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Neural mechanisms underlying improved new-word learning with high-density transcranial direct current stimulation
•Anodal HD-tDCS facilitated verb learning.•Enhanced connectivity between IFG and TPJ improved verb learning.•Robust word learning linked to enhanced network interactions.•Behavioral activation of one area and tDCS of another area can induce network modulation. Neurobehavioral studies have provided e...
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description | •Anodal HD-tDCS facilitated verb learning.•Enhanced connectivity between IFG and TPJ improved verb learning.•Robust word learning linked to enhanced network interactions.•Behavioral activation of one area and tDCS of another area can induce network modulation.
Neurobehavioral studies have provided evidence for the effectiveness of anodal tDCS on language production, by stimulation of the left Inferior Frontal Gyrus (IFG) or of left Temporo-Parietal Junction (TPJ). However, tDCS is currently not used in clinical practice outside of trials, because behavioral effects have been inconsistent and underlying neural effects unclear. Here, we propose to elucidate the neural correlates of verb and noun learning and to determine if they can be modulated with anodal high-definition (HD) tDCS stimulation. Thirty-six neurotypical participants were randomly allocated to anodal HD-tDCS over either the left IFG, the left TPJ, or sham stimulation. On day one, participants performed a naming task (pre-test). On day two, participants underwent a new-word learning task with rare nouns and verbs concurrently to HD-tDCS for 20 min. The third day consisted of a post-test of naming performance. EEG was recorded at rest and during naming on each day. Verb learning was significantly facilitated by left IFG stimulation. HD-tDCS over the left IFG enhanced functional connectivity between the left IFG and TPJ and this correlated with improved learning. HD-tDCS over the left TPJ enabled stronger local activation of the stimulated area (as indexed by greater alpha and beta-band power decrease) during naming, but this did not translate into better learning. Thus, tDCS can induce local activation or modulation of network interactions. Only the enhancement of network interactions, but not the increase in local activation, leads to robust improvement of word learning. This emphasizes the need to develop new neuromodulation methods influencing network interactions. Our study suggests that this may be achieved through behavioral activation of one area and concomitant activation of another area with HD-tDCS. |
doi_str_mv | 10.1016/j.neuroimage.2024.120649 |
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Neurobehavioral studies have provided evidence for the effectiveness of anodal tDCS on language production, by stimulation of the left Inferior Frontal Gyrus (IFG) or of left Temporo-Parietal Junction (TPJ). However, tDCS is currently not used in clinical practice outside of trials, because behavioral effects have been inconsistent and underlying neural effects unclear. Here, we propose to elucidate the neural correlates of verb and noun learning and to determine if they can be modulated with anodal high-definition (HD) tDCS stimulation. Thirty-six neurotypical participants were randomly allocated to anodal HD-tDCS over either the left IFG, the left TPJ, or sham stimulation. On day one, participants performed a naming task (pre-test). On day two, participants underwent a new-word learning task with rare nouns and verbs concurrently to HD-tDCS for 20 min. The third day consisted of a post-test of naming performance. EEG was recorded at rest and during naming on each day. Verb learning was significantly facilitated by left IFG stimulation. HD-tDCS over the left IFG enhanced functional connectivity between the left IFG and TPJ and this correlated with improved learning. HD-tDCS over the left TPJ enabled stronger local activation of the stimulated area (as indexed by greater alpha and beta-band power decrease) during naming, but this did not translate into better learning. Thus, tDCS can induce local activation or modulation of network interactions. Only the enhancement of network interactions, but not the increase in local activation, leads to robust improvement of word learning. This emphasizes the need to develop new neuromodulation methods influencing network interactions. Our study suggests that this may be achieved through behavioral activation of one area and concomitant activation of another area with HD-tDCS.