Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention

Abstract

Advance information about an impending stimulus facilitates its subsequent identification and ensuing behavioral responses. This facilitation is thought to be mediated by top-down control signals from frontal and parietal cortex that modulate sensory cortical activity. Here we show, using Granger causality measures on blood oxygen level-dependent time series, that frontal eye field (FEF) and intraparietal sulcus (IPS) activity predicts visual occipital activity before an expected visual stimulus. Top-down levels of Granger causality from FEF and IPS to visual occipital cortex were significantly greater than both bottom-up and mean cortex-wide levels in all individual subjects and the group. In the group and most individual subjects, Granger causality was significantly greater from FEF to IPS than from IPS to FEF, and significantly greater from both FEF and IPS to intermediate-tier than lower-tier ventral visual areas. Moreover, top-down Granger causality from right IPS to intermediate-tier areas was predictive of correct behavioral performance. These results suggest that FEF and IPS modulate visual occipital cortex, and FEF modulates IPS, in relation to visual attention. The current approach may prove advantageous for the investigation of interregional directed influences in other human brain functions.

Figure 1.

Visual spatial attention behavioral paradigm. An auditory preparatory cue (“Left” or “Right”) began each trial, instructing subjects to attend a location left or right of the vertical meridian. After a stimulus-onset asynchrony (10.32 s), visual targets appeared for 100 ms centered at both locations, concurrent with an auditory report cue (“Left” or “Right”). BOLD data were acquired with TR = 2.064 s. The sample times used for analysis are marked by triangles. The figure is not drawn to scale.

Figure 2.

Top-down (left) and bottom-up (middle) Granger causality F-statistic histograms for a representative ROI pair, right aIPS and right V3A, in one subject. The critical value of F is 3.87 for significance (p < 0.05) in both directions. A larger fraction of the total number of voxel pairs (1064) has significant F statistics in the top-down (16.9%) than in the bottom-up (8.7%) direction. The schematic diagram (right) shows Granger causality represented as arrows in the two directions between these ROIs on a standard brain image. Arrow thickness corresponds to the significant fraction, representing Granger causality strength.

Figure 3.

A–E, Top-down versus bottom-up Granger causality. The mean fraction of significant F is significantly greater for top-down (blue) than for bottom-up (red) Granger causality when measured separately for each subject (A) and for 59 of 60 ROI pairs with all subjects combined (C), but not in the voxel-randomized (D) or trial-randomized (E) data. Error bars indicate variability across ROI pairs (A, B, D, E) or across subjects (C). B, The mean fraction of significant F is significantly greater from FEF to IPS than from IPS to FEF for five of six subjects. C, ROI pairs follow left-to-right, top-to-bottom ordering in Figure 4A.

Figure 4.

Top-down Granger causality before correct versus incorrect performance. A, Grid specifying the significance of correct versus incorrect performance difference in a group analysis of top-down Granger causality: *p < 0.05, **p < 1.0 × 10⁻¹⁰, ***p < 1.0 × 10⁻³⁰; white, not significant. Each cell represents Granger causality from the row-labeled ROI to the column-labeled ROI. B, The fraction of significant top-down Granger causality from right aIPS to left VP was significantly greater before correct (blue) than incorrect (red) performance in five of six subjects.