Literature DB >> 26204232

Online feedback enhances early consolidation of motor sequence learning and reverses recall deficit from transcranial stimulation of motor cortex.

Leonora Wilkinson1, Adam Steel2, Eric Mooshagian3, Trelawny Zimmermann4, Aysha Keisler5, Jeffrey D Lewis6, Eric M Wassermann7.   

Abstract

Feedback and monetary reward can enhance motor skill learning, suggesting reward system involvement. Continuous theta burst (cTBS) transcranial magnetic stimulation (TMS) of the primary motor area (M1) disrupts processing, reduces excitability and impairs motor learning. To see whether feedback and reward can overcome the learning impairment associated with M1 cTBS, we delivered real or sham stimulation to two groups of participants before they performed a motor sequence learning task with and without feedback. Participants were trained on two intermixed sequences, one occurring 85% of the time (the "probable" sequence) and the other 15% of the time (the "improbable" sequence). We measured sequence learning as the difference in reaction time (RT) and error rate between probable and improbable trials (RT and error difference scores). Participants were also tested for sequence recall with the same indices of learning 60 min after cTBS. Real stimulation impaired initial sequence learning and sequence knowledge recall as measured by error difference scores and impaired sequence knowledge recall as measured by RT difference score. Relative to non-feedback learning, the introduction of feedback during sequence learning improved subsequent sequence knowledge recall indexed by RT difference score, in both real and sham stimulation groups and feedback reversed the RT difference score based sequence knowledge recall impairment from real cTBS that we observed in the non-feedback learning condition. Only the real cTBS group in the non-feedback condition showed no evidence of explicit sequence knowledge when tested at the end of the study. Feedback improves recall of implicit and explicit motor sequence knowledge and can protect sequence knowledge against the effect of M1 inhibition. Adding feedback and monetary reward/punishment to motor skill learning may help overcome retention impairments or accelerate training in clinical and other settings. Published by Elsevier Ltd.

Entities:  

Keywords:  Consolidation; Motor cortex; Motor skill; Sequence learning; Serial reaction time task; Theta burst stimulation

Mesh:

Year:  2015        PMID: 26204232      PMCID: PMC4575846          DOI: 10.1016/j.cortex.2015.06.012

Source DB:  PubMed          Journal:  Cortex        ISSN: 0010-9452            Impact factor:   4.027


  61 in total

1.  A safety screening questionnaire for transcranial magnetic stimulation.

Authors:  J C Keel; M J Smith; E M Wassermann
Journal:  Clin Neurophysiol       Date:  2001-04       Impact factor: 3.708

2.  Direct comparison of neural systems mediating conscious and unconscious skill learning.

Authors:  Daniel B Willingham; Joanna Salidis; John D E Gabrieli
Journal:  J Neurophysiol       Date:  2002-09       Impact factor: 2.714

3.  Functional mapping of sequence learning in normal humans.

Authors:  S T Grafton; E Hazeltine; R Ivry
Journal:  J Cogn Neurosci       Date:  1995       Impact factor: 3.225

4.  Basal ganglia-dependent processes in recalling learned visual-motor adaptations.

Authors:  Patrick Bédard; Jerome N Sanes
Journal:  Exp Brain Res       Date:  2011-02-11       Impact factor: 1.972

5.  An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning.

Authors:  Haline E Schendan; Meghan M Searl; Rebecca J Melrose; Chantal E Stern
Journal:  Neuron       Date:  2003-03-27       Impact factor: 17.173

6.  Altered bidirectional plasticity and reduced implicit motor learning in concussed athletes.

Authors:  Louis De Beaumont; Sébastien Tremblay; Judes Poirier; Maryse Lassonde; Hugo Théoret
Journal:  Cereb Cortex       Date:  2011-05-13       Impact factor: 5.357

7.  Learning sequence movements in a homogenous sample of patients with Parkinson's disease.

Authors:  Natacha Deroost; Eric Kerckhofs; Maya Coene; Geert Wijnants; Eric Soetens
Journal:  Neuropsychologia       Date:  2006-05-03       Impact factor: 3.139

8.  Response-dependent contributions of human primary motor cortex and angular gyrus to manual and perceptual sequence learning.

Authors:  Clive R Rosenthal; Emma E Roche-Kelly; Masud Husain; Christopher Kennard
Journal:  J Neurosci       Date:  2009-12-02       Impact factor: 6.167

9.  Intentional control and implicit sequence learning.

Authors:  Leonora Wilkinson; David R Shanks
Journal:  J Exp Psychol Learn Mem Cogn       Date:  2004-03       Impact factor: 3.051

10.  Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology.

Authors:  D Shohamy; C E Myers; S Grossman; J Sage; M A Gluck; R A Poldrack
Journal:  Brain       Date:  2004-03-10       Impact factor: 13.501

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  7 in total

1.  Motor cortex inhibition by TMS reduces cognitive non-motor procedural learning when immediate incentives are present.

Authors:  Leonora Wilkinson; Philip J Koshy; Adam Steel; Devin Bageac; Selene Schintu; Eric M Wassermann
Journal:  Cortex       Date:  2017-10-06       Impact factor: 4.027

2.  Shifts in connectivity during procedural learning after motor cortex stimulation: A combined transcranial magnetic stimulation/functional magnetic resonance imaging study.

Authors:  Adam Steel; Sunbin Song; Devin Bageac; Kristine M Knutson; Aysha Keisler; Ziad S Saad; Stephen J Gotts; Eric M Wassermann; Leonora Wilkinson
Journal:  Cortex       Date:  2015-10-23       Impact factor: 4.027

3.  The impact of reward and punishment on skill learning depends on task demands.

Authors:  Adam Steel; Edward H Silson; Charlotte J Stagg; Chris I Baker
Journal:  Sci Rep       Date:  2016-10-27       Impact factor: 4.379

4.  Pharmacological Dopamine Manipulation Does Not Alter Reward-Based Improvements in Memory Retention during a Visuomotor Adaptation Task.

Authors:  Graziella Quattrocchi; Jessica Monaco; Andy Ho; Friederike Irmen; Wolfgang Strube; Diane Ruge; Sven Bestmann; Joseph M Galea
Journal:  eNeuro       Date:  2018-07-16

5.  Beyond Motor Noise: Considering Other Causes of Impaired Reinforcement Learning in Cerebellar Patients.

Authors:  Pierre Vassiliadis; Gerard Derosiere; Julie Duque
Journal:  eNeuro       Date:  2019-02-22

6.  Persistent Enhancement of Hippocampal Network Connectivity by Parietal rTMS Is Reproducible.

Authors:  Michael Freedberg; Jack A Reeves; Andrew C Toader; Molly S Hermiller; Joel L Voss; Eric M Wassermann
Journal:  eNeuro       Date:  2019-10-16

7.  Reward boosts reinforcement-based motor learning.

Authors:  Pierre Vassiliadis; Gerard Derosiere; Cecile Dubuc; Aegryan Lete; Frederic Crevecoeur; Friedhelm C Hummel; Julie Duque
Journal:  iScience       Date:  2021-07-07
  7 in total

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