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Context-dependent decay of motor memories during skill acquisition.

ABSTRACT: Current models of motor learning posit that skill acquisition involves both the formation and decay of multiple motor memories that can be engaged in different contexts. Memory formation is assumed to be context dependent, so that errors most strongly update motor memories associated with the current context. In contrast, memory decay is assumed to be context independent, so that movement in any context leads to uniform decay across all contexts. We demonstrate that for both object manipulation and force-field adaptation, contrary to previous models, memory decay is highly context dependent. We show that the decay of memory associated with a given context is greatest for movements made in that context, with more distant contexts showing markedly reduced decay. Thus, both memory formation and decay are strongest for the current context. We propose that this apparently paradoxical organization provides a mechanism for optimizing performance. While memory decay tends to reduce force output, memory formation can correct for any errors that arise, allowing the motor system to regulate force output so as to both minimize errors and avoid unnecessary energy expenditure. The motor commands for any given context thus result from a balance between memory formation and decay, while memories for other contexts are preserved.

SUBMITTER: Ingram JN

PROVIDER: S-EPMC3688072 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Context-dependent decay of motor memories during skill acquisition.

Ingram James N JN Flanagan J Randall JR Wolpert Daniel M DM

Current biology : CB 20130530 12

Current models of motor learning posit that skill acquisition involves both the formation and decay of multiple motor memories that can be engaged in different contexts. Memory formation is assumed to be context dependent, so that errors most strongly update motor memories associated with the current context. In contrast, memory decay is assumed to be context independent, so that movement in any context leads to uniform decay across all contexts. We demonstrate that for both object manipulation ...[more]

PMID: 23727092

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Project description:Motor performance and learning have distinct behavioral and neural signatures and can be uniquely modulated by various informational and motivational factors. Contemporary frameworks describe four different motor learning mechanisms mapped onto specific neural regions which are key for motor skill acquisition: error-based learning (cerebellum), reinforcement learning (basal ganglia), cognitive strategies (prefrontal cortex), and use-dependent learning (motor cortex). However, little is known about the neural circuits engaged during skill acquisition that are modulated specifically by practice-based performance improvement and those that predict recall performance. Based on previous work, we hypothesize that brain activity during practice in primary motor cortex and basal ganglia (1) is associated with trial-by-trial practice performance and (2) is predictive of immediate recall performance. Leveraging the contemporary framework, we use a well-known task paradigm that primarily relies upon cognitive strategy, reinforcement, and use-based learning mechanisms to test our hypotheses. Forty neurotypical young adults were asked to practice a pinch force tracking task. Participants received performance feedback after each trial during practice. We used whole brain analysis of functional magnetic resonance imaging (fMRI) and behavioral performance measures (i.e., time-on-target and self-efficacy) during the practice phase to determine which brain activation patterns are (1) associated with trial-by-trial tracking performance and (2) predictive of immediate no-feedback retention performance. We observed brain activations in the frontal orbital cortex, putamen, amygdala, and insula correlated with tracking performance improvement during practice. In contrast, a different set of performance-related activated regions were observed that were associated with immediate retention performance that included the primary motor cortex, superior frontal gyrus, somatosensory cortex, angular gyrus, and parietal gyrus. Our findings demonstrate that improved practice performance and recall of a sensorimotor skill are correlated with distinct neural activity patterns during acquisition, drawing on different motor learning mechanisms during encoding. While motor performance improvements depend on both cortical and subcortical regions, motor skill recall depends primarily on prefrontal and motor cortices. We discuss possible interpretations for why our hypothesis regarding basal ganglia activity and retention performance was not supported. Understanding the different neural mechanisms engaged in motor performance and learning may inform novel interventions to enhance motor skill learning.

Project description:The plasticity of the human nervous system allows us to acquire an open-ended repository of sensorimotor skills in adulthood, such as the mastery of tools, musical instruments or sports. How novel sensorimotor skills are learned from scratch is yet largely unknown. In particular, the so-called inverse mapping from goal states to motor states is underdetermined because a goal can often be achieved by many different movements (motor redundancy). How humans learn to resolve motor redundancy and by which principles they explore high-dimensional motor spaces has hardly been investigated. To study this question, we trained human participants in an unfamiliar and redundant visually-guided manual control task. We qualitatively compare the experimental results with simulation results from a population of artificial agents that learned the same task by Goal Babbling, which is an inverse-model learning approach for robotics. In Goal Babbling, goal-related feedback guides motor exploration and thereby enables robots to learn an inverse model directly from scratch, without having to learn a forward model first. In the human experiment, we tested whether different initial conditions (starting positions of the hand) influence the acquisition of motor synergies, which we identified by Principal Component Analysis in the motor space. The results show that the human participants' solutions are spatially biased towards the different starting positions in motor space and are marked by a gradual co-learning of synergies and task success, similar to the dynamics of motor learning by Goal Babbling. However, there are also differences between human learning and the Goal Babbling simulations, as humans tend to predominantly use Degrees of Freedom that do not have a large effect on the hand position, whereas in Goal Babbling, Degrees of Freedom with a large effect on hand position are used predominantly. We conclude that humans use goal-related feedback to constrain motor exploration and resolve motor redundancy when learning a new sensorimotor mapping, but in a manner that differs from the current implementation of Goal Babbling due to different constraints on motor exploration.

Dataset Information

Context-dependent decay of motor memories during skill acquisition.

Publications

Context-dependent decay of motor memories during skill acquisition.

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