Abstract

The human sensorimotor system is sensitive to both limb-related prediction errors and task-related performance errors. Prediction error signals are believed to drive implicit refinements to motor plans. However, an understanding of the mechanisms that performance errors stimulate has remained unclear largely because their effects have not been probed in isolation from prediction errors. Diverging from past work, we induced performance errors independent of prediction errors by shifting the location of a reach target but keeping the intended and actual kinematic consequences of the motion matched. Our first two experiments revealed that rather than implicit learning, motor adjustments in response to performance errors reflect the use of deliberative, volitional strategies. Our third experiment revealed a potential dissociation of performance-error-driven strategies based on error size. Specifically, behavioral changes following large errors were consistent with goal-directed or model-based control, known to be supported by connections between prefrontal cortex and associative striatum. In contrast, motor changes following smaller performance errors carried signatures of model-free stimulus-response learning, of the kind underpinned by pathways between motor cortical areas and sensorimotor striatum. Across all experiments, we also found remarkably faster re-learning, advocating that such “savings” is associated with retrieval of previously learned strategic error compensation and may not require a history of exposure to limb-related errors.

Highlights

  • Studies of motor adaptation, the capacity to recalibrate our actions to changing body and environmental conditions, have been instrumental in characterizing many fundamental principles of sensorimotor learning

  • Perturbations applied to moving effectors produce not just sensory prediction errors (SPEs), but can result in task performance errors (TPEs)

  • Our results indicate that: 1) in the absence of an SPE, adaptive responses to consistently presented TPEs occur in the form of volitional strategies, 2) these strategies could be sensitive to the size of the TPE, and 3) strategy use facilitates savings; a history of exposure to SPEs is not needed for savings to occur

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Summary

Introduction

The capacity to recalibrate our actions to changing body and environmental conditions, have been instrumental in characterizing many fundamental principles of sensorimotor learning. It is generally believed that such sensory prediction errors (SPEs) are compensated by implicitly recalibrating motor plans (Mazzoni and Krakauer, 2006; Morehead et al, 2017; Oza et al, 2020). SPE-driven changes in motor output are dependent on cerebellar (Flament et al, 1996; Martin et al, 1996; Morehead et al, 2017) and posterior parietal networks (Clower et al, 1996; Della-Maggiore et al., 2004; Kumar et al, 2020); disruption in these regions, either naturally due to Stroke or degeneration, or artificially using brain stimulation techniques, produces clear deficits in SPE-based learning. Perturbations applied to moving effectors produce not just SPEs, but can result in task performance errors (TPEs). Learning to compensate TPEs plausibly requires intact cortico-striatal circuits (Anguera et al., 2010; Taylor and Ivry, 2012), a measure of the TPE itself could come from the simple spike discharge of cerebellar Purkinje neurons (Popa et al, 2017)

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