Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems
It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional...
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| Veröffentlicht in: | NeuroImage (Orlando, Fla.) Fla.), 2015-03, Vol.108, p.423-434 |
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| creator | Albouy, Genevieve Fogel, Stuart King, Bradley R. Laventure, Samuel Benali, Habib Karni, Avi Carrier, Julie Robertson, Edwin M. Doyon, Julien |
| description | It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.
•Hippocampus and striatum support spatial and motor components of sequence learning.•Hippocampus supports sleep-dependent enhancement in motor sequence performance.•Striatum supports time-dependent maintenance in motor sequence performance.•Hippocampus and striatum show antagonist relationship with memory consolidation. |
| doi_str_mv | 10.1016/j.neuroimage.2014.12.049 |
| format | Article |
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•Hippocampus and striatum support spatial and motor components of sequence learning.•Hippocampus supports sleep-dependent enhancement in motor sequence performance.•Striatum supports time-dependent maintenance in motor sequence performance.•Hippocampus and striatum show antagonist relationship with memory consolidation.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2014.12.049</identifier><identifier>PMID: 25542533</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animal memory ; Consolidation ; Corpus Striatum - physiology ; Female ; Hippocampus ; Hippocampus - physiology ; Humans ; Magnetic resonance imaging ; Male ; Memory - physiology ; Memory consolidation ; Motor sequence learning ; Motors ; Networks ; Neural networks ; Performance enhancement ; Representations ; Sleep ; Striatum ; Wakefulness ; Wakes ; Young Adult</subject><ispartof>NeuroImage (Orlando, Fla.), 2015-03, Vol.108, p.423-434</ispartof><rights>2014 Elsevier Inc.</rights><rights>Copyright © 2014 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Mar 1, 2015</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c538t-63a3d6f608e857523f38537d1b30d3af53991bf95c0a4641d3ddf181ab7ae6673</citedby><cites>FETCH-LOGICAL-c538t-63a3d6f608e857523f38537d1b30d3af53991bf95c0a4641d3ddf181ab7ae6673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/1652788741?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25542533$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Albouy, Genevieve</creatorcontrib><creatorcontrib>Fogel, Stuart</creatorcontrib><creatorcontrib>King, Bradley R.</creatorcontrib><creatorcontrib>Laventure, Samuel</creatorcontrib><creatorcontrib>Benali, Habib</creatorcontrib><creatorcontrib>Karni, Avi</creatorcontrib><creatorcontrib>Carrier, Julie</creatorcontrib><creatorcontrib>Robertson, Edwin M.</creatorcontrib><creatorcontrib>Doyon, Julien</creatorcontrib><title>Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.
•Hippocampus and striatum support spatial and motor components of sequence learning.•Hippocampus supports sleep-dependent enhancement in motor sequence performance.•Striatum supports time-dependent maintenance in motor sequence performance.•Hippocampus and striatum show antagonist relationship with memory consolidation.</description><subject>Animal memory</subject><subject>Consolidation</subject><subject>Corpus Striatum - physiology</subject><subject>Female</subject><subject>Hippocampus</subject><subject>Hippocampus - physiology</subject><subject>Humans</subject><subject>Magnetic resonance imaging</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Memory consolidation</subject><subject>Motor sequence learning</subject><subject>Motors</subject><subject>Networks</subject><subject>Neural networks</subject><subject>Performance enhancement</subject><subject>Representations</subject><subject>Sleep</subject><subject>Striatum</subject><subject>Wakefulness</subject><subject>Wakes</subject><subject>Young Adult</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkUuL1TAUgIsozjj6FyTgxk1rTtO83OmgzsCIILoOucnpnVzapibthfn3k3JHBTfOIiQHvpPz-KqKAG2Agnh3aCZcUwyj3WPTUugaaBva6SfVOVDNa81l-3R7c1YrAH1Wvcj5QCnV0Knn1VnLeddyxs6r_VcbpqWcMO3JMTcEp1s7uS0a4xITyfhrxckhGXGMKWB-T75jntEt4YgkxQEziT3JSwp2sQOxkye3YZ6js-Nc4nyXFxzzy-pZb4eMrx7ui-rn508_Lq_qm29fri8_3NSOM7XUglnmRS-oQsUlb1nPFGfSw45Rz2zPmdaw6zV31HaiA8-870GB3UmLQkh2Ub09_TunWBrPixlDdjgMdsK4ZgNCSs20oOwRqKAddJTxR6CcQStAiYK--Qc9xDVNZeaNaqVSsoNCqRPlUsw5YW_mVGymOwPUbIrNwfxVbDbFBlpTFJfU1w8F1t2I_k_ib6cF-HgCsOz5GDCZ7MKm0IdUtBkfw_-r3AP6lLxl</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Albouy, Genevieve</creator><creator>Fogel, Stuart</creator><creator>King, Bradley R.</creator><creator>Laventure, Samuel</creator><creator>Benali, Habib</creator><creator>Karni, Avi</creator><creator>Carrier, Julie</creator><creator>Robertson, Edwin M.</creator><creator>Doyon, Julien</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>7QO</scope><scope>7TB</scope><scope>7U5</scope><scope>L7M</scope></search><sort><creationdate>20150301</creationdate><title>Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems</title><author>Albouy, Genevieve ; Fogel, Stuart ; King, Bradley R. ; Laventure, Samuel ; Benali, Habib ; Karni, Avi ; Carrier, Julie ; Robertson, Edwin M. ; Doyon, Julien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c538t-63a3d6f608e857523f38537d1b30d3af53991bf95c0a4641d3ddf181ab7ae6673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animal memory</topic><topic>Consolidation</topic><topic>Corpus Striatum - 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Academic</collection><collection>Biotechnology Research Abstracts</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Albouy, Genevieve</au><au>Fogel, Stuart</au><au>King, Bradley R.</au><au>Laventure, Samuel</au><au>Benali, Habib</au><au>Karni, Avi</au><au>Carrier, Julie</au><au>Robertson, Edwin M.</au><au>Doyon, Julien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>108</volume><spage>423</spage><epage>434</epage><pages>423-434</pages><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.
•Hippocampus and striatum support spatial and motor components of sequence learning.•Hippocampus supports sleep-dependent enhancement in motor sequence performance.•Striatum supports time-dependent maintenance in motor sequence performance.•Hippocampus and striatum show antagonist relationship with memory consolidation.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25542533</pmid><doi>10.1016/j.neuroimage.2014.12.049</doi><tpages>12</tpages></addata></record> |
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| subjects | Animal memory Consolidation Corpus Striatum - physiology Female Hippocampus Hippocampus - physiology Humans Magnetic resonance imaging Male Memory - physiology Memory consolidation Motor sequence learning Motors Networks Neural networks Performance enhancement Representations Sleep Striatum Wakefulness Wakes Young Adult |
| title | Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems |
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