Oscillatory correlates of auditory working memory examined with human electrocorticography
This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in audit...
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Veröffentlicht in: | Neuropsychologia 2021-01, Vol.150, p.107691-107691, Article 107691 |
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description | This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschl’s gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior- and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. This work demonstrates sustained activity patterns during AWM maintenance, with prominent low-frequency increases in medial temporal lobe regions.
•Local field potentials recorded in humans while they keep sound in working memory.•Sustained increase in delta power observed in primary auditory cortex.•Pattern of change in power in non-primary cortex depends on the hierarchical level.•Hippocampus and parahippocampus showed increase in low frequency power. |
doi_str_mv | 10.1016/j.neuropsychologia.2020.107691 |
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•Local field potentials recorded in humans while they keep sound in working memory.•Sustained increase in delta power observed in primary auditory cortex.•Pattern of change in power in non-primary cortex depends on the hierarchical level.•Hippocampus and parahippocampus showed increase in low frequency power.</description><identifier>ISSN: 0028-3932</identifier><identifier>EISSN: 1873-3514</identifier><identifier>DOI: 10.1016/j.neuropsychologia.2020.107691</identifier><identifier>PMID: 33227284</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Acoustic Stimulation ; Auditory Cortex ; Auditory working memory ; Brain Mapping ; Electrocorticography ; Hippocampus ; Humans ; Magnetic Resonance Imaging ; Memory, Short-Term ; Neurophysiology ; Oscillatory activity ; Temporal Lobe</subject><ispartof>Neuropsychologia, 2021-01, Vol.150, p.107691-107691, Article 107691</ispartof><rights>2020 The Authors</rights><rights>Copyright © 2020 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><rights>2020 The Authors 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c503t-71bea9d7d79ddfacbc831b17786ca0ec48d6255eeaddd629797b0c459004e7653</citedby><cites>FETCH-LOGICAL-c503t-71bea9d7d79ddfacbc831b17786ca0ec48d6255eeaddd629797b0c459004e7653</cites><orcidid>0000-0001-8066-4381 ; 0000-0002-1960-9487</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuropsychologia.2020.107691$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,3537,27905,27906,45976</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33227284$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kumar, Sukhbinder</creatorcontrib><creatorcontrib>Gander, Phillip E.</creatorcontrib><creatorcontrib>Berger, Joel I.</creatorcontrib><creatorcontrib>Billig, Alexander J.</creatorcontrib><creatorcontrib>Nourski, Kirill V.</creatorcontrib><creatorcontrib>Oya, Hiroyuki</creatorcontrib><creatorcontrib>Kawasaki, Hiroto</creatorcontrib><creatorcontrib>Howard, Matthew A.</creatorcontrib><creatorcontrib>Griffiths, Timothy D.</creatorcontrib><title>Oscillatory correlates of auditory working memory examined with human electrocorticography</title><title>Neuropsychologia</title><addtitle>Neuropsychologia</addtitle><description>This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschl’s gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior- and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. This work demonstrates sustained activity patterns during AWM maintenance, with prominent low-frequency increases in medial temporal lobe regions.
