Dissociable Roles of FEF Neurons in Initiating Saccades

Abstract

The frontal eye field (FEF) plays a key role in initiating saccades. To explain how single neurons in this region may enable the initiation of saccades, Jeffery Schall proposed the "variable rate model" (Hanes and Schall, 1996) which assumes that the discharge of a neuron must reach a fixed activation threshold for a saccade to be evoked. However, the validity of this model has been questioned as results from later work testing saccades in different behavioral contexts seemed to require the assumption of variable thresholds. Moreover, even when sticking to the original behavioral context, not all types of frontal eye field neurons seemed to behave according to a variable rate model. In an attempt to reconsider the viability of the variable rate model avoiding limitations of previous research, we studied single neurons recorded from the FEF of two rhesus monkeys while they performed a memory-guided saccade task. We evaluated the degree to which each type of FEF neurons complied with the variable rate model by quantifying how precisely their discharge predicted an imminent saccade based on their immediate presaccadic activity. In addition, we asked whether there might be a hierarchical relation between visuomotor and motor neurons with only the latter responsible for the release of saccades and therefore satisfying the assumption of the variable rate model. We show that decoders trained on single motor neurons presaccadic activity performed better than decoders trained on visuomotor neurons in predicting an imminent saccade, in line with the assumption of a top position in a putative processing hierarchy. While this position might have suggested significant resilience to perturbation of the visual input to the FEF, we found quite the opposite that motor neurons but not visuomotor neurons were susceptible to perturbation. As a matter of fact, they lost the ability to predict the initiation of a saccade based on their immediate pressacadic discharge rate. Our results support the notion that motor neurons and visuomotor neurons have dissociable functions in information processing for saccades with motor neurons more closely related to saccade initiation, in line with the tenets of the variable rate model. Yet, they also clearly indicate that even these supposedly top layer neurons exhibit an unexpected degree of dependence on afferent input questions the viability of the assumption of a simple processing hierarchy.