Priors Engaged in Long-Latency Responses to Mechanical Perturbations Suggest a Rapid Update in State Estimation

In every motor task, our brain must handle external forces acting on the body. For example, riding a bike on cobblestones or skating on irregular surface requires us to appropriately respond to external perturbations. In these situations, motor predictions cannot help anticipate the motion of the body induced by external factors, and direct use of delayed sensory feedback will tend to generate instability. Here, we show that to solve this problem the motor system uses a rapid sensory prediction to correct the estimated state of the limb. We used a postural task with mechanical perturbations to address whether sensory predictions were engaged in upper-limb corrective movements. Subjects altered their initial motor response in ∼60 ms, depending on the expected perturbation profile, suggesting the use of an internal model, or prior, in this corrective process. Further, we found trial-to-trial changes in corrective responses indicating a rapid update of these perturbation priors. We used a computational model based on Kalman filtering to show that the response modulation was compatible with a rapid correction of the estimated state engaged in the feedback response. Such a process may allow us to handle external disturbances encountered in virtually every physical activity, which is likely an important feature of skilled motor behaviour.Author Summary: It is commonly assumed that the brain uses internal estimates of the state of the body to adjust motor commands and perform successful movements. A problem arises when external disturbances deviate the limb from the ongoing task. In such cases, the estimated state of the body must be corrected based on sensory feedback. Because neural transmission delays can destabilize feedback control, an important challenge for motor systems is to correct the estimated state as quickly as possible. In this paper, we tested whether such a rapid correction is performed following mechanical loads applied to the upper limb. Our results indicate that long latency responses (∼50–100 ms) exhibit knowledge of the relationship between the delayed sensed joint displacement and the current state of the limb at the onset of the motor response. Importantly, this knowledge can be adjusted from one perturbation response to the next, should a distinct perturbation profile be experienced. These results suggest that a correction of state estimation is performed within the limb rapid-feedback pathways, allowing fast and stable feedback control.