Laminar pattern of sensory-evoked dynamic high-frequency oscillatory activity in the macaque auditory cortex
Abstract High-frequency (>60 Hz) neuroelectric signals likely have functional roles distinct from low-frequency (60 Hz) does not simply equate to neuronal spiking, they are highly correlated, having similar information encoding. High-gamma activity is typically considered broadband and poorly pha...
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Veröffentlicht in: | Cerebral cortex (New York, N.Y. 1991) N.Y. 1991), 2024-08, Vol.34 (8) |
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container_title | Cerebral cortex (New York, N.Y. 1991) |
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creator | Kajikawa, Yoshinao Mackey, Chase A O’Connell, Monica Noelle |
description | Abstract
High-frequency (>60 Hz) neuroelectric signals likely have functional roles distinct from low-frequency (60 Hz) does not simply equate to neuronal spiking, they are highly correlated, having similar information encoding. High-gamma activity is typically considered broadband and poorly phase-locked to sensory stimuli and thus is typically analyzed after transformations into absolute amplitude or spectral power. However, those analyses discard signal polarity, compromising the interpretation of neuroelectric events that are essentially dipolar. In the spectrotemporal profiles of field potentials in auditory cortex, we show high-frequency spectral peaks not phase-locked to sound onset, which follow the broadband peak of phase-locked onset responses. Isolating the signal components comprising the high-frequency peaks reveals narrow-band high-frequency oscillatory events, whose instantaneous frequency changes rapidly from >150 to 60 Hz, which may underlie broadband high-frequency spectral peaks in previous reports. The laminar amplitude distributions of the isolated activity had two peak positions, while the laminar phase patterns showed a counterphase relationship between those peaks, indicating the formation of dipoles. Our findings suggest that nonphase-locked HGA arises in part from oscillatory or recurring activity of supragranular-layer neuronal ensembles in auditory cortex. |
doi_str_mv | 10.1093/cercor/bhae338 |
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High-frequency (>60 Hz) neuroelectric signals likely have functional roles distinct from low-frequency (<30 Hz) signals. While high-gamma activity (>60 Hz) does not simply equate to neuronal spiking, they are highly correlated, having similar information encoding. High-gamma activity is typically considered broadband and poorly phase-locked to sensory stimuli and thus is typically analyzed after transformations into absolute amplitude or spectral power. However, those analyses discard signal polarity, compromising the interpretation of neuroelectric events that are essentially dipolar. In the spectrotemporal profiles of field potentials in auditory cortex, we show high-frequency spectral peaks not phase-locked to sound onset, which follow the broadband peak of phase-locked onset responses. Isolating the signal components comprising the high-frequency peaks reveals narrow-band high-frequency oscillatory events, whose instantaneous frequency changes rapidly from >150 to 60 Hz, which may underlie broadband high-frequency spectral peaks in previous reports. The laminar amplitude distributions of the isolated activity had two peak positions, while the laminar phase patterns showed a counterphase relationship between those peaks, indicating the formation of dipoles. Our findings suggest that nonphase-locked HGA arises in part from oscillatory or recurring activity of supragranular-layer neuronal ensembles in auditory cortex.</description><identifier>ISSN: 1047-3211</identifier><identifier>ISSN: 1460-2199</identifier><identifier>EISSN: 1460-2199</identifier><identifier>DOI: 10.1093/cercor/bhae338</identifier><identifier>PMID: 39128941</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Acoustic Stimulation - methods ; Animals ; Auditory Cortex - physiology ; Electroencephalography ; Evoked Potentials, Auditory - physiology ; Gamma Rhythm - physiology ; Macaca mulatta ; Male</subject><ispartof>Cerebral cortex (New York, N.Y. 1991), 2024-08, Vol.34 (8)</ispartof><rights>The Author(s) 2024. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c214t-f74682f8fc60fa98acd9d719ff5c3b7b25f46202288d36164936fff87953a1a23</cites><orcidid>0000-0002-0403-9637 ; 0000-0003-3953-642X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,1579,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39128941$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kajikawa, Yoshinao</creatorcontrib><creatorcontrib>Mackey, Chase A</creatorcontrib><creatorcontrib>O’Connell, Monica Noelle</creatorcontrib><title>Laminar pattern of sensory-evoked dynamic high-frequency oscillatory activity in the macaque auditory cortex</title><title>Cerebral cortex (New York, N.Y. 1991)</title><addtitle>Cereb Cortex</addtitle><description>Abstract
