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Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease

BACKGROUND: Deep brain stimulation (DBS) of the nucleus basalis of Meynert (NBM) has shown potential for the treatment of mild-to-moderate Alzheimer’s disease (AD). However, there is little evidence of whether NBM-DBS can improve cognitive functioning in patients with advanced AD. In addition, the m...

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Autores principales: Jiang, Yin, Yuan, Tian-Shuo, Chen, Ying-Chuan, Guo, Peng, Lian, Teng-Hong, Liu, Yu-Ye, Liu, Wei, Bai, Yu-Tong, Zhang, Quan, Zhang, Wei, Zhang, Jian-Guo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721033/
https://www.ncbi.nlm.nih.gov/pubmed/36471370
http://dx.doi.org/10.1186/s40035-022-00327-9
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author Jiang, Yin
Yuan, Tian-Shuo
Chen, Ying-Chuan
Guo, Peng
Lian, Teng-Hong
Liu, Yu-Ye
Liu, Wei
Bai, Yu-Tong
Zhang, Quan
Zhang, Wei
Zhang, Jian-Guo
author_facet Jiang, Yin
Yuan, Tian-Shuo
Chen, Ying-Chuan
Guo, Peng
Lian, Teng-Hong
Liu, Yu-Ye
Liu, Wei
Bai, Yu-Tong
Zhang, Quan
Zhang, Wei
Zhang, Jian-Guo
author_sort Jiang, Yin
collection PubMed
description BACKGROUND: Deep brain stimulation (DBS) of the nucleus basalis of Meynert (NBM) has shown potential for the treatment of mild-to-moderate Alzheimer’s disease (AD). However, there is little evidence of whether NBM-DBS can improve cognitive functioning in patients with advanced AD. In addition, the mechanisms underlying the modulation of brain networks remain unclear. This study was aimed to assess the cognitive function and the resting-state connectivity following NBM-DBS in patients with advanced AD. METHODS: Eight patients with advanced AD underwent bilateral NBM-DBS and were followed up for 12 months. Clinical outcomes were assessed by neuropsychological examinations using the Mini-Mental State Examination (MMSE) and Alzheimer’s Disease Assessment Scale. Resting-state functional magnetic resonance imaging and positron emission tomography data were also collected. RESULTS: The cognitive functioning of AD patients did not change from baseline to the 12-month follow-up. Interestingly, the MMSE score indicated clinical efficacy at 1 month of follow-up. At this time point, the connectivity between the hippocampal network and frontoparietal network tended to increase in the DBS-on state compared to the DBS-off state. Additionally, the increased functional connectivity between the parahippocampal gyrus (PHG) and the parietal cortex was associated with cognitive improvement. Further dynamic functional network analysis showed that NBM-DBS increased the proportion of the PHG-related connections, which was related to improved cognitive performance. CONCLUSION: The results indicated that NBM-DBS improves short-term cognitive performance in patients with advanced AD, which may be related to the modulation of multi-network connectivity patterns, and the hippocampus plays an important role within these networks. TRIAL REGISTRATION: ChiCTR, ChiCTR1900022324. Registered 5 April 2019—Prospective registration. https://www.chictr.org.cn/showproj.aspx?proj=37712 SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40035-022-00327-9.
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spelling pubmed-97210332022-12-06 Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease Jiang, Yin Yuan, Tian-Shuo Chen, Ying-Chuan Guo, Peng Lian, Teng-Hong Liu, Yu-Ye Liu, Wei Bai, Yu-Tong Zhang, Quan Zhang, Wei Zhang, Jian-Guo Transl Neurodegener Research BACKGROUND: Deep brain stimulation (DBS) of the nucleus basalis of Meynert (NBM) has shown potential for the treatment of mild-to-moderate Alzheimer’s disease (AD). However, there is little evidence of whether NBM-DBS can improve cognitive functioning in patients with advanced AD. In addition, the mechanisms underlying the modulation of brain networks remain unclear. This study was aimed to assess the cognitive function and the resting-state connectivity following NBM-DBS in patients with advanced AD. METHODS: Eight patients with advanced AD underwent bilateral NBM-DBS and were followed up for 12 months. Clinical outcomes were assessed by neuropsychological examinations using the Mini-Mental State Examination (MMSE) and Alzheimer’s Disease Assessment Scale. Resting-state functional magnetic resonance imaging and positron emission tomography data were also collected. RESULTS: The cognitive functioning of AD patients did not change from baseline to the 12-month follow-up. Interestingly, the MMSE score indicated clinical efficacy at 1 month of follow-up. At this time point, the connectivity between the hippocampal network and frontoparietal network tended to increase in the DBS-on state compared to the DBS-off state. Additionally, the increased functional connectivity between the parahippocampal gyrus (PHG) and the parietal cortex was associated with cognitive improvement. Further dynamic functional network analysis showed that NBM-DBS increased the proportion of the PHG-related connections, which was related to improved cognitive performance. CONCLUSION: The results indicated that NBM-DBS improves short-term cognitive performance in patients with advanced AD, which may be related to the modulation of multi-network connectivity patterns, and the hippocampus plays an important role within these networks. TRIAL REGISTRATION: ChiCTR, ChiCTR1900022324. Registered 5 April 2019—Prospective registration. https://www.chictr.org.cn/showproj.aspx?proj=37712 SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40035-022-00327-9. BioMed Central 2022-12-05 /pmc/articles/PMC9721033/ /pubmed/36471370 http://dx.doi.org/10.1186/s40035-022-00327-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Jiang, Yin
Yuan, Tian-Shuo
Chen, Ying-Chuan
Guo, Peng
Lian, Teng-Hong
Liu, Yu-Ye
Liu, Wei
Bai, Yu-Tong
Zhang, Quan
Zhang, Wei
Zhang, Jian-Guo
Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title_full Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title_fullStr Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title_full_unstemmed Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title_short Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal–frontoparietal networks in patients with advanced Alzheimer’s disease
title_sort deep brain stimulation of the nucleus basalis of meynert modulates hippocampal–frontoparietal networks in patients with advanced alzheimer’s disease
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721033/
https://www.ncbi.nlm.nih.gov/pubmed/36471370
http://dx.doi.org/10.1186/s40035-022-00327-9
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