Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study
Episodic memory (EM) deficit is the core cognitive dysfunction of amnestic mild cognitive impairment (aMCI). However, the episodic retrieval pattern detected by functional MRI (fMRI) appears preserved in aMCI subjects. To address this discrepancy, simultaneous electroencephalography (EEG)-fMRI recor...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2021-01-01
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| Series: | NeuroImage: Clinical |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158221000164 |
| _version_ | 1818836828581527552 |
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| author | Hao Shu Lihua Gu Ping Yang Molly V. Lucas Lijuan Gao Hongxing Zhang Haisan Zhang Zhan Xu Wei Wu Ling Li Zhijun Zhang |
| author_facet | Hao Shu Lihua Gu Ping Yang Molly V. Lucas Lijuan Gao Hongxing Zhang Haisan Zhang Zhan Xu Wei Wu Ling Li Zhijun Zhang |
| author_sort | Hao Shu |
| collection | DOAJ |
| description | Episodic memory (EM) deficit is the core cognitive dysfunction of amnestic mild cognitive impairment (aMCI). However, the episodic retrieval pattern detected by functional MRI (fMRI) appears preserved in aMCI subjects. To address this discrepancy, simultaneous electroencephalography (EEG)-fMRI recording was employed to determine whether temporal dynamics of brain episodic retrieval activity were disturbed in patients with aMCI. Twenty-six aMCI and 29 healthy control (HC) subjects completed a word-list memory retrieval task during simultaneous EEG-fMRI. The retrieval success activation pattern was detected with fMRI analysis, and the familiarity- and recollection-related components of episodic retrieval activity were identified using event-related potential (ERP) analysis. The fMRI-constrained ERP analysis explored the temporal dynamics of brain activity in the retrieval success pattern, and the ERP-informed fMRI analysis detected fMRI correlates of the ERP components related to familiarity and recollection processes. The two groups exhibited similar retrieval success patterns in the bilateral posteromedial parietal cortex, the left inferior parietal lobule (IPL), and the left lateral prefrontal cortex (LPFC). The fMRI-constrained ERP analysis showed that the aMCI group did not exhibit old/new effects in the IPL and LPFC that were observed in the HC group. In addition, the aMCI group showed disturbed fMRI correlate of ERP recollection component that was associated with inferior EM performance. Therefore, in this study, we identified disturbed temporal dynamics in episodic retrieval activity with a preserved spatial activity pattern in aMCI. Taken together, the simultaneous EEG-fMRI technique demonstrated the potential to identify individuals with a high risk of cognitive deterioration. |
| first_indexed | 2024-12-19T03:12:49Z |
| format | Article |
| id | doaj.art-f21723d1fd154eab874387cf702d1469 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-19T03:12:49Z |
| publishDate | 2021-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-f21723d1fd154eab874387cf702d14692022-12-21T20:37:58ZengElsevierNeuroImage: Clinical2213-15822021-01-0130102572Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI studyHao Shu0Lihua Gu1Ping Yang2Molly V. Lucas3Lijuan Gao4Hongxing Zhang5Haisan Zhang6Zhan Xu7Wei Wu8Ling Li9Zhijun Zhang10Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, ChinaDepartment of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, ChinaInstitute for Brain Research and Rehabilitation, South China Normal University, Guangzhou 510631, ChinaDepartment of Psychiatry and Behavioral Sciences and Wu Tsai Neuroscience Institute, Stanford University, Stanford, CA 94305, USA; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, CA 94394, USADepartment of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, ChinaDepartment of Psychiatry, The Second Affiliated Hospital of Xingxiang Medical University, Xinxiang, Henan 453002, ChinaDepartment of Psychiatry, The Second Affiliated Hospital of Xingxiang Medical University, Xinxiang, Henan 453002, ChinaImaging Physics, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030, USASchool of Automation Science and Engineering, South China University of Technology, Guangzhou 510640, China; Department of Psychiatry and Behavioral Sciences and Wu Tsai Neuroscience Institute, Stanford University, Stanford, CA 94305, USA; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, CA 94394, USA; Corresponding authors at: Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, China (Z. Zhang). Key Laboratory for NeuroInformation of Ministry of Education, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China (L. Li). School of Automation Science and Engineering, South China University of Technology, Guangzhou 510640, China (W. Wu).Key Laboratory for NeuroInformation of Ministry of Education, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China; Corresponding authors at: Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, China (Z. Zhang). Key Laboratory for NeuroInformation of Ministry of Education, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China (L. Li). School of Automation Science and Engineering, South China University of Technology, Guangzhou 510640, China (W. Wu).Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, China; Key Laboratory for NeuroInformation of Ministry of Education, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China; Department of Psychiatry, The Second Affiliated Hospital of Xingxiang Medical University, Xinxiang, Henan 453002, China; Corresponding authors at: Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Neuropsychiatric Institute, The Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing, Jiangsu 210009, China (Z. Zhang). Key Laboratory for NeuroInformation of Ministry of Education, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China (L. Li). School of Automation Science and Engineering, South China University of Technology, Guangzhou 510640, China (W. Wu).Episodic memory (EM) deficit is the core cognitive dysfunction of amnestic mild cognitive impairment (aMCI). However, the episodic retrieval pattern detected by functional MRI (fMRI) appears preserved in aMCI subjects. To address this discrepancy, simultaneous electroencephalography (EEG)-fMRI recording was employed to determine whether temporal dynamics of brain episodic retrieval activity were disturbed in patients with aMCI. Twenty-six aMCI and 29 healthy control (HC) subjects completed a word-list memory retrieval task during simultaneous EEG-fMRI. The retrieval success activation pattern was detected with fMRI analysis, and the familiarity- and recollection-related components of episodic retrieval activity were identified using event-related potential (ERP) analysis. The fMRI-constrained ERP analysis explored the temporal dynamics of brain activity in the retrieval success pattern, and the ERP-informed fMRI analysis detected fMRI correlates of the ERP components related to familiarity and recollection processes. The two groups exhibited similar retrieval success patterns in the bilateral posteromedial parietal cortex, the left inferior parietal lobule (IPL), and the left lateral prefrontal cortex (LPFC). The fMRI-constrained ERP analysis showed that the aMCI group did not exhibit old/new effects in the IPL and LPFC that were observed in the HC group. In addition, the aMCI group showed disturbed fMRI correlate of ERP recollection component that was associated with inferior EM performance. Therefore, in this study, we identified disturbed temporal dynamics in episodic retrieval activity with a preserved spatial activity pattern in aMCI. Taken together, the simultaneous EEG-fMRI technique demonstrated the potential to identify individuals with a high risk of cognitive deterioration.http://www.sciencedirect.com/science/article/pii/S2213158221000164Amnestic mild cognitive impairmentEpisodic memoryFamiliarityRecollectionRetrievalSimultaneous EEG-fMRI |
| spellingShingle | Hao Shu Lihua Gu Ping Yang Molly V. Lucas Lijuan Gao Hongxing Zhang Haisan Zhang Zhan Xu Wei Wu Ling Li Zhijun Zhang Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study NeuroImage: Clinical Amnestic mild cognitive impairment Episodic memory Familiarity Recollection Retrieval Simultaneous EEG-fMRI |
| title | Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study |
| title_full | Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study |
| title_fullStr | Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study |
| title_full_unstemmed | Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study |
| title_short | Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study |
| title_sort | disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment a simultaneous eeg fmri study |
| topic | Amnestic mild cognitive impairment Episodic memory Familiarity Recollection Retrieval Simultaneous EEG-fMRI |
| url | http://www.sciencedirect.com/science/article/pii/S2213158221000164 |
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