Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study

Hao Shu; Lihua Gu; Ping Yang; Molly V Lucas; Lijuan Gao; Hongxing Zhang; Haisan Zhang; Zhan Xu; Wei Wu; Ling Li; Zhijun Zhang

doi:10.1016/j.nicl.2021.102572

Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study

Neuroimage Clin. 2021:30:102572. doi: 10.1016/j.nicl.2021.102572. Epub 2021 Jan 26.

Authors

Hao Shu¹, Lihua Gu¹, Ping Yang², Molly V Lucas³, Lijuan Gao¹, Hongxing Zhang⁴, Haisan Zhang⁴, Zhan Xu⁵, Wei Wu⁶, Ling Li⁷, Zhijun Zhang⁸

Affiliations

¹ 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.
² Institute for Brain Research and Rehabilitation, South China Normal University, Guangzhou 510631, China.
³ 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.
⁴ Department of Psychiatry, The Second Affiliated Hospital of Xingxiang Medical University, Xinxiang, Henan 453002, China.
⁵ Imaging Physics, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030, USA.
⁶ School 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. Electronic address: weiwuneuro@gmail.com.
⁷ 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. Electronic address: liling@uestc.edu.cn.
⁸ 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. Electronic address: janemengzhang@vip.163.com.

Abstract

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.

Keywords: Amnestic mild cognitive impairment; Episodic memory; Familiarity; Recollection; Retrieval; Simultaneous EEG-fMRI.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain / diagnostic imaging
Cognitive Dysfunction* / diagnostic imaging
Electroencephalography
Humans
Magnetic Resonance Imaging
Memory, Episodic*
Neuropsychological Tests