Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation

Using the finger-to-thumb opposition sequence (FOS) learning task, we characterized motor skill learning in sub-acute patients hospitalized for rehabilitation following traumatic brain injury (TBI). Ten patients (Trained TBI) and 11 healthy participants (Trained Healthy) were trained using a multi-s...

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Main Authors: Maria Korman, Sharon Shaklai, Keren Cisamariu, Carmit Gal, Rinatia Maaravi-Hesseg, Ishay Levy, Ofer Keren, Avi Karni, Yaron Sacher
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-01-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fnhum.2018.00010/full
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author Maria Korman
Sharon Shaklai
Sharon Shaklai
Keren Cisamariu
Carmit Gal
Carmit Gal
Rinatia Maaravi-Hesseg
Ishay Levy
Ishay Levy
Ofer Keren
Ofer Keren
Avi Karni
Avi Karni
Avi Karni
Yaron Sacher
Yaron Sacher
author_facet Maria Korman
Sharon Shaklai
Sharon Shaklai
Keren Cisamariu
Carmit Gal
Carmit Gal
Rinatia Maaravi-Hesseg
Ishay Levy
Ishay Levy
Ofer Keren
Ofer Keren
Avi Karni
Avi Karni
Avi Karni
Yaron Sacher
Yaron Sacher
author_sort Maria Korman
collection DOAJ
description Using the finger-to-thumb opposition sequence (FOS) learning task, we characterized motor skill learning in sub-acute patients hospitalized for rehabilitation following traumatic brain injury (TBI). Ten patients (Trained TBI) and 11 healthy participants (Trained Healthy) were trained using a multi-session protocol: a single session was afforded in the first week of the study, and four daily sessions were afforded during the second week. Intensity of practice was adapted to patients. Performance speed and accuracy were tested before and after each session. Retention was tested 1 month later. Ten patients (Control TBI) had no FOS training and were tested only at the beginning and the end of the 6 week period. Although baseline performance on the FOS was very slow, all three phases of skill learning found in healthy adults (acquisition, between-session consolidation gains, and long-term retention) could be identified in patients with TBI. However, their time-course of learning was atypical. The Trained TBI group improved in speed about double the spontaneous improvements observed in the Control TBI group, with no speed-accuracy tradeoff. Normalized to their initial performance on the FOS, the gains accrued by the Trained TBI group after a first training were comparable to those accrued by healthy adults. Only during the second week with daily training, the rate of improvement of the Trained TBI group lagged behind that of the Trained Healthy group, due to increasing within-sessions losses in performance speed; no such losses were found in healthy participants. The Functional Independence Measure scores at the start of the study correlated with the total gains attained at the end of the study; no correlations were found with severity of injury or explicit memory impairments. Despite within-sessions losses in performance, which we propose reflect cognitive fatigue, training resulted in robust overall learning and long-term retention in patients with moderate-severe TBI. Given that the gains in performance evolved mainly between sessions, as delayed, offline, gains, our results suggest that memory consolidation processes can be effectively engaged in patients with TBI. However, practice protocols and schedules may need to be optimized to better engage the potential for long-term plasticity in these patients.
