A fundamental question in sensorimotor control concerns the transformation of spatial signals from the retina into eye and head motor commands required for accurate gaze shifts. Here, we investigated these transformations by identifying the spatial codes embedded in visually evoked and movement-related responses in the frontal eye fields (FEFs) during head-unrestrained gaze shifts. Monkeys made delayed gaze shifts to the remembered location of briefly presented visual stimuli, with delay serving to dissociate visual and movement responses. A statistical analysis of nonparametric model fits to response field data from 57 neurons (38 with visual and 49 with movement activities) eliminated most effector-specific, head-fixed, and space-fixed models, but confirmed the dominance of eye-centered codes observed in head-restrained studies. More importantly, the visual response encoded target location, whereas the movement response mainly encoded the final position of the imminent gaze shift (including gaze errors). This spatiotemporal distinction between target and gaze coding was present not only at the population level, but even at the single-cell level. We propose that an imperfect visual–motor transformation occurs during the brief memory interval between perception and action, and further transformations from the FEF's eye-centered gaze motor code to effector-specific codes in motor frames occur downstream in the subcortical areas.

Medial frontal cortex enables performance monitoring, indexed by the error-related negativity (ERN) and manifest by performance adaptations. In monkeys performing a saccade countermanding (stop signal) task, we recorded EEG over and neural spiking across all layers of the supplementary eye field (SEF), an agranular cortical area. Neurons signaling error production, feedback predicting reward gain or loss, and delivery of fluid reward had different spike widths and were concentrated differently across layers. Neurons signaling error or loss of reward were more common in layers 2 and 3 (L2/3), while neurons signaling gain of reward were more common in layers 5 and 6 (L5/6). Variation of error- and reinforcement-related spike rates in L2/3 but not L5/6 predicted response time adaptation. Variation in error-related spike rate in L2/3 but not L5/6 predicted ERN magnitude. These findings reveal novel features of cortical microcircuitry supporting performance monitoring and confirm one cortical source of the ERN.

The visual system is thought to separate egocentric and allocentric representations, but behavioral experiments show that these codes are optimally integrated to influence goal-directed movements. To test if frontal cortex participates in this integration, we recorded primate frontal eye field activity during a cue-conflict memory delay saccade task. To dissociate egocentric and allocentric coordinates, we surreptitiously shifted a visual landmark during the delay period, causing saccades to deviate by 37% in the same direction. To assess the cellular mechanisms, we fit neural response fields against an egocentric (eye-centered target-to-gaze) continuum, and an allocentric shift (eye-to-landmark-centered) continuum. Initial visual responses best-fit target position. Motor responses (after the landmark shift) predicted future gaze position but embedded within the motor code was a 29% shift toward allocentric coordinates. This shift appeared transiently in memory-related visuomotor activity, and then reappeared in motor activity before saccades. Notably, fits along the egocentric and allocentric shift continua were initially independent, but became correlated across neurons just before the motor burst. Overall, these results implicate frontal cortex in the integration of egocentric and allocentric visual information for goal-directed action, and demonstrate the cell-specific, temporal progression of signal multiplexing for this process in the gaze system.