From reactive to anticipatory control of tongue movements for interception in mice

Abstract

Object interception requires integrating prediction and sensory feedback, making it a powerful model for studying sensorimotor transformations. However, traditional head-fixed mouse paradigms reduce behavior to stereotyped stimulus-response associations and lack key features of natural interception. To address this limitation, we developed a behavioral task in which head-fixed mice use their tongue to intercept a food pellet moving at one of seven constant speeds randomly selected on each trial. We characterized the 3D kinematics of discrete tongue-reaching movements, their distinct motor phases, and learning-dependent changes in movement timing and kinematics. Mice adapted both tongue kinematics and movement onset to pellet speed, initially relying on reactive control and later adopting an anticipatory strategy. Anticipatory control depended largely on vision and intact lateral cerebellar circuits. This paradigm provides a powerful platform for investigating the neural mechanisms underlying predictive sensorimotor control and object interception in head-fixed mice. Significance StatementIn natural environments, interception requires seamless sensory-motor transformation, yet traditional paradigms like classical conditioning and virtual reality fall short of capturing this complex behavior. We introduce a behavioral paradigm in which trained mice intercept food pellets moving at constant speeds that vary randomly across trials, with discrete tongue licks. Remarkably, mice exhibit a shift from a reactive to a more anticipatory motor strategy, adaptively tuning lick initiation and projection speed in a learning-dependent manner. This work establishes a simplified interception-like framework for studying sensorimotor dynamics in head-fixed mice.