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spelling doaj.art-78a894a885a94b6d9c6bf08b270e05f82022-12-22T00:01:56ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-01-011210.3389/fnhum.2018.00010297546Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory ConsolidationMaria Korman0Sharon Shaklai1Sharon Shaklai2Keren Cisamariu3Carmit Gal4Carmit Gal5Rinatia Maaravi-Hesseg6Ishay Levy7Ishay Levy8Ofer Keren9Ofer Keren10Avi Karni11Avi Karni12Avi Karni13Yaron Sacher14Yaron Sacher15Edmond. J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Haifa, IsraelLoewenstein Rehabilitation Hospital, Ra'anana, IsraelSackler Medical Faculty, Tel-Aviv University, Tel Aviv, IsraelLoewenstein Rehabilitation Hospital, Ra'anana, IsraelEdmond. J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Haifa, IsraelSagol Department of Neurobiology, Brain–Behavior Research Center, University of Haifa, Haifa, IsraelSagol Department of Neurobiology, Brain–Behavior Research Center, University of Haifa, Haifa, IsraelEdmond. J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Haifa, IsraelSagol Department of Neurobiology, Brain–Behavior Research Center, University of Haifa, Haifa, IsraelSackler Medical Faculty, Tel-Aviv University, Tel Aviv, IsraelSheba Medical Center, Ramat Gan, IsraelEdmond. J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Haifa, IsraelSagol Department of Neurobiology, Brain–Behavior Research Center, University of Haifa, Haifa, IsraelSheba Medical Center, Ramat Gan, IsraelLoewenstein Rehabilitation Hospital, Ra'anana, IsraelSackler Medical Faculty, Tel-Aviv University, Tel Aviv, IsraelUsing the finger-to-thumb opposition sequence (FOS) learning task, we characterized motor skill learning in sub-acute patients hospitalized for rehabilitation following traumatic brain injury (TBI). Ten patients (Trained TBI) and 11 healthy participants (Trained Healthy) were trained using a multi-session protocol: a single session was afforded in the first week of the study, and four daily sessions were afforded during the second week. Intensity of practice was adapted to patients. Performance speed and accuracy were tested before and after each session. Retention was tested 1 month later. Ten patients (Control TBI) had no FOS training and were tested only at the beginning and the end of the 6 week period. Although baseline performance on the FOS was very slow, all three phases of skill learning found in healthy adults (acquisition, between-session consolidation gains, and long-term retention) could be identified in patients with TBI. However, their time-course of learning was atypical. The Trained TBI group improved in speed about double the spontaneous improvements observed in the Control TBI group, with no speed-accuracy tradeoff. Normalized to their initial performance on the FOS, the gains accrued by the Trained TBI group after a first training were comparable to those accrued by healthy adults. Only during the second week with daily training, the rate of improvement of the Trained TBI group lagged behind that of the Trained Healthy group, due to increasing within-sessions losses in performance speed; no such losses were found in healthy participants. The Functional Independence Measure scores at the start of the study correlated with the total gains attained at the end of the study; no correlations were found with severity of injury or explicit memory impairments. Despite within-sessions losses in performance, which we propose reflect cognitive fatigue, training resulted in robust overall learning and long-term retention in patients with moderate-severe TBI. Given that the gains in performance evolved mainly between sessions, as delayed, offline, gains, our results suggest that memory consolidation processes can be effectively engaged in patients with TBI. However, practice protocols and schedules may need to be optimized to better engage the potential for long-term plasticity in these patients.http://journal.frontiersin.org/article/10.3389/fnhum.2018.00010/fullprocedural learningmotor sequenceatypical consolidationtraining schedulelong-term memoryfatigue
spellingShingle Maria Korman
Sharon Shaklai
Sharon Shaklai
Keren Cisamariu
Carmit Gal
Carmit Gal
Rinatia Maaravi-Hesseg
Ishay Levy
Ishay Levy
Ofer Keren
Ofer Keren
Avi Karni
Avi Karni
Avi Karni
Yaron Sacher
Yaron Sacher
Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
Frontiers in Human Neuroscience
procedural learning
motor sequence
atypical consolidation
training schedule
long-term memory
fatigue
title Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
title_full Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
title_fullStr Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
title_full_unstemmed Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
title_short Atypical Within-Session Motor Procedural Learning after Traumatic Brain Injury but Well-Preserved Between-Session Procedural Memory Consolidation
title_sort atypical within session motor procedural learning after traumatic brain injury but well preserved between session procedural memory consolidation
topic procedural learning
motor sequence
atypical consolidation
training schedule
long-term memory
fatigue
url http://journal.frontiersin.org/article/10.3389/fnhum.2018.00010/full
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