Consolidation of human skill linked to waking hippocampo-neocortical replay

被引:63
作者
Buch, Ethan R. [1 ]
Claudino, Leonardo [1 ,2 ]
Quentin, Romain [1 ,3 ]
Bonstrup, Marlene [1 ,4 ]
Cohen, Leonardo G. [1 ]
机构
[1] NINDS, Human Cort Physiol & Neurorehabil Sect, NIH, Bldg 36,Rm 4D04, Bethesda, MD 20892 USA
[2] NIMH, Sect Neurobiol Fear & Anxiety, NIH, Bethesda, MD 20892 USA
[3] Univ Claude Bernard Lyon 1, Lyon Neurosci Res Ctr CRNL, INSERM U1028, CNRS,UMR5292, Lyon, France
[4] Univ Leipzig, Dept Neurol, Med Ctr, Leipzig, Germany
关键词
MEDIAL TEMPORAL-LOBE; MEMORY CONSOLIDATION; MOTOR IMAGERY; PERFORMANCE; EXPERIENCES; SEQUENCES; MULTIPLE; CORTEX; SPACE;
D O I
10.1016/j.celrep.2021.109193
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
The introduction of rest intervals interspersed with practice strengthens wakeful consolidation of skill. The mechanisms by which the brain binds discrete action representations into consolidated, highly temporally resolved skill sequences during waking rest are not known. To address this question, we recorded magnetoencephalography (MEG) during acquisition and rapid consolidation of a sequential motor skill. We report the presence of prominent, fast waking neural replay during the same rest periods in which rapid consolidation occurs. The observed replay is temporally compressed by approximately 20-fold relative to the acquired skill, is selective for the trained sequence, and predicts the magnitude of skill consolidation. Replay representations extend beyond the hippocampus and entorhinal cortex to the contralateral sensorimotor cortex. These results document the presence of robust hippocampo-neocortical replay supporting rapid wakeful consolidation of skill.
引用
收藏
页数:13
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共 54 条
[1]   Machine learning for neuroirnaging with scikit-learn [J].
Abraham, Alexandre ;
Pedregosa, Fabian ;
Eickenberg, Michael ;
Gervais, Philippe ;
Mueller, Andreas ;
Kossaifi, Jean ;
Gramfort, Alexandre ;
Thirion, Bertrand ;
Varoquaux, Gael .
FRONTIERS IN NEUROINFORMATICS, 2014, 8
[2]   Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems [J].
Albouy, Genevieve ;
Fogel, Stuart ;
King, Bradley R. ;
Laventure, Samuel ;
Benali, Habib ;
Karni, Avi ;
Carrier, Julie ;
Robertson, Edwin M. ;
Doyon, Julien .
NEUROIMAGE, 2015, 108 :423-434
[3]   MEMORY CONSOLIDATION AND THE MEDIAL TEMPORAL-LOBE - A SIMPLE NETWORK MODEL [J].
ALVAREZ, P ;
SQUIRE, LR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1994, 91 (15) :7041-7045
[4]   What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior [J].
Behrens, Timothy E. J. ;
Muller, Timothy H. ;
Whittington, James C. R. ;
Mark, Shirley ;
Baram, Alon B. ;
Stachenfeld, Kimberly L. ;
Kurth-Nelson, Zeb .
NEURON, 2018, 100 (02) :490-509
[5]   A Rapid Form of Offline Consolidation in Skill Learning [J].
Boenstrup, Marlene ;
Iturrate, Inaki ;
Thompson, Ryan ;
Cruciani, Gabriel ;
Censor, Nitzan ;
Cohen, Leonardo G. .
CURRENT BIOLOGY, 2019, 29 (08) :1346-+
[6]   Mechanisms of offline motor learning at a microscale of seconds in large-scale crowdsourced data [J].
Bonstrup, Marlene ;
Iturrate, Inaki ;
Hebart, Martin N. ;
Censor, Nitzan ;
Cohen, Leonardo G. .
NPJ SCIENCE OF LEARNING, 2020, 5 (01)
[7]   Space and Time: The Hippocampus as a Sequence Generator [J].
Buzsaki, Gyorgy ;
Tingley, David .
TRENDS IN COGNITIVE SCIENCES, 2018, 22 (10) :853-869
[8]   Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval [J].
Carr, Margaret F. ;
Jadhav, Shantanu P. ;
Frank, Loren M. .
NATURE NEUROSCIENCE, 2011, 14 (02) :147-153
[9]   The Binding of Learning to Action in Motor Adaptation [J].
Castro, Luis Nicolas Gonzalez ;
Monsen, Craig Bryant ;
Smith, Maurice A. .
PLOS COMPUTATIONAL BIOLOGY, 2011, 7 (06)
[10]   Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories [J].
Censor, Nitzan ;
Dayan, Eran ;
Cohen, Leonardo G. .
CORTEX, 2014, 58 :281-288