stimuli. In contrast, in retention of verbal working memory, alpha over visual cortex increases, signifying decreased excitability to gate out stimulus input to protect the information held online from sensory interference. According to the prevailing model, this goal-oriented biasing of sensory cortex is effected by top-down control signals from frontal and parietal cortices. The present study tests and substantiates this hypothesis by (a) identifying the signals that mediate the top-down biasing influence, (b) examining whether the cortical areas issuing these signals are task-specific or task-independent, and (c) establishing the possible mechanism of the biasing action. High-density human EEG data were recorded in two experimental paradigms: a trial-by-trial cued visual spatial attention task and a modified Sternberg working memory task. Applying Granger causality to both sensor-level and source-level data we report the following findings. In covert visual spatial attention, the regions exerting top-down control over visual activity are lateralized to the right hemisphere, with the dipoles located at the right frontal eye field (FEF) and the right inferior frontal gyrus (IFG) being the main sources of top-down influences. During retention of verbal working memory, the regions exerting top-down control over visual activity are lateralized to the left hemisphere, with the dipoles located at the left middle frontal gyrus (MFG) being the main source of top-down influences. In both experiments, top-down influences are mediated by alpha oscillations, and the biasing effect is likely achieved via an inhibition-disinhibition mechanism.

Keywords: EEG; alpha oscillaitons; granger causality; top-down control; visual spatial attention; working memory.

Figure 1

The two experimental paradigms. (A) Timeline of the visual spatial attention task (Experiment 1). Depicted is a valid trial where the imperative stimulus appeared on the attended side. (B) Timeline of the modified Sternberg task (Experiment 2). Depicted is a trial where the memory load is 5 and the probe digit belongs to the cue digit set.

Figure 2

Regional dipole sources used to convert sensor-level data to source-level data. The Talairach coordinate system was used.

Figure 3

Power and Granger causality analysis at the scalp CSD level for Experiment 1. (A) Topographical map of percentage change of alpha power by contrasting attend-left condition against attend-right condition. The channels which showed strong alpha modulation were marked by black triangles and selected as sensory channels of interest for Granger causality analysis. (B) Grand average power spectra from a left posterior channel (PO3) under attend (attend-right) and ignore (attend-left) conditions. The shaded area indicates the standard error of the mean. (C) Topographical map of top-down modulation index (TDMI) in the alpha band. Channels with high TDMI values are channels whose causal influences to the marked occipital channels are highly modulated by spatial attention. Channels inside the square box are considered top channels. Here the analysis window is −500 to 0 ms with 0 ms denoting stimulus onset. (D) Grand average Granger causality spectra from a right frontal channel (FC4) to the marked occipital channels (black triangles) under attend and ignore conditions (see Methods).

Figure 4

Granger causality analysis at the source level for Experiment 1. (A) Top-down modulation index (TDMI) of regional sources during anticipatory visual spatial attention. MFG, middle frontal gyrus; IFG, inferior frontal gyrus; FEF, frontal eye field; IPS, intraparietal sulcus; ITG, inferior temporal gyrus; ACC, anterior cingulate cortex. (B) TDMI of left hemisphere sources and right hemisphere sources ^*p < 0.05. (C) Schematic showing that alpha-band causal influences, the right FEF→OC (occipital cortex) and the right IFG→OC, significantly decreased in the attend condition compared to the ignore condition.

Figure 5

Power and Granger causality analysis at the scalp CSD level for Experiment 2. (A) Topographical map of the alpha power percentage change between load-5 and load-1. Channels showing strong alpha modulation were marked by black triangles and selected as sensory channels of interest for Granger causality analysis. (B) Grand average power spectra from an occipital channel (Oz) under load-1, load-3, and load-5 conditions. The shaded area indicates the standard error of the mean. (C) Topographical map of the top-down modulation index (TDMI) in the alpha band. The channels with high TDMI values mean that their causal influences to the marked occipital channels are highly modulated by working memory load. Channels inside the square box are considered top channels. Here the analysis window is −2000 to −1000 ms with 0 ms denoting probe onset. (D) Grand average Granger causality spectra from a left frontal channel (AF3) to the marked occipital channels under load-1, load-3, and load-5 conditions.

Figure 6

Granger causality analysis at the source level for Experiment 2. (A) Top-down modulation index (TDMI) of regional sources during working memory retention. (B) TDMI of left hemisphere sources and right hemisphere sources ^*p < 0.05. (C) Schematic showing that alpha-band causal influence, left MFG→OC, significantly increased in load-5 condition compared to load-1 condition.