Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping

Detalhes bibliográficos
Autor(a) principal: Costa, Gabriel Nascimento
Data de Publicação: 2024
Outros Autores: Schaum, Michael, Duarte, João Valente, Martins, Ricardo, Duarte, Isabel Catarina, Castelhano, João, Wibral, Michael, Castelo-Branco, Miguel
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Texto Completo: https://hdl.handle.net/10316/116654
https://doi.org/10.1002/hbm.26779
Resumo: Recently, there has been a resurgence in experimental and conceptual efforts to understand how brain rhythms can serve to organize visual information. Oscillations can provide temporal structure for neuronal processing and form a basis for integrating information across brain areas. Here, we use a bistable paradigm and a data-driven approach to test the hypothesis that oscillatory modulations associate with the integration or segregation of visual elements. Spectral signatures of perception of bound and unbound configurations of visual moving stimuli were studied using magnetoencephalography (MEG) in ambiguous and unambiguous conditions. Using a 2 × 2 design, we were able to isolate correlates from visual integration, either perceptual or stimulus-driven, from attentional and ambiguity-related activity. Two frequency bands were found to be modulated by visual integration: an alpha/beta frequency and a higher frequency gamma-band. Alpha/beta power was increased in several early visual cortical and dorsal visual areas during visual integration, while gamma-band power was surprisingly increased in the extrastriate visual cortex during segregation. This points to an integrative role for alpha/beta activity, likely from top-down signals maintaining a single visual representation. On the other hand, when more representations have to be processed in parallel gamma-band activity is increased, which is at odds with the notion that gamma oscillations are related to perceptual coherence. These modulations were confirmed in intracranial EEG recordings and partially originate from distinct brain areas. Our MEG and stereo-EEG data confirms predictions of binding mechanisms depending on low-frequency activity for long-range integration and for organizing visual processing while refuting a straightforward correlation between gamma-activity and perceptual binding. PRACTITIONER POINTS: Distinct neurophysiological signals underlie competing bistable percepts. Increased alpha/beta activity correlate with visual integration while gamma correlates with segmentation. Ambiguous percepts drive alpha/beta activity in the posterior cingulate cortex.
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spelling Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual groupingalpha and beta rhythms; gamma activity; intracranial recordings; magnetoencephalography (MEG); oscillations; perceptual binding; stereoEEGRecently, there has been a resurgence in experimental and conceptual efforts to understand how brain rhythms can serve to organize visual information. Oscillations can provide temporal structure for neuronal processing and form a basis for integrating information across brain areas. Here, we use a bistable paradigm and a data-driven approach to test the hypothesis that oscillatory modulations associate with the integration or segregation of visual elements. Spectral signatures of perception of bound and unbound configurations of visual moving stimuli were studied using magnetoencephalography (MEG) in ambiguous and unambiguous conditions. Using a 2 × 2 design, we were able to isolate correlates from visual integration, either perceptual or stimulus-driven, from attentional and ambiguity-related activity. Two frequency bands were found to be modulated by visual integration: an alpha/beta frequency and a higher frequency gamma-band. Alpha/beta power was increased in several early visual cortical and dorsal visual areas during visual integration, while gamma-band power was surprisingly increased in the extrastriate visual cortex during segregation. This points to an integrative role for alpha/beta activity, likely from top-down signals maintaining a single visual representation. On the other hand, when more representations have to be processed in parallel gamma-band activity is increased, which is at odds with the notion that gamma oscillations are related to perceptual coherence. These modulations were confirmed in intracranial EEG recordings and partially originate from distinct brain areas. Our MEG and stereo-EEG data confirms predictions of binding mechanisms depending on low-frequency activity for long-range integration and for organizing visual processing while refuting a straightforward correlation between gamma-activity and perceptual binding. PRACTITIONER POINTS: Distinct neurophysiological signals underlie competing bistable percepts. Increased alpha/beta activity correlate with visual integration while gamma correlates with segmentation. Ambiguous percepts drive alpha/beta activity in the posterior cingulate cortex.2024-08-15info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://hdl.handle.net/10316/116654https://hdl.handle.net/10316/116654https://doi.org/10.1002/hbm.26779eng1065-94711097-0193391857351097-0193https://doi.org/10.1002/hbm.26779Costa, Gabriel NascimentoSchaum, MichaelDuarte, João ValenteMartins, RicardoDuarte, Isabel CatarinaCastelhano, JoãoWibral, MichaelCastelo-Branco, Miguelinfo:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2024-09-30T15:50:22Zoai:estudogeral.uc.pt:10316/116654Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-29T06:10:21.457693Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
title Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
spellingShingle Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
Costa, Gabriel Nascimento
alpha and beta rhythms; gamma activity; intracranial recordings; magnetoencephalography (MEG); oscillations; perceptual binding; stereoEEG
title_short Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
title_full Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
title_fullStr Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
title_full_unstemmed Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
title_sort Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping
author Costa, Gabriel Nascimento
author_facet Costa, Gabriel Nascimento
Schaum, Michael
Duarte, João Valente
Martins, Ricardo
Duarte, Isabel Catarina
Castelhano, João
Wibral, Michael
Castelo-Branco, Miguel
author_role author
author2 Schaum, Michael
Duarte, João Valente
Martins, Ricardo
Duarte, Isabel Catarina
Castelhano, João
Wibral, Michael
Castelo-Branco, Miguel
author2_role author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Costa, Gabriel Nascimento
Schaum, Michael
Duarte, João Valente
Martins, Ricardo
Duarte, Isabel Catarina
Castelhano, João
Wibral, Michael
Castelo-Branco, Miguel
dc.subject.por.fl_str_mv alpha and beta rhythms; gamma activity; intracranial recordings; magnetoencephalography (MEG); oscillations; perceptual binding; stereoEEG
topic alpha and beta rhythms; gamma activity; intracranial recordings; magnetoencephalography (MEG); oscillations; perceptual binding; stereoEEG
description Recently, there has been a resurgence in experimental and conceptual efforts to understand how brain rhythms can serve to organize visual information. Oscillations can provide temporal structure for neuronal processing and form a basis for integrating information across brain areas. Here, we use a bistable paradigm and a data-driven approach to test the hypothesis that oscillatory modulations associate with the integration or segregation of visual elements. Spectral signatures of perception of bound and unbound configurations of visual moving stimuli were studied using magnetoencephalography (MEG) in ambiguous and unambiguous conditions. Using a 2 × 2 design, we were able to isolate correlates from visual integration, either perceptual or stimulus-driven, from attentional and ambiguity-related activity. Two frequency bands were found to be modulated by visual integration: an alpha/beta frequency and a higher frequency gamma-band. Alpha/beta power was increased in several early visual cortical and dorsal visual areas during visual integration, while gamma-band power was surprisingly increased in the extrastriate visual cortex during segregation. This points to an integrative role for alpha/beta activity, likely from top-down signals maintaining a single visual representation. On the other hand, when more representations have to be processed in parallel gamma-band activity is increased, which is at odds with the notion that gamma oscillations are related to perceptual coherence. These modulations were confirmed in intracranial EEG recordings and partially originate from distinct brain areas. Our MEG and stereo-EEG data confirms predictions of binding mechanisms depending on low-frequency activity for long-range integration and for organizing visual processing while refuting a straightforward correlation between gamma-activity and perceptual binding. PRACTITIONER POINTS: Distinct neurophysiological signals underlie competing bistable percepts. Increased alpha/beta activity correlate with visual integration while gamma correlates with segmentation. Ambiguous percepts drive alpha/beta activity in the posterior cingulate cortex.
publishDate 2024
dc.date.none.fl_str_mv 2024-08-15
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https://doi.org/10.1002/hbm.26779
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