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2024.120649</identifier><identifier>PMID: 38759354</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Aphasia ; Clinical trials ; Educational activities ; Electrical stimulation of the brain ; Electroencephalography - methods ; ESB ; Female ; Frontal gyrus ; Functional connectivity (FC) ; Humans ; Language ; Learning ; Learning - physiology ; Left inferior frontal gyrus (IFG) ; Left temporo-parietal junction (TPJ) ; Male ; Naming ; Neural networks ; Neuromodulation ; New-word learning ; Nouns ; Parietal Lobe - physiology ; Phonology ; Prefrontal Cortex - physiology ; Stroke ; Temporal Lobe - physiology ; Transcranial direct current stimulation ; Transcranial direct current stimulation (tDCS) ; Transcranial Direct Current Stimulation - methods ; Verbal Learning - physiology ; Verbs ; Vocabulary learning ; Young Adult</subject><ispartof>NeuroImage (Orlando, Fla.), 2024-07, Vol.294, p.120649-120649, Article 120649</ispartof><rights>2024</rights><rights>Copyright © 2024. Published by Elsevier Inc.</rights><rights>Copyright Elsevier Limited Jul 1, 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c463t-3b9601e4b23df26d9843fa00ec4588d52b496a19a5642d04e373342c936dd03c3</cites><orcidid>0000-0002-4054-0939 ; 0000-0003-4708-9201 ; 0000-0001-7178-7793 ; 0000-0001-5878-212X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,12831,27903,27904,31248</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38759354$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Farcy, Camille</creatorcontrib><creatorcontrib>Chauvigné, Lea A.S.</creatorcontrib><creatorcontrib>Laganaro, Marina</creatorcontrib><creatorcontrib>Corre, Marion</creatorcontrib><creatorcontrib>Ptak, Radek</creatorcontrib><creatorcontrib>Guggisberg, Adrian G.</creatorcontrib><title>Neural mechanisms underlying improved new-word learning with high-density transcranial direct current stimulation</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>•Anodal HD-tDCS facilitated verb learning.•Enhanced connectivity between IFG and TPJ improved verb learning.•Robust word learning linked to enhanced network interactions.•Behavioral activation of one area and tDCS of another area can induce network modulation.
Neurobehavioral studies have provided evidence for the effectiveness of anodal tDCS on language production, by stimulation of the left Inferior Frontal Gyrus (IFG) or of left Temporo-Parietal Junction (TPJ). However, tDCS is currently not used in clinical practice outside of trials, because behavioral effects have been inconsistent and underlying neural effects unclear. Here, we propose to elucidate the neural correlates of verb and noun learning and to determine if they can be modulated with anodal high-definition (HD) tDCS stimulation. Thirty-six neurotypical participants were randomly allocated to anodal HD-tDCS over either the left IFG, the left TPJ, or sham stimulation. On day one, participants performed a naming task (pre-test). On day two, participants underwent a new-word learning task with rare nouns and verbs concurrently to HD-tDCS for 20 min. The third day consisted of a post-test of naming performance. EEG was recorded at rest and during naming on each day. Verb learning was significantly facilitated by left IFG stimulation. HD-tDCS over the left IFG enhanced functional connectivity between the left IFG and TPJ and this correlated with improved learning. HD-tDCS over the left TPJ enabled stronger local activation of the stimulated area (as indexed by greater alpha and beta-band power decrease) during naming, but this did not translate into better learning. Thus, tDCS can induce local activation or modulation of network interactions. Only the enhancement of network interactions, but not the increase in local activation, leads to robust improvement of word learning. This emphasizes the need to develop new neuromodulation methods influencing network interactions. Our study suggests that this may be achieved through behavioral activation of one area and concomitant activation of another area with HD-tDCS.</description><subject>Adult</subject><subject>Aphasia</subject><subject>Clinical trials</subject><subject>Educational activities</subject><subject>Electrical stimulation of the brain</subject><subject>Electroencephalography - methods</subject><subject>ESB</subject><subject>Female</subject><subject>Frontal gyrus</subject><subject>Functional connectivity (FC)</subject><subject>Humans</subject><subject>Language</subject><subject>Learning</subject><subject>Learning - physiology</subject><subject>Left inferior frontal gyrus (IFG)</subject><subject>Left temporo-parietal junction (TPJ)</subject><subject>Male</subject><subject>Naming</subject><subject>Neural networks</subject><subject>Neuromodulation</subject><subject>New-word learning</subject><subject>Nouns</subject><subject>Parietal Lobe - physiology</subject><subject>Phonology</subject><subject>Prefrontal Cortex - 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methods</topic><topic>ESB</topic><topic>Female</topic><topic>Frontal gyrus</topic><topic>Functional connectivity (FC)</topic><topic>Humans</topic><topic>Language</topic><topic>Learning</topic><topic>Learning - physiology</topic><topic>Left inferior frontal gyrus (IFG)</topic><topic>Left temporo-parietal junction (TPJ)</topic><topic>Male</topic><topic>Naming</topic><topic>Neural networks</topic><topic>Neuromodulation</topic><topic>New-word learning</topic><topic>Nouns</topic><topic>Parietal Lobe - physiology</topic><topic>Phonology</topic><topic>Prefrontal Cortex - physiology</topic><topic>Stroke</topic><topic>Temporal Lobe - physiology</topic><topic>Transcranial direct current stimulation</topic><topic>Transcranial direct current stimulation (tDCS)</topic><topic>Transcranial Direct Current Stimulation - methods</topic><topic>Verbal Learning - physiology</topic><topic>Verbs</topic><topic>Vocabulary learning</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Farcy, Camille</creatorcontrib><creatorcontrib>Chauvigné, Lea A.S.