The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

Abstract

The cerebellum is essential for error-driven motor learning and is strongly implicated in detecting and correcting for motor errors. Therefore, elucidating how motor errors are represented in the cerebellum is essential in understanding cerebellar function, in general, and its role in motor learning, in particular. This review examines how motor errors are encoded in the cerebellar cortex in the context of a forward internal model that generates predictions about the upcoming movement and drives learning and adaptation. In this framework, sensory prediction errors, defined as the discrepancy between the predicted consequences of motor commands and the sensory feedback, are crucial for both on-line movement control and motor learning. While many studies support the dominant view that motor errors are encoded in the complex spike discharge of Purkinje cells, others have failed to relate complex spike activity with errors. Given these limitations, we review recent findings in the monkey showing that complex spike modulation is not necessarily required for motor learning or for simple spike adaptation. Also, new results demonstrate that the simple spike discharge provides continuous error signals that both lead and lag the actual movements in time, suggesting errors are encoded as both an internal prediction of motor commands and the actual sensory feedback. These dual error representations have opposing effects on simple spike discharge, consistent with the signals needed to generate sensory prediction errors used to update a forward internal model.

Climbing Fibers Control Purkinje Cell Representations of Behavior

“…This study used a previously described pseudorandom tracking task (Paninski et al, 2004;Hewitt et al, 2011;Popa et al, 2012); therefore, the paradigm is only briefly detailed here. Two rhesus monkeys were trained to use a robotic manipulandum (InMotion 2 ) that controls a cross-shaped cursor to track a circular shaped target (2.5 cm diameter) on a computer screen (see Fig.…”

“…The paradigm required that the monkey maintain the cursor within the target, and allowed only brief excursions outside the target (Ͻ500 ms). Pseudo-random tracking has several advantages compared with other tasks, including providing more comprehensive and uniform coverage of parameter workspaces and dissociating kinematic from error parameters (Paninski et al, 2004;Hewitt et al, 2011). Hand (X and Y, based on cursor position) and target (X tg , Y tg ) position were sampled at 200 Hz.…”

“…Although substantial evidence supports a role for climbing fibers in error signaling and motor learning, CSs are not invariably activated by errors (for review, see Popa et al, 2016). Also, CSs are not essential for cerebellar motor learning (Ke et al, 2009;Nguyen-Vu et al, 2013;, SS discharge carries robust error signals (Popa et al, 2012), and there are significant challenges to the role of cerebellar LTD in motor learning (Schonewille et al, 2011).…”

“…Several hypotheses on CS contribution to real-time motor control emphasize short-term changes in Purkinje cell excitability. The "gain change" and "bistability" hypotheses suggest that CSs control the responses of a Purkinje cell to parallel fiber inputs (Ebner et al, 1983) and switch between "up" and "down" SS firing states (Loewenstein et al, 2005;McKay et al, 2007;Yartsev et al, 2009), respectively. Also, during behavior, CSs and SSs exhibit a reciprocal firing pattern that is mediated by climbing fiber input (Graf et al, 1988;Simpson et al, 1995;Yakhnitsa and Barmack, 2006;Badura et al, 2013).…”

Why New Spinal Cord Plasticity Does Not Disrupt Old Motor Behaviors

“…Whenever the behavior is performed, the associated sensory feedback is compared with the expected feedback (i.e., the feedback associated with normal performance). This comparison (which may occur in the cerebellum; D' Angelo et al, 2016;Popa et al, 2016) detects deviations from the key features of the behavior. These deviations constitute error signals that guide appropriate changes in the brain and spinal substrate responsible for the behavior.…”