The Role of the Frontal Eye Fields in Selecting Mixed-Strategy Saccades

Abstract

In a multi‐agent environment, animals must often adopt a stochastic mixed‐strategy approach to maximize reward and minimize costs; otherwise, competitive opponents can exploit predictable choice patterns. This thesis tested the hypothesis that the frontal eye field (FEF) are involved in selecting mixed‐strategy saccades. To this end, I recorded preparatory activity of single FEF neurons and manipulated the preparatory activity of neuronal ensembles within the FEF while a monkey played an oculomotor version of the mixed­‐strategy game ‘matching­‐pennies’. Each trial began with fixation on a central visual stimulus which was extinguished for a predetermined warning period before two targets were presented; one in the center and the other opposite the neuron’s response field. If both the monkey and the adaptive computer opponent chose the same target, the monkey received a liquid reward; otherwise the monkey received no reward for that trial. Like humans, monkeys chose each target in equal proportions but showed a ‘win‐stay’ bias in their choice patterns. Signal detection theory was used to analyze how accurately FEF preparatory activity predicted upcoming saccade choices. My data demonstrates that the accuracy by which FEF preparatory activity predicted upcoming strategic choices gradually increased as the time of saccade execution approached. This pattern of preparatory activity is consistent with an accumulation of evidence for each potential option towards a decision threshold. Subthreshold micro­‐stimulation biased mixed‐strategy saccadic choices, further suggesting a role for the FEF in choosing mixed­‐strategy saccades, albeit unexpectedly, in favor of saccades opposite the stimulation sites. Lastly, a particular advantage of my experiment is that the same monkey performed this task using neurophysiological experimentation in the FEF and intermediate layers of the superior colliculus (SCi). This allowed me to compare the timing and magnitude of neuronal selectivity and effects of subthreshold microstimulation across these two structures, during strategic decision‐making. My results indicate that the selection of mixed­‐strategy saccades occurred earlier and was greater in magnitude in the FEF compared to the SC, indicative of a decision process that occurs earlier in the frontal cortex before being relayed on to premotor regions in the midbrain.