Dissociating the Contributions of Frontal Eye Field Activity to Spatial Working Memory and Motor Preparation

Neurons within dorsolateral prefrontal cortex (PFC) of primates are characterized by robust persistent spiking activity exhibited during the delay period of working memory tasks. This includes the frontal eye field (FEF) where nearly half of the neurons are active when spatial locations are held in working memory. Past evidence has established the FEF's contribution to the planning and triggering of saccadic eye movements as well as to the control of visual spatial attention. However, it remains unclear whether persistent delay activity reflects a similar dual role in movement planning and visuospatial working memory. We trained male monkeys to alternate between different forms of a spatial working memory task which could dissociate remembered stimulus locations from planned eye movements. We tested the effects of inactivation of FEF sites on behavioral performance in the different tasks. Consistent with previous studies, FEF inactivation impaired the execution of memory-guided saccades (MGSs), and impaired performance when remembered locations matched the planned eye movement. In contrast, memory performance was largely unaffected when the remembered location was dissociated from the correct eye movement response. Overall, the inactivation effects demonstrated clear deficits in eye movements, regardless of task type, but little or no evidence of a deficit in spatial working memory. Thus, our results indicate that persistent delay activity in the FEF contributes primarily to the preparation of eye movements and not to spatial working memory.SIGNIFICANCE STATEMENT Many frontal eye field (FEF) neurons exhibit spatially tuned persistent spiking activity during the delay period of working memory tasks. However, the role of the FEF in spatial working memory remains unresolved. We tested the effects of inactivation of FEF sites on behavioral performance in different forms of a spatial working memory task, one of which dissociated the remembered stimulus locations from planned eye movements. We found that FEF inactivation produced clear deficits in eye movements, regardless of task type, but no deficit in spatial working memory when dissociated from those movements.