Interacting adaptive processes with different timescales underlie short-term motor learning

Smith, Maurice A; Ghazizadeh, Ali; Shadmehr, Reza

doi:10.1371/journal.pbio.0040179

Cited by 1,113Motor Control and AdaptationMemory and Neural MechanismsTactile and Sensory Interactions

Interacting adaptive processes with different timescales underlie short-term motor learning

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Smith, Maurice A, Ghazizadeh, Ali, Shadmehr, Reza·2006·PLoS Biology

DOI 10.1371/journal.pbio.0040179PMC PMC1463025

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Abstract

Multiple processes may contribute to motor skill acquisition, but it is thought that many of these processes require sleep or the passage of long periods of time ranging from several hours to many days or weeks. Here we demonstrate that within a timescale of minutes, two distinct fast-acting processes drive motor adaptation. One process responds weakly to error but retains information well, whereas the other responds strongly but has poor retention. This two-state learning system makes the surprising prediction of spontaneous recovery (or adaptation rebound) if error feedback is clamped at zero following an adaptation-extinction training episode. We used a novel paradigm to experimentally confirm this prediction in human motor learning of reaching, and we show that the interaction between the learning processes in this simple two-state system provides a unifying explanation for several different, apparently unrelated, phenomena in motor adaptation including savings, anterograde interference, spontaneous recovery, and rapid unlearning. Our results suggest that motor adaptation depends on at least two distinct neural systems that have different sensitivity to error and retain information at different rates.

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SSM variants that include multiple timescales of learning explain savings over short timescales but fail to predict savings following a prolonged period of washout.
“Although SSM variants that include multiple timescales of learning (Kording et al., 2007; Smith et al., 2006) are able to explain savings over short timescales, this approach fails to predict the fact that savings still occurs following a prolonged period of washout of initial learning (Krakauer et al., 2005; Zarahn et al., 2008).”
From Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models (2011) · cites this paper as Smith et al., 2006
Savings is a form of procedural and motor memory that manifests as faster relearning compared with initial learning.
“Savings is a form of procedural and motor memory that manifests as faster relearning compared with initial learning (Ebbinghaus, 1913; Smith et al., 2006; Zarahn et al., 2008).”
From Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models (2011) · cites this paper as Smith et al., 2006
A recent motor learning model has been conceptualized in terms of the existence of fast and slow error-based processes.
“A recent motor learning model has been conceptualized in terms of the existence of fast and slow error-based processes (Kording et al., 2007; Smith et al., 2006).”
From Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models (2011) · cites this paper as Smith et al., 2006

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Authors: Smith, M. A., Ghazizadeh, A., & Shadmehr, R.
Affiliations: Harvard University (US)
University of California, Berkeley (US)
Johns Hopkins University (US)
Corresponding author: Smith, Maurice A
ORCID: Smith, Maurice A
Ghazizadeh, Ali
Shadmehr, Reza
Venue: PLoS Biology
Publisher: Public Library of Science (PLoS)
Published: 2006-05-23
Volume: 4
Issue: 6
Pages: e179
ISSN: 1544-9173 (ISSN-L)
1545-7885
DOI: 10.1371/journal.pbio.0040179
PMC: PMC1463025
OpenAlex: W2028612696
Cited by: 1,113
References: 34
Citations by year: 2026: 54 · 2025: 57 · 2024: 69 · 2023: 61 · 2022: 63 · 2021: 74 · 2020: 79 · 2019: 65 · 2018: 70 · 2017: 55 · 2016: 59 · 2015: 70 · 2014: 52 · 2013: 54 · 2012: 48
FWCI: 12.46
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Biology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Figshare (submittedVersion, cc-by)
Funders: National Institute of Neurological Disorders and Stroke (NS16375, P01NS016375, NS 37422, R01NS037422, R56NS037422)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords: motor learning, motor adaptation, error feedback, spontaneous recovery, savings, reaching, neural systems
MeSH terms: Adaptation, Physiological, Adult, Humans, Learning, Models, Neurological, Motor Skills, Saccades, Time Factors

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Interacting adaptive processes with different timescales underlie short-term motor learning

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