High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance

Autores
Weiss, Shennan Aibel; Sawczuk, Nicolás; Rubinstein, Daniel Y.; Sperling, Michael R.; Wendel Mitoraj, Katrina; Österman, Päivi; Dumay Roscher, René; Mikell, Charles B.; Mofakham, Sima; Coulehan, Kelly; Djuric, Petar M.; Fernandez Slezak, Diego; Kamienkowski, Juan Esteban
Año de publicación
2025
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Introduction: The left supramarginal gyrus (LSMG) contributes to attentional allocation for memory encoding and may also reflect memory state and performance. Given the roles of high-gamma and beta bursts in cognition and memory, this proof-of-concept study investigated whether these signals within the LSMG could classify memory state and performance.Methods: Using secondary data from 103 epilepsy patients undergoing presurgical iEEG evaluation, we analyzed 141 delayed verbal free recall experiments. Intracranial EEG (iEEG) data, recorded solely from LSMG electrode contacts, were processed to create two-dimensional (2D) tensors of convolved high-gamma (HG), and beta (15–40 Hz) burst activity. Convolutional neural networks (CNNs) were trained and cross-validated on these 2D tensors to classify memory state (encoding versus recall) and performance (remembered versus forgotten items) within subjects.Results: The latter CNN, used to label subsequently recalled words based on iEEG recorded during the encoding epoch, performed at or below chance in 79 of the 141 experiments. In all but 3 of these 79 experiments, the iEEG was contaminated or low amplitude. In the other 62 experiments this CNN labeled recalled words with an area under the receiver operating curve (AUROC) score of greater than 0.52. A generalized linear model explained the variance of the AUROC score for labelling recalled words correctly in these 62 experiments (n = 62, d.f. = 20, F = 1.7, p = 1 × 10−4). The most significant term in the model was a positive interaction between (1) mean HG burst signal to noise ratio; (2) mean beta burst signal to noise ratio; (3) the number of electrode contacts in the LSMG; and (4) recall probability (t = 3.04, p = 0.006). We identified 14 experiments that labeled subsequently recalled words during encoding with an AUROC score greater than 0.6. To address over-training, we also trained and then tested the CNN on distinct datasets in four subjects. In most of these experiments CNN performed better than chance. We also found that a CNN utilizing 2D tensors of HG and beta bursts could distinguish encoding from scrambled recall epochs.Discussion: This work indicates LSMG is a memory hotspot and that HG and beta bursts may serve as temporal memory information packets or signify attention related to memory.
Fil: Weiss, Shennan Aibel. Stony Brook University ; State University Of New York;
Fil: Sawczuk, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Rubinstein, Daniel Y.. Thomas Jefferson University; Estados Unidos
Fil: Sperling, Michael R.. Thomas Jefferson University; Estados Unidos
Fil: Wendel Mitoraj, Katrina. No especifíca;
Fil: Österman, Päivi. No especifíca;
Fil: Dumay Roscher, René. No especifíca;
Fil: Mikell, Charles B.. Stony Brook University ; State University Of New York;
Fil: Mofakham, Sima. Stony Brook University ; State University Of New York;
Fil: Coulehan, Kelly. Stony Brook University ; State University Of New York;
Fil: Djuric, Petar M.. Stony Brook University ; State University Of New York;
Fil: Fernandez Slezak, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Kamienkowski, Juan Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Materia
verbal memory
left supramaginal gyrus
posterior parietal cortex
encoding
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/290938

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oai_identifier_str oai:ri.conicet.gov.ar:11336/290938
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performanceWeiss, Shennan AibelSawczuk, NicolásRubinstein, Daniel Y.Sperling, Michael R.Wendel Mitoraj, KatrinaÖsterman, PäiviDumay Roscher, RenéMikell, Charles B.Mofakham, SimaCoulehan, KellyDjuric, Petar M.Fernandez Slezak, DiegoKamienkowski, Juan Estebanverbal memoryleft supramaginal gyrusposterior parietal cortexencodinghttps://purl.org/becyt/ford/1.2https://purl.org/becyt/ford/1Introduction: The left supramarginal gyrus (LSMG) contributes to attentional allocation for memory encoding and may also reflect memory state and performance. Given the roles of high-gamma and beta bursts in cognition and memory, this proof-of-concept study investigated whether these signals within the LSMG could classify memory state and performance.Methods: Using secondary data from 103 epilepsy patients undergoing presurgical iEEG evaluation, we analyzed 141 delayed verbal free recall experiments. Intracranial