Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

Abstract

Saccades require a spatiotemporal transformation of activity between the intermediate layers of the superior colliculus (iSC) and downstream brainstem burst generator. The dynamic linear ensemble-coding model (Goossens and Van Opstal, 2006) proposes that each iSC spike contributes a fixed mini-vector to saccade displacement. Although biologically-plausible, this model assumes cortical areas like the frontal eye fields (FEF) simply provide the saccadic goal to be executed by the iSC and brainstem burst generator. However, the FEF and iSC operate in unison during saccades, and a pathway from the FEF to the brainstem burst generator that bypasses the iSC exists. Here, we investigate the impact of large yet reversible inactivation of the FEF on iSC activity in the context of the model across four saccade tasks. We exploit the overlap of saccade vectors generated when the FEF is inactivated or not, comparing the number of iSC spikes for metrically-matched saccades. We found that the iSC emits fewer spikes for metrically-matched saccades during FEF inactivation. The decrease in spike count is task-dependent, with a greater decrease accompanying more cognitively-demanding saccades. Our results show that FEF integrity influences the readout of iSC activity in a task-dependent manner. We propose that the dynamic linear ensemble-coding model be modified so that FEF inactivation increases the gain of a readout parameter, effectively increasing the influence of a single iSC spike. We speculate that this modification could be instantiated by a direct pathway from the FEF to the omnipause region that modulates the excitability of the brainstem burst generator.\n\nSignificance statementOne of the enduring puzzles in the oculomotor system is how it achieves the spatiotemporal transformation, converting spatial activity within the intermediate layers of the superior colliculus (iSC) into a rate code within the brainstem burst generator. The spatiotemporal transformation has traditionally been viewed as the purview of the oculomotor brainstem. Here, within the context of testing a biologically-plausible model of the spatiotemporal transformation, we show that reversible inactivation of the frontal eye fields (FEF) decreases the number of spikes issued by the iSC for metrically-matched saccades, with greater decreases accompanying more cognitively-demanding tasks. These results show that signals from the FEF influence the spatiotemporal transformation.