Cognitive Control of Saccadic Selection and Inhibition from within the Core Cortical Saccadic Network

Abstract

The ability to select the task-relevant stimulus for a saccadic eye movement, while inhibiting saccades to task-irrelevant stimuli, is crucial for active vision. Here, we present a novel saccade-contingent behavioral paradigm and investigate the neural basis of the central cognitive functions underpinning such behavior, saccade selection, saccade inhibition, and saccadic choice, in female and male human participants. The paradigm allows for exceptionally well-matched contrasts, with task demands formalized with stochastic accumulation-to-threshold models. Using fMRI, we replicated the core cortical eye-movement network for saccade generation (frontal eye fields, posterior parietal cortex, and higher-level visual areas). However, in contrast to previously published tasks, saccadic selection and inhibition recruited only this core network. Brain-behavior analyses further showed that inhibition efficiency may be underpinned by white-matter integrity of tracts between key saccade-generating regions, and that inhibition efficiency is associated with right inferior frontal gyrus engagement, potentially implementing general-purpose inhibition. The core network, however, was insufficient for saccadic choice, which recruited anterior regions commonly attributed to saccadic action selection, including dorsolateral prefrontal cortex and anterior cingulate cortex. Jointly, the results indicate that extra-saccadic activity observed for free choice, and in previously published tasks probing saccadic control, is likely due to increased load on higher-level cognitive processes, and not saccadic selection per se, which is achieved within the canonical cortical eye movement network.SIGNIFICANCE STATEMENT The ability to selectively attend to, and to not attend to, parts of the world is crucial for successful action. Mapping the neural substrate of the key cognitive functions underlying such behavior, saccade selection and inhibition, is a challenge. Canonical tasks, often preceding the cognitive neuroscience revolution by decennia, were not designed to isolate single cognitive functions, and result in extremely widespread brain activity. We developed a novel behavioral paradigm, which demonstrates the following: (1) the cognitive control of saccades is achieved within key cortical saccadic brain regions; (2) individual variability in control efficiency is related to white-matter connectivity between the same regions; and (3) widespread activity in canonical tasks is likely related to higher-level cognitive demands and not saccadic control.

Keywords: cognitive control; eye-tracking; fMRI; inhibition; saccades; selection.

Figure 1.

A, A driving scene, low-level visual salience map (Harel et al., 2006), and salience map overlaid on scene. The most salient part of the image is the road sign. The task-relevant car on the left has very low salience. B, Trial structure. Each block of saccades began with fixation at one of the four possible target locations. After an interstimulus interval in the 0.75–1.25 s range (shifted and truncated exponential distribution), target stimuli were displayed. Once the eyes deviated by >3° from the current fixation, the targets were extinguished and replaced by a fixation dot at the target location. Blocks of 20 s of saccades were interleaved with blocks of 20 s of continuous fixation. C, Conditions. Pro-saccades involve saccading to a single target, high-contrast involves saccading to the most salient of two targets, low-contrast involves saccading to the least salient of two targets, and choice involves a free choice between the targets. Pairwise contrasts reflect: selection, inhibition, and choice. D, Stochastic accumulator model. Blue traces represent the target accumulator. Red traces represent the distractor. Dashed line indicates the threshold at which a decision is made. Gray line for the low-contrast condition indicates the distractor without inhibition. The model includes within- and across-trial Gaussian noise and lateral inhibition.

Figure 2.

fMRI session behavior. A, Median SRT as a function of condition. Error bars indicate IQR. B, Boxplots of ΔSRT as a function of contrasts between pairwise conditions. C, Boxplots of differences in error rates (Δerror rate) between pairwise conditions. Errors are undefined for the choice condition and therefore for the choice contrast.

Figure 3.

BOLD effects of pro-saccades and pairwise task contrasts. Pro-saccades show regions with greater activation for pro-saccades than fixation. Selection shows regions with greater activity for high-contrast blocks than for pro-saccade blocks. Inhibition shows regions with greater activity for low-contrast blocks than for high-contrast blocks. Choice shows regions with greater activity for choice blocks than for low-contrast blocks. Heat maps were cluster-corrected at z = 2.3 and p = 0.05, and scaled to lie in the Z = 2.3–4 interval. Slice coordinates are in MNI space.

Figure 4.

BOLD effects of error frequency and saccade frequency control regressors. Cooler colors represent greater activation. Maps were cluster-corrected at z = 2.3 and p = 0.05, and heat maps are scaled to lie in the Z = 2.3–4 interval. Slice coordinates are in MNI space.

Figure 5.

Individual ΔSRT and BOLD effects. For pro-saccades, blue colormaps represent areas in which faster SRT was associated with greater activation. For pairwise contrasts, red heat maps represent areas for which greater difference in SRT (ΔSRT) was associated with greater activation. Blue heat maps represent areas for which smaller ΔSRT was associated with greater activation. Maps were cluster-corrected at z = 2.3 and p = 0.05, and heat maps are scaled to lie in the Z = −4 to −2.3, 2.3 to 4 interval. Slice coordinates are in MNI space.

Figure 6.

TBSS analyses of the relationship between SRT for pro-saccades, and ΔSRT for inhibition, and FA. Participants were median split into high and low SRT groups, and inferences performed on positive and negative associations between SRT and FA. Scatter plots represent the underlying continuous relationship between SRT (pro-saccades) and FA, and ΔSRT (inhibition) and FA averaged across all clusters of significant effects. Heat maps are probability maps thresholded at p = 0.05 (corrected).