Integration of eye-centered and landmark-centered codes in frontal eye field gaze responses

ABSTRACT 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 process, we recorded primate frontal eye field (FEF) 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 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.