Literature DB >> 33558432

Did We Get Sensorimotor Adaptation Wrong? Implicit Adaptation as Direct Policy Updating Rather than Forward-Model-Based Learning.

Alkis M Hadjiosif1, John W Krakauer2,3,4,5, Adrian M Haith2.   

Abstract

The human motor system can rapidly adapt its motor output in response to errors. The prevailing theory of this process posits that the motor system adapts an internal forward model that predicts the consequences of outgoing motor commands and uses this forward model to plan future movements. However, despite clear evidence that adaptive forward models exist and are used to help track the state of the body, there is no definitive evidence that such models are used in movement planning. An alternative to the forward-model-based theory of adaptation is that movements are generated based on a learned policy that is adjusted over time by movement errors directly ("direct policy learning"). This learning mechanism could act in parallel with, but independent of, any updates to a predictive forward model. Forward-model-based learning and direct policy learning generate very similar predictions about behavior in conventional adaptation paradigms. However, across three experiments with human participants (N = 47, 26 female), we show that these mechanisms can be dissociated based on the properties of implicit adaptation under mirror-reversed visual feedback. Although mirror reversal is an extreme perturbation, it still elicits implicit adaptation; however, this adaptation acts to amplify rather than to reduce errors. We show that the pattern of this adaptation over time and across targets is consistent with direct policy learning but not forward-model-based learning. Our findings suggest that the forward-model-based theory of adaptation needs to be re-examined and that direct policy learning provides a more plausible explanation of implicit adaptation.SIGNIFICANCE STATEMENT The ability of our brain to adapt movements in response to error is one of the most widely studied phenomena in motor learning. Yet, we still do not know the process by which errors eventually result in adaptation. It is known that the brain maintains and updates an internal forward model, which predicts the consequences of motor commands, and the prevailing theory of motor adaptation posits that this updated forward model is responsible for trial-by-trial adaptive changes. Here, we question this view and show instead that adaptation is better explained by a simpler process whereby motor output is directly adjusted by task errors. Our findings cast doubt on long-held beliefs about adaptation.
Copyright © 2021 the authors.

Entities:  

Keywords:  control policy; distal learning; forward model; mirror reversal; motor adaptation; motor learning

Year:  2021        PMID: 33558432      PMCID: PMC8018745          DOI: 10.1523/JNEUROSCI.2125-20.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  65 in total

1.  Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control.

Authors:  Opher Donchin; Joseph T Francis; Reza Shadmehr
Journal:  J Neurosci       Date:  2003-10-08       Impact factor: 6.167

2.  Rapid online correction is selectively suppressed during movement with a visuomotor transformation.

Authors:  V Gritsenko; J F Kalaska
Journal:  J Neurophysiol       Date:  2010-09-15       Impact factor: 2.714

3.  Generalization as a behavioral window to the neural mechanisms of learning internal models.

Authors:  Reza Shadmehr
Journal:  Hum Mov Sci       Date:  2004-11       Impact factor: 2.161

4.  The influence of movement preparation time on the expression of visuomotor learning and savings.

Authors:  Adrian M Haith; David M Huberdeau; John W Krakauer
Journal:  J Neurosci       Date:  2015-04-01       Impact factor: 6.167

5.  Explicit and implicit contributions to learning in a sensorimotor adaptation task.

Authors:  Jordan A Taylor; John W Krakauer; Richard B Ivry
Journal:  J Neurosci       Date:  2014-02-19       Impact factor: 6.167

6.  Sensitivity derivatives for flexible sensorimotor learning.

Authors:  M N Abdelghani; T P Lillicrap; D B Tweed
Journal:  Neural Comput       Date:  2008-08       Impact factor: 2.026

7.  Learning course adjustments during arm movements with reversed sensitivity derivatives.

Authors:  Mohamed N Abdelghani; Douglas B Tweed
Journal:  BMC Neurosci       Date:  2010-11-26       Impact factor: 3.288

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

Authors:  Maurice A Smith; Ali Ghazizadeh; Reza Shadmehr
Journal:  PLoS Biol       Date:  2006-05-23       Impact factor: 8.029

9.  Unlearning versus savings in visuomotor adaptation: comparing effects of washout, passage of time, and removal of errors on motor memory.

Authors:  Tomoko Kitago; Sophia L Ryan; Pietro Mazzoni; John W Krakauer; Adrian M Haith
Journal:  Front Hum Neurosci       Date:  2013-06-28       Impact factor: 3.169

10.  Invariant errors reveal limitations in motor correction rather than constraints on error sensitivity.

Authors:  Hyosub E Kim; J Ryan Morehead; Darius E Parvin; Reza Moazzezi; Richard B Ivry
Journal:  Commun Biol       Date:  2018-03-22
View more
  11 in total

1.  Response-based outcome predictions and confidence regulate feedback processing and learning.

Authors:  Romy Frömer; Matthew R Nassar; Rasmus Bruckner; Birgit Stürmer; Werner Sommer; Nick Yeung
Journal:  Elife       Date:  2021-04-30       Impact factor: 8.140

2.  Implicit adaptation to mirror reversal is in the correct coordinate system but the wrong direction.

Authors:  Tianhe Wang; Jordan A Taylor
Journal:  J Neurophysiol       Date:  2021-10-06       Impact factor: 2.714

Review 3.  How learning unfolds in the brain: toward an optimization view.

Authors:  Jay A Hennig; Emily R Oby; Darby M Losey; Aaron P Batista; Byron M Yu; Steven M Chase
Journal:  Neuron       Date:  2021-10-13       Impact factor: 17.173

4.  Motor learning without movement.

Authors:  Olivia A Kim; Alexander D Forrence; Samuel D McDougle
Journal:  Proc Natl Acad Sci U S A       Date:  2022-07-19       Impact factor: 12.779

5.  Evidence for an internal model of friction when controlling kinetic energy at impact to slide an object along a surface toward a target.

Authors:  Sylvain Famié; Mehdi Ammi; Vincent Bourdin; Michel-Ange Amorim
Journal:  PLoS One       Date:  2022-02-24       Impact factor: 3.240

6.  De novo learning versus adaptation of continuous control in a manual tracking task.

Authors:  Christopher S Yang; Noah J Cowan; Adrian M Haith
Journal:  Elife       Date:  2021-06-25       Impact factor: 8.140

7.  Speech auditory-motor adaptation to formant-shifted feedback lacks an explicit component: Reduced adaptation in adults who stutter reflects limitations in implicit sensorimotor learning.

Authors:  Kwang S Kim; Ludo Max
Journal:  Eur J Neurosci       Date:  2021-04-10       Impact factor: 3.386

8.  Revisiting the Role of the Medial Temporal Lobe in Motor Learning.

Authors:  Samuel D McDougle; Sarah A Wilterson; Nicholas B Turk-Browne; Jordan A Taylor
Journal:  J Cogn Neurosci       Date:  2022-02-01       Impact factor: 3.225

9.  Long-Term Motor Learning in the "Wild" With High Volume Video Game Data.

Authors:  Jennifer B Listman; Jonathan S Tsay; Hyosub E Kim; Wayne E Mackey; David J Heeger
Journal:  Front Hum Neurosci       Date:  2021-12-20       Impact factor: 3.169

10.  A single exposure to altered auditory feedback causes observable sensorimotor adaptation in speech.

Authors:  Lana Hantzsch; Benjamin Parrell; Caroline A Niziolek
Journal:  Elife       Date:  2022-07-11       Impact factor: 8.713

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.