Eye-hand coordination beyond vision: preceding gaze history shapes reaching memories

Abstract

Skilled reaching behaviors, such as grasping a cup or catching a ball, require adaptive changes in response to error signals. In natural behavior, reaches are typically coordinated with preceding eye movements toward the target. Despite this behavioral relevance, the potential linkage between preceding eye movements themselves, rather than static gaze positions, and memory formation for reaching has been largely overlooked. Here, we used a visuomotor rotation task to investigate how recent dynamic gaze states contribute to the formation and retrieval of reaching memories. We show that, in the learning of two conflicting visuomotor maps that would normally interfere with one another (namely, clockwise and counterclockwise rotation), not only the static spatial relationship between the gaze and the target but also the dynamic state of the eye movements themselves can serve as contextual cues that enable learning. We further show that the generalization pattern of reach learning across different gaze conditions can be explained by the gaze states distance computed with temporal weighting. These findings indicate that reaching memories are encoded in tight association with the recent history of preceding gaze states. Our results expand the functional role of eye-hand coordination beyond visual guidance, revealing its importance in orchestrating flexible motor learning. Significant StatementIn everyday behavior, goal-directed arm movements are typically preceded by eye movements, and eye-hand coordination has been regarded mainly as a functional mechanism for visual guidance of action. This study expands that view by showing that preceding gaze states also shape how the brain learns and retrieves motor memories of reaches. We demonstrate that conflicting visuomotor maps, which are usually difficult to learn because of memory interference, can be learned simultaneously when they are associated with different preceding eye movements. Furthermore, generalization experiments show that reach learning depends on the recent history of gaze states within a brief time window before reach onset. These findings indicate that preceding gaze history plays a significant role in shaping flexible reach memories.