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Distinct types of neural reorganization during long-term learning.

ABSTRACT: What are the neural mechanisms of skill acquisition? Many studies find that long-term practice is associated with a functional reorganization of cortical neural activity. However, the link between these changes in neural activity and the behavioral improvements that occur is not well understood, especially for long-term learning that takes place over several weeks. To probe this link in detail, we leveraged a brain-computer interface (BCI) paradigm in which rhesus monkeys learned to master nonintuitive mappings between neural spiking in primary motor cortex and computer cursor movement. Critically, these BCI mappings were designed to disambiguate several different possible types of neural reorganization. We found that during the initial phase of learning, lasting minutes to hours, rapid changes in neural activity common to all neurons led to a fast suppression of motor error. In parallel, local changes to individual neurons gradually accrued over several weeks of training. This slower timescale cortical reorganization persisted long after the movement errors had decreased to asymptote and was associated with more efficient control of movement. We conclude that long-term practice evokes two distinct neural reorganization processes with vastly different timescales, leading to different aspects of improvement in motor behavior. NEW & NOTEWORTHY We leveraged a brain-computer interface learning paradigm to track the neural reorganization occurring throughout the full time course of motor skill learning lasting several weeks. We report on two distinct types of neural reorganization that mirror distinct phases of behavioral improvement: a fast phase, in which global reorganization of neural recruitment leads to a quick suppression of motor error, and a slow phase, in which local changes in individual tuning lead to improvements in movement efficiency.

SUBMITTER: Zhou X

PROVIDER: S-EPMC6485743 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Distinct types of neural reorganization during long-term learning.

Zhou Xiao X Tien Rex N RN Ravikumar Sadhana S Chase Steven M SM

Journal of neurophysiology 20190206 4

What are the neural mechanisms of skill acquisition? Many studies find that long-term practice is associated with a functional reorganization of cortical neural activity. However, the link between these changes in neural activity and the behavioral improvements that occur is not well understood, especially for long-term learning that takes place over several weeks. To probe this link in detail, we leveraged a brain-computer interface (BCI) paradigm in which rhesus monkeys learned to master nonin ...[more]

PMID: 30726164

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Project description:BackgroundBrain-computer interfaces (BCIs) are systems capable of translating human brain patterns, measured through electroencephalography (EEG), into commands for an external device. Despite the great advances in machine learning solutions to enhance the performance of BCI decoders, the translational impact of this technology remains elusive. The reliability of BCIs is often unsatisfactory for end-users, limiting their application outside a laboratory environment.MethodsWe present the analysis on the data acquired from an end-user during the preparation for two Cybathlon competitions, where our pilot won the gold medal twice in a row. These data are of particular interest given the mutual learning approach adopted during the longitudinal training phase (8 months), the long training break in between the two events (1 year) and the demanding evaluation scenario. A multifaceted perspective on long-term user learning is proposed: we enriched the information gathered through conventional metrics (e.g., accuracy, application performances) by investigating novel neural correlates of learning in different neural domains.ResultsFirst, we showed that by focusing the training on user learning, the pilot was capable of significantly improving his performance over time even with infrequent decoder re-calibrations. Second, we revealed that the analysis of the within-class modifications of the pilot's neural patterns in the Riemannian domain is more effective in tracking the acquisition and the stabilization of BCI skills, especially after the 1-year break. These results further confirmed the key role of mutual learning in the acquisition of BCI skills, and particularly highlighted the importance of user learning as a key to enhance BCI reliability.ConclusionWe firmly believe that our work may open new perspectives and fuel discussions in the BCI field to shift the focus of future research: not only to the machine learning of the decoder, but also in investigating novel training procedures to boost the user learning and the stability of the BCI skills in the long-term. To this end, the analyses and the metrics proposed could be used to monitor the user learning during training and provide a marker guiding the decoder re-calibration to maximize the mutual adaptation of the user to the BCI system.

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Distinct types of neural reorganization during long-term learning.

Publications

Distinct types of neural reorganization during long-term learning.

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