EEG (iEEG) data, recorded solely from LSMG electrode contacts, were processed to create two-dimensional (2D) tensors of convolved high-gamma (HG), and beta (15–40 Hz) burst activity. Convolutional neural networks (CNNs) were trained and cross-validated on these 2D tensors to classify memory state (encoding versus recall) and performance (remembered versus forgotten items) within subjects.Results: The latter CNN, used to label subsequently recalled words based on iEEG recorded during the encoding epoch, performed at or below chance in 79 of the 141 experiments. In all but 3 of these 79 experiments, the iEEG was contaminated or low amplitude. In the other 62 experiments this CNN labeled recalled words with an area under the receiver operating curve (AUROC) score of greater than 0.52. A generalized linear model explained the variance of the AUROC score for labelling recalled words correctly in these 62 experiments (n = 62, d.f. = 20, F = 1.7, p = 1 × 10−4). The most significant term in the model was a positive interaction between (1) mean HG burst signal to noise ratio; (2) mean beta burst signal to noise ratio; (3) the number of electrode contacts in the LSMG; and (4) recall probability (t = 3.04, p = 0.006). We identified 14 experiments that labeled subsequently recalled words during encoding with an AUROC score greater than 0.6. To address over-training, we also trained and then tested the CNN on distinct datasets in four subjects. In most of these experiments CNN performed better than chance. We also found that a CNN utilizing 2D tensors of HG and beta bursts could distinguish encoding from scrambled recall epochs.Discussion: This work indicates LSMG is a memory hotspot and that HG and beta bursts may serve as temporal memory information packets or signify attention related to memory.Fil: Weiss, Shennan Aibel. Stony Brook University ; State University Of New York;Fil: Sawczuk, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; ArgentinaFil: Rubinstein, Daniel Y.. Thomas Jefferson University; Estados UnidosFil: Sperling, Michael R.. Thomas Jefferson University; Estados UnidosFil: Wendel Mitoraj, Katrina. No especifíca;Fil: Österman, Päivi. No especifíca;Fil: Dumay Roscher, René. No especifíca;Fil: Mikell, Charles B.. Stony Brook University ; State University Of New York;Fil: Mofakham, Sima. Stony Brook University ; State University Of New York;Fil: Coulehan, Kelly. Stony Brook University ; State University Of New York;Fil: Djuric, Petar M.. Stony Brook University ; State University Of New York;Fil: Fernandez Slezak, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; ArgentinaFil: Kamienkowski, Juan Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; ArgentinaFrontiers Media2025-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/290938Weiss, Shennan Aibel; Sawczuk, Nicolás; Rubinstein, Daniel Y.; Sperling, Michael R.; Wendel Mitoraj, Katrina; et al.; High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance; Frontiers Media; Frontiers in Neurology; 16; 7-2025; 1-181664-2295CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fneur.2025.1627528/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fneur.2025.1627528info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-08-25T15:50:41Zoai:ri.conicet.gov.ar:11336/290938instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-08-25 15:50:42.113CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
title High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
spellingShingle High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
Weiss, Shennan Aibel
verbal memory
left supramaginal gyrus
posterior parietal cortex
encoding
title_short High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
title_full High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
title_fullStr High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
title_full_unstemmed High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
title_sort High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance
dc.creator.none.fl_str_mv Weiss, Shennan Aibel
Sawczuk, Nicolás
Rubinstein, Daniel Y.
Sperling, Michael R.
Wendel Mitoraj, Katrina
Österman, Päivi
Dumay Roscher, René
Mikell, Charles B.
Mofakham, Sima
Coulehan, Kelly
Djuric, Petar M.
Fernandez Slezak, Diego
Kamienkowski, Juan Esteban
author Weiss, Shennan Aibel
author_facet Weiss, Shennan Aibel
Sawczuk, Nicolás
Rubinstein, Daniel Y.
Sperling, Michael R.
Wendel Mitoraj, Katrina
Österman, Päivi
Dumay Roscher, René
Mikell, Charles B.
Mofakham, Sima
Coulehan, Kelly
Djuric, Petar M.
Fernandez Slezak, Diego
Kamienkowski, Juan Esteban
author_role author
author2 Sawczuk, Nicolás
Rubinstein, Daniel Y.
Sperling, Michael R.
Wendel Mitoraj, Katrina
Österman, Päivi
Dumay Roscher, René
Mikell, Charles B.
Mofakham, Sima
Coulehan, Kelly
Djuric, Petar M.
