Action space restructures visual working memory in prefrontal cortex

Abstract

Visual working memory enables flexible behavior by decoupling sensory stimuli from behavioral actions. While previous studies have predominantly focused on the storage component of working memory, the role of future actions in shaping working memory remains unknown. To answer this question, we used two working memory tasks that allowed the dissociation of sensory and action components of working memory. We measured behavioral performance and neuronal activity in the macaque prefrontal cortex area, frontal eye fields. We show that the action space reshapes working memory, as evidenced by distinct patterns of memory tuning and attentional orienting between the two tasks. Notably, neuronal activity during the working memory period predicted future behavior and exhibited mixed selectivity in relation to the sensory space but linear selectivity relative to the action space. This linear selectivity was achieved through the rapid transformation from sensory to action space and was subsequently maintained as a stable cross-temporal population activity pattern. Combined, we provide direct physiological evidence of the action-oriented nature of frontal eye field neurons during memory tasks and demonstrate that the anticipation of behavioral outcomes plays a significant role in transforming and maintaining the contents of visual working memory.