</creatorcontrib><creatorcontrib>Laganaro, Marina</creatorcontrib><creatorcontrib>Corre, Marion</creatorcontrib><creatorcontrib>Ptak, Radek</creatorcontrib><creatorcontrib>Guggisberg, Adrian G.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Linguistics and Language Behavior Abstracts (LLBA)</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Databases</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Psychology Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>DOAJ: Directory of Open Access Journals</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Farcy, Camille</au><au>Chauvigné, Lea A.S.</au><au>Laganaro, Marina</au><au>Corre, Marion</au><au>Ptak, Radek</au><au>Guggisberg, Adrian G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural mechanisms underlying improved new-word learning with high-density transcranial direct current stimulation</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2024-07-01</date><risdate>2024</risdate><volume>294</volume><spage>120649</spage><epage>120649</epage><pages>120649-120649</pages><artnum>120649</artnum><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>•Anodal HD-tDCS facilitated verb learning.•Enhanced connectivity between IFG and TPJ improved verb learning.•Robust word learning linked to enhanced network interactions.•Behavioral activation of one area and tDCS of another area can induce network modulation.
Neurobehavioral studies have provided evidence for the effectiveness of anodal tDCS on language production, by stimulation of the left Inferior Frontal Gyrus (IFG) or of left Temporo-Parietal Junction (TPJ). However, tDCS is currently not used in clinical practice outside of trials, because behavioral effects have been inconsistent and underlying neural effects unclear. Here, we propose to elucidate the neural correlates of verb and noun learning and to determine if they can be modulated with anodal high-definition (HD) tDCS stimulation. Thirty-six neurotypical participants were randomly allocated to anodal HD-tDCS over either the left IFG, the left TPJ, or sham stimulation. On day one, participants performed a naming task (pre-test). On day two, participants underwent a new-word learning task with rare nouns and verbs concurrently to HD-tDCS for 20 min. The third day consisted of a post-test of naming performance. EEG was recorded at rest and during naming on each day. Verb learning was significantly facilitated by left IFG stimulation. HD-tDCS over the left IFG enhanced functional connectivity between the left IFG and TPJ and this correlated with improved learning. HD-tDCS over the left TPJ enabled stronger local activation of the stimulated area (as indexed by greater alpha and beta-band power decrease) during naming, but this did not translate into better learning. Thus, tDCS can induce local activation or modulation of network interactions. Only the enhancement of network interactions, but not the increase in local activation, leads to robust improvement of word learning. This emphasizes the need to develop new neuromodulation methods influencing network interactions. Our study suggests that this may be achieved through behavioral activation of one area and concomitant activation of another area with HD-tDCS.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>38759354</pmid><doi>10.1016/j.neuroimage.2024.120649</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-4054-0939</orcidid><orcidid>https://orcid.org/0000-0003-4708-9201</orcidid><orcidid>https://orcid.org/0000-0001-7178-7793</orcidid><orcidid>https://orcid.org/0000-0001-5878-212X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Aphasia Clinical trials Educational activities Electrical stimulation of the brain Electroencephalography - methods ESB Female Frontal gyrus Functional connectivity (FC) Humans Language Learning Learning - physiology Left inferior frontal gyrus (IFG) Left temporo-parietal junction (TPJ) Male Naming Neural networks Neuromodulation New-word learning Nouns Parietal Lobe - physiology Phonology Prefrontal Cortex - physiology Stroke Temporal Lobe - physiology Transcranial direct current stimulation Transcranial direct current stimulation (tDCS) Transcranial Direct Current Stimulation - methods Verbal Learning - physiology Verbs Vocabulary learning Young Adult |
title | Neural mechanisms underlying improved new-word learning with high-density transcranial direct current stimulation |
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