Fernandez Slezak, Diego
Kamienkowski, Juan Esteban
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv verbal memory
left supramaginal gyrus
posterior parietal cortex
encoding
topic verbal memory
left supramaginal gyrus
posterior parietal cortex
encoding
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.2
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Introduction: The left supramarginal gyrus (LSMG) contributes to attentional allocation for memory encoding and may also reflect memory state and performance. Given the roles of high-gamma and beta bursts in cognition and memory, this proof-of-concept study investigated whether these signals within the LSMG could classify memory state and performance.Methods: Using secondary data from 103 epilepsy patients undergoing presurgical iEEG evaluation, we analyzed 141 delayed verbal free recall experiments. Intracranial EEG (iEEG) data, recorded solely from LSMG electrode contacts, were processed to create two-dimensional (2D) tensors of convolved high-gamma (HG), and beta (15–40 Hz) burst activity. Convolutional neural networks (CNNs) were trained and cross-validated on these 2D tensors to classify memory state (encoding versus recall) and performance (remembered versus forgotten items) within subjects.Results: The latter CNN, used to label subsequently recalled words based on iEEG recorded during the encoding epoch, performed at or below chance in 79 of the 141 experiments. In all but 3 of these 79 experiments, the iEEG was contaminated or low amplitude. In the other 62 experiments this CNN labeled recalled words with an area under the receiver operating curve (AUROC) score of greater than 0.52. A generalized linear model explained the variance of the AUROC score for labelling recalled words correctly in these 62 experiments (n = 62, d.f. = 20, F = 1.7, p = 1 × 10−4). The most significant term in the model was a positive interaction between (1) mean HG burst signal to noise ratio; (2) mean beta burst signal to noise ratio; (3) the number of electrode contacts in the LSMG; and (4) recall probability (t = 3.04, p = 0.006). We identified 14 experiments that labeled subsequently recalled words during encoding with an AUROC score greater than 0.6. To address over-training, we also trained and then tested the CNN on distinct datasets in four subjects. In most of these experiments CNN performed better than chance. We also found that a CNN utilizing 2D tensors of HG and beta bursts could distinguish encoding from scrambled recall epochs.Discussion: This work indicates LSMG is a memory hotspot and that HG and beta bursts may serve as temporal memory information packets or signify attention related to memory.
Fil: Weiss, Shennan Aibel. Stony Brook University ; State University Of New York;
Fil: Sawczuk, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Rubinstein, Daniel Y.. Thomas Jefferson University; Estados Unidos
Fil: Sperling, Michael R.. Thomas Jefferson University; Estados Unidos
Fil: Wendel Mitoraj, Katrina. No especifíca;
Fil: Österman, Päivi. No especifíca;
Fil: Dumay Roscher, René. No especifíca;
Fil: Mikell, Charles B.. Stony Brook University ; State University Of New York;
Fil: Mofakham, Sima. Stony Brook University ; State University Of New York;
Fil: Coulehan, Kelly. Stony Brook University ; State University Of New York;
Fil: Djuric, Petar M.. Stony Brook University ; State University Of New York;
Fil: Fernandez Slezak, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Kamienkowski, Juan Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
description Introduction: The left supramarginal gyrus (LSMG) contributes to attentional allocation for memory encoding and may also reflect memory state and performance. Given the roles of high-gamma and beta bursts in cognition and memory, this proof-of-concept study investigated whether these signals within the LSMG could classify memory state and performance.Methods: Using secondary data from 103 epilepsy patients undergoing presurgical iEEG evaluation, we analyzed 141 delayed verbal free recall experiments. Intracranial EEG (iEEG) data, recorded solely from LSMG electrode contacts, were processed to create two-dimensional (2D) tensors of convolved high-gamma (HG), and beta (15–40 Hz) burst activity. Convolutional neural networks (CNNs) were trained and cross-validated on these 2D tensors to classify memory state (encoding versus recall) and performance (remembered versus forgotten items) within subjects.Results: The latter CNN, used to label subsequently recalled words based on iEEG recorded during the encoding epoch, performed at or below chance in 79 of the 141 experiments. In all but 3 of these 79 experiments, the iEEG was contaminated or low amplitude. In the other 62 experiments this CNN labeled recalled words with an area under the receiver operating curve (AUROC) score of greater than 0.52. A generalized linear model explained the variance of the AUROC score for labelling recalled words correctly in these 62 experiments (n = 62, d.f. = 20, F = 1.7, p = 1 × 10−4). The most significant term in the model was a positive interaction between (1) mean HG burst signal to noise ratio; (2) mean beta burst signal to noise ratio; (3) the number of electrode contacts in the LSMG; and (4) recall probability (t = 3.04, p = 0.006). We identified 14 experiments that labeled subsequently recalled words during encoding with an AUROC score greater than 0.6. To address over-training, we also trained and then tested the CNN on distinct datasets in four subjects. In most of these experiments CNN performed better than chance. We also found that a CNN utilizing 2D tensors of HG and beta bursts could distinguish encoding from scrambled recall epochs.Discussion: This work indicates LSMG is a memory hotspot and that HG and beta bursts may serve as temporal memory information packets or signify attention related to memory.
publishDate 2025
dc.date.none.fl_str_mv 2025-07
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/290938
Weiss, Shennan Aibel; Sawczuk, Nicolás; Rubinstein, Daniel Y.; Sperling, Michael R.; Wendel Mitoraj, Katrina; et al.; High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance; Frontiers Media; Frontiers in Neurology; 16; 7-2025; 1-18
1664-2295
CONICET Digital
CONICET
url http://hdl.handle.net/11336/290938
identifier_str_mv Weiss, Shennan Aibel; Sawczuk, Nicolás; Rubinstein, Daniel Y.; Sperling, Michael R.; Wendel Mitoraj, Katrina; et al.; High-gamma and beta bursts in the left supramarginal gyrus can differentiate verbal memory states and performance; Frontiers Media; Frontiers in Neurology; 16; 7-2025; 1-18
1664-2295
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fneur.2025.1627528/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fneur.2025.1627528
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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