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Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna

Neural oscillatory activities in basal ganglia have prominent roles in cognitive processes. However, the characteristics of oscillatory activities during cognitive tasks have not been extensively explored in human Globus Pallidus internus (GPi). This study aimed to compare oscillatory characteristic...

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Autores principales: Choubdar, Hadi, Mahdavi, Mahdi, Rostami, Zahra, Zabeh, Erfan, Gillies, Martin J., Green, Alexander L., Aziz, Tipu Z., Lashgari, Reza
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10011395/
https://www.ncbi.nlm.nih.gov/pubmed/36914686
http://dx.doi.org/10.1038/s41598-023-30832-4
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author Choubdar, Hadi
Mahdavi, Mahdi
Rostami, Zahra
Zabeh, Erfan
Gillies, Martin J.
Green, Alexander L.
Aziz, Tipu Z.
Lashgari, Reza
author_facet Choubdar, Hadi
Mahdavi, Mahdi
Rostami, Zahra
Zabeh, Erfan
Gillies, Martin J.
Green, Alexander L.
Aziz, Tipu Z.
Lashgari, Reza
author_sort Choubdar, Hadi
collection PubMed
description Neural oscillatory activities in basal ganglia have prominent roles in cognitive processes. However, the characteristics of oscillatory activities during cognitive tasks have not been extensively explored in human Globus Pallidus internus (GPi). This study aimed to compare oscillatory characteristics of GPi between dystonia and Parkinson's Disease (PD). A dystonia and a PD patient performed the Intra-Extra-Dimension shift (IED) task during both on and off-medication states. During the IED task, patients had to correctly choose between two visual stimuli containing shapes or lines based on a hidden rule via trial and error. Immediate auditory and visual feedback was provided upon the choice to inform participants if they chose correctly. Bilateral GPi Local Field Potentials (LFP) activity was recorded via externalized DBS leads. Transient high gamma activity (~ 100–150 Hz) was observed immediately after feedback in the dystonia patient. Moreover, these bursts were phase synchronous between left and right GPi with an antiphase clustering of phase differences. In contrast, no synchronous high gamma activity was detected in the PD patient with or without dopamine administration. The off-med PD patient also displayed enhanced low frequency clusters, which were ameliorated by medication. The current study provides a rare report of antiphase homotopic synchrony in human GPi, potentially related to incorporating and processing feedback information. The absence of these activities in off and on-med PD patient indicates the potential presence of impaired medication independent feedback processing circuits. Together, these findings suggest a potential role for GPi’s synchronized activity in shaping feedback processing mechanisms required in cognitive tasks.
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spelling pubmed-100113952023-03-15 Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna Choubdar, Hadi Mahdavi, Mahdi Rostami, Zahra Zabeh, Erfan Gillies, Martin J. Green, Alexander L. Aziz, Tipu Z. Lashgari, Reza Sci Rep Article Neural oscillatory activities in basal ganglia have prominent roles in cognitive processes. However, the characteristics of oscillatory activities during cognitive tasks have not been extensively explored in human Globus Pallidus internus (GPi). This study aimed to compare oscillatory characteristics of GPi between dystonia and Parkinson's Disease (PD). A dystonia and a PD patient performed the Intra-Extra-Dimension shift (IED) task during both on and off-medication states. During the IED task, patients had to correctly choose between two visual stimuli containing shapes or lines based on a hidden rule via trial and error. Immediate auditory and visual feedback was provided upon the choice to inform participants if they chose correctly. Bilateral GPi Local Field Potentials (LFP) activity was recorded via externalized DBS leads. Transient high gamma activity (~ 100–150 Hz) was observed immediately after feedback in the dystonia patient. Moreover, these bursts were phase synchronous between left and right GPi with an antiphase clustering of phase differences. In contrast, no synchronous high gamma activity was detected in the PD patient with or without dopamine administration. The off-med PD patient also displayed enhanced low frequency clusters, which were ameliorated by medication. The current study provides a rare report of antiphase homotopic synchrony in human GPi, potentially related to incorporating and processing feedback information. The absence of these activities in off and on-med PD patient indicates the potential presence of impaired medication independent feedback processing circuits. Together, these findings suggest a potential role for GPi’s synchronized activity in shaping feedback processing mechanisms required in cognitive tasks. Nature Publishing Group UK 2023-03-13 /pmc/articles/PMC10011395/ /pubmed/36914686 http://dx.doi.org/10.1038/s41598-023-30832-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Choubdar, Hadi
Mahdavi, Mahdi
Rostami, Zahra
Zabeh, Erfan
Gillies, Martin J.
Green, Alexander L.
Aziz, Tipu Z.
Lashgari, Reza
Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title_full Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title_fullStr Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title_full_unstemmed Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title_short Neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
title_sort neural oscillatory characteristics of feedback-associated activity in globus pallidus interna
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10011395/
https://www.ncbi.nlm.nih.gov/pubmed/36914686
http://dx.doi.org/10.1038/s41598-023-30832-4
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