High-frequency (>60 Hz) neuroelectric signals likely have functional roles distinct from low-frequency (<30 Hz) signals. While high-gamma activity (>60 Hz) does not simply equate to neuronal spiking, they are highly correlated, having similar information encoding. High-gamma activity is typically considered broadband and poorly phase-locked to sensory stimuli and thus is typically analyzed after transformations into absolute amplitude or spectral power. However, those analyses discard signal polarity, compromising the interpretation of neuroelectric events that are essentially dipolar. In the spectrotemporal profiles of field potentials in auditory cortex, we show high-frequency spectral peaks not phase-locked to sound onset, which follow the broadband peak of phase-locked onset responses. Isolating the signal components comprising the high-frequency peaks reveals narrow-band high-frequency oscillatory events, whose instantaneous frequency changes rapidly from >150 to 60 Hz, which may underlie broadband high-frequency spectral peaks in previous reports. The laminar amplitude distributions of the isolated activity had two peak positions, while the laminar phase patterns showed a counterphase relationship between those peaks, indicating the formation of dipoles. Our findings suggest that nonphase-locked HGA arises in part from oscillatory or recurring activity of supragranular-layer neuronal ensembles in auditory cortex.</description><subject>Acoustic Stimulation - methods</subject><subject>Animals</subject><subject>Auditory Cortex - physiology</subject><subject>Electroencephalography</subject><subject>Evoked Potentials, Auditory - physiology</subject><subject>Gamma Rhythm - physiology</subject><subject>Macaca mulatta</subject><subject>Male</subject><issn>1047-3211</issn><issn>1460-2199</issn><issn>1460-2199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0DtPwzAUBWALgWgprIzIIwxp_cjDHhHiJVVigTlyHJsYkjjYTkX-PYYUViZ7-O7R0QHgHKM1RpxupHLSuk3VCEUpOwBLnOYoIZjzw_hHaZFQgvECnHj_hhAuSEaOwYJyTBhP8RK0W9GZXjg4iBCU66HV0KveWzclamffVQ3rqY9Gwsa8Nol26mNUvZyg9dK0rQhRQiGD2ZkwQdPD0CjYCSkig2KszQ-IHYP6PAVHWrRene3fFXi5u32-eUi2T_ePN9fbRBKchkQXac6IZlrmSAvOhKx5XWCudSZpVVQk02lOECGM1TTHecpprrVmBc-owILQFbiccwdnYw0fys54qWLbXtnRlxRxgjAqCI50PVPprPdO6XJwphNuKjEqvxcu54XL_cLx4GKfPVadqv_476QRXM3AjsN_YV9d1omm</recordid><startdate>20240801</startdate><enddate>20240801</enddate><creator>Kajikawa, Yoshinao</creator><creator>Mackey, Chase A</creator><creator>O’Connell, Monica Noelle</creator><general>Oxford University Press</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>7X8</scope><orcidid>https://orcid.org/0000-0002-0403-9637</orcidid><orcidid>https://orcid.org/0000-0003-3953-642X</orcidid></search><sort><creationdate>20240801</creationdate><title>Laminar pattern of sensory-evoked dynamic high-frequency oscillatory activity in the macaque auditory cortex</title><author>Kajikawa, Yoshinao ; Mackey, Chase A ; O’Connell, Monica Noelle</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c214t-f74682f8fc60fa98acd9d719ff5c3b7b25f46202288d36164936fff87953a1a23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acoustic Stimulation - methods</topic><topic>Animals</topic><topic>Auditory Cortex - physiology</topic><topic>Electroencephalography</topic><topic>Evoked Potentials, Auditory - physiology</topic><topic>Gamma Rhythm - physiology</topic><topic>Macaca mulatta</topic><topic>Male</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kajikawa, Yoshinao</creatorcontrib><creatorcontrib>Mackey, Chase A</creatorcontrib><creatorcontrib>O’Connell, Monica Noelle</creatorcontrib><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><jtitle>Cerebral cortex (New York, N.Y. 1991)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kajikawa, Yoshinao</au><au>Mackey, Chase A</au><au>O’Connell, Monica Noelle</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Laminar pattern of sensory-evoked dynamic high-frequency oscillatory activity in the macaque auditory cortex</atitle><jtitle>Cerebral cortex (New York, N.Y. 1991)</jtitle><addtitle>Cereb Cortex</addtitle><date>2024-08-01</date><risdate>2024</risdate><volume>34</volume><issue>8</issue><issn>1047-3211</issn><issn>1460-2199</issn><eissn>1460-2199</eissn><abstract>Abstract
High-frequency (>60 Hz) neuroelectric signals likely have functional roles distinct from low-frequency (<30 Hz) signals. While high-gamma activity (>60 Hz) does not simply equate to neuronal spiking, they are highly correlated, having similar information encoding. High-gamma activity is typically considered broadband and poorly phase-locked to sensory stimuli and thus is typically analyzed after transformations into absolute amplitude or spectral power. However, those analyses discard signal polarity, compromising the interpretation of neuroelectric events that are essentially dipolar. In the spectrotemporal profiles of field potentials in auditory cortex, we show high-frequency spectral peaks not phase-locked to sound onset, which follow the broadband peak of phase-locked onset responses. Isolating the signal components comprising the high-frequency peaks reveals narrow-band high-frequency oscillatory events, whose instantaneous frequency changes rapidly from >150 to 60 Hz, which may underlie broadband high-frequency spectral peaks in previous reports. The laminar amplitude distributions of the isolated activity had two peak positions, while the laminar phase patterns showed a counterphase relationship between those peaks, indicating the formation of dipoles. Our findings suggest that nonphase-locked HGA arises in part from oscillatory or recurring activity of supragranular-layer neuronal ensembles in auditory cortex.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>39128941</pmid><doi>10.1093/cercor/bhae338</doi><orcidid>https://orcid.org/0000-0002-0403-9637</orcidid><orcidid>https://orcid.org/0000-0003-3953-642X</orcidid></addata></record> |
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subjects | Acoustic Stimulation - methods Animals Auditory Cortex - physiology Electroencephalography Evoked Potentials, Auditory - physiology Gamma Rhythm - physiology Macaca mulatta Male |
title | Laminar pattern of sensory-evoked dynamic high-frequency oscillatory activity in the macaque auditory cortex |
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