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.