•Local field potentials recorded in humans while they keep sound in working memory.•Sustained increase in delta power observed in primary auditory cortex.•Pattern of change in power in non-primary cortex depends on the hierarchical level.•Hippocampus and parahippocampus showed increase in low frequency power.</description><subject>Acoustic Stimulation</subject><subject>Auditory Cortex</subject><subject>Auditory working memory</subject><subject>Brain Mapping</subject><subject>Electrocorticography</subject><subject>Hippocampus</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Memory, Short-Term</subject><subject>Neurophysiology</subject><subject>Oscillatory activity</subject><subject>Temporal Lobe</subject><issn>0028-3932</issn><issn>1873-3514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtP3DAUhS1EBcPjL1RZoW4y-JXY3iBViBYkJDbtphvLse9MPE3iqZ0MnX9fDwOUdsXK177X59jnQ-iC4DnBpL5czQeYYlinrW1DF5bezCmmu6aoFTlAMyIFK1lF-CGaYUxlyRSjx-gkpRXGmFdUHqFjxigVVPIZ-vGQrO86M4a4LWyIEXINqQiLwkzOPx0_hvjTD8uih363hd-m9wO44tGPbdFOvRkK6MCOMWSB0duwjGbdbs_Qh4XpEpw_r6fo-5ebb9e35f3D17vrz_elrTAbS0EaMMoJJ5RzC2MbKxlpiBCytgaD5dLVtKoAjHO5UkKJBlteqfwbEHXFTtHVXnc9NT04C8MYTafX0fcmbnUwXv_bGXyrl2GjhZRcYZUFPj0LxPBrgjTq3icLOZUBwpQ05TUnnLNK_fWyMaQUYfFqQ7DeAdIr_T8gvQOk94CywMe3j329_kIkD9zuByBHtvEQdQYEgwXnY85Yu-Df6_UHleKxSw</recordid><startdate>20210108</startdate><enddate>20210108</enddate><creator>Kumar, Sukhbinder</creator><creator>Gander, Phillip E.</creator><creator>Berger, Joel I.</creator><creator>Billig, Alexander J.</creator><creator>Nourski, Kirill V.</creator><creator>Oya, Hiroyuki</creator><creator>Kawasaki, Hiroto</creator><creator>Howard, Matthew A.</creator><creator>Griffiths, Timothy D.</creator><general>Elsevier Ltd</general><general>Pergamon Press</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8066-4381</orcidid><orcidid>https://orcid.org/0000-0002-1960-9487</orcidid></search><sort><creationdate>20210108</creationdate><title>Oscillatory correlates of auditory working memory examined with human electrocorticography</title><author>Kumar, Sukhbinder ; Gander, Phillip E. ; Berger, Joel I. ; Billig, Alexander J. ; Nourski, Kirill V. ; Oya, Hiroyuki ; Kawasaki, Hiroto ; Howard, Matthew A. ; Griffiths, Timothy D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-71bea9d7d79ddfacbc831b17786ca0ec48d6255eeaddd629797b0c459004e7653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acoustic Stimulation</topic><topic>Auditory Cortex</topic><topic>Auditory working memory</topic><topic>Brain Mapping</topic><topic>Electrocorticography</topic><topic>Hippocampus</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Memory, Short-Term</topic><topic>Neurophysiology</topic><topic>Oscillatory activity</topic><topic>Temporal Lobe</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kumar, Sukhbinder</creatorcontrib><creatorcontrib>Gander, Phillip E.</creatorcontrib><creatorcontrib>Berger, Joel I.</creatorcontrib><creatorcontrib>Billig, Alexander J.</creatorcontrib><creatorcontrib>Nourski, Kirill V.</creatorcontrib><creatorcontrib>Oya, Hiroyuki</creatorcontrib><creatorcontrib>Kawasaki, Hiroto</creatorcontrib><creatorcontrib>Howard, Matthew A.</creatorcontrib><creatorcontrib>Griffiths, Timothy D.</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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kumar, Sukhbinder</au><au>Gander, Phillip E.</au><au>Berger, Joel I.</au><au>Billig, Alexander J.</au><au>Nourski, Kirill V.</au><au>Oya, Hiroyuki</au><au>Kawasaki, Hiroto</au><au>Howard, Matthew A.</au><au>Griffiths, Timothy D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oscillatory correlates of auditory working memory examined with human electrocorticography</atitle><jtitle>Neuropsychologia</jtitle><addtitle>Neuropsychologia</addtitle><date>2021-01-08</date><risdate>2021</risdate><volume>150</volume><spage>107691</spage><epage>107691</epage><pages>107691-107691</pages><artnum>107691</artnum><issn>0028-3932</issn><eissn>1873-3514</eissn><abstract>This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschl’s gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior- and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. This work demonstrates sustained activity patterns during AWM maintenance, with prominent low-frequency increases in medial temporal lobe regions.
•Local field potentials recorded in humans while they keep sound in working memory.•Sustained increase in delta power observed in primary auditory cortex.•Pattern of change in power in non-primary cortex depends on the hierarchical level.•Hippocampus and parahippocampus showed increase in low frequency power.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>33227284</pmid><doi>10.1016/j.neuropsychologia.2020.107691</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-8066-4381</orcidid><orcidid>https://orcid.org/0000-0002-1960-9487</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic Stimulation Auditory Cortex Auditory working memory Brain Mapping Electrocorticography Hippocampus Humans Magnetic Resonance Imaging Memory, Short-Term Neurophysiology Oscillatory activity Temporal Lobe |
title | Oscillatory correlates of auditory working memory examined with human electrocorticography |
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