Frontal eye field inactivation reduces saccade preparation in the superior colliculus, but does not alter how preparatory activity relates to saccade latency

Abstract

A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of preparatory activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of iSC preparatory activity precede shorter SRTs. The frontal eye fields (FEF) are one likely source of such iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEFs role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys we examined iSC preparatory activity during unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced fixation-related activity in the rostral iSC. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. These analyses revealed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades, suggesting that the integration of preparatory and visual signals in the SC just before saccade initiation is largely independent of the FEF for saccades generated in this task.\n\nSignificance statementHow does the brain decide when to move? Here, we investigate the role of two oculomotor structures, the superior colliculus (SC) and frontal eye fields (FEF), in dictating visually-guided saccadic reaction times (SRTs). In both structures, higher levels of preparatory activity precede shorter SRTs. Here, we show that FEF inactivation increases SRTs and decreases SC preparatory activity. Surprisingly, a population-level analysis of SC preparatory activity showed a negligible impact of FEF inactivation, providing one examines SRT-matched saccades. Thus, while the FEF is one source of preparatory input to the SC, it is not a critical source, and it is not involved in the integration of preparatory activity and visual signals that precedes saccade initiation in simple visually-guided saccade tasks.