Fast Feedback Responses to Categorical Sensorimotor Errors That Do Not Indicate Error Magnitude Are Optimized Based on Short- and Long-Term Memory

Abstract

Skilled motor performance depends critically on rapid corrective responses that act to preserve the goal of the movement in the face of perturbations. Although it is well established that the gain of corrective responses elicited while reaching toward objects adapts to different contexts, little is known about the adaptability of corrective responses supporting the manipulation of objects after they are grasped. Here, we investigated the adaptability of the corrective response elicited when an object being lifted is heavier than expected and fails to lift off when predicted. This response involves a monotonic increase in vertical load force triggered, within ∼90 ms, by the absence of expected sensory feedback signaling lift off and terminated when actual lift off occurs. Critically, because the actual weight of the object cannot be directly sensed at the moment the object fails to lift off, any adaptation of the corrective response would have to be based on memory from previous lifts. We show that when humans, including men and women, repeatedly lift an object that on occasional catch trials increases from a baseline weight to a fixed heavier weight, they scale the gain of the response (i.e., the rate of force increase) to the heavier weight within two to three catch trials. We also show that the gain of the response scales, on the first catch trial, with the baseline weight of the object. Thus, the gain of the lifting response can be adapted by both short- and long-term experience. Finally, we demonstrate that this adaptation preserves the efficacy of the response across contexts.SIGNIFICANCE STATEMENTHere, we present the first investigation of the adaptability of the corrective lifting response elicited when an object is heavier than expected and fails to lift off when predicted. A striking feature of the response, which is driven by a sensory prediction error arising from the absence of expected sensory feedback, is that the magnitude of the error is unknown. That is, the motor system only receives a categorical error indicating that the object is heavier than expected but not its actual weight. Although the error magnitude is not known at the moment the response is elicited, we show that the response can be scaled to predictions of error magnitude based on both recent and long-term memories.