Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye fields

Abstract

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of rapid saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model wherein activity related to the two saccade plans bilaterally and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence, compete for the processing capacity by perturbation of the saccade-related ramping activity. Finally, we show that in contrast to movement related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that for perceptually simple tasks, inhibition amongst movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.