Electrophysiological Processes on Motor Imagery Mediate the Association Between Increased Gray Matter Volume and Cognition in Amnestic Mild Cognitive Impairment
Motor imagery is considered as an ideal window to observe neural processes of action representations. Behavioral evidence has indicated an alteration of motor imagery in amnestic mild cognitive impairment (aMCI). However, it still remains unclear on the altered neurophysiological processing mechanism of motor imagery and whether this mechanism links the abnormal biological basis of motor imagery with impaired cognition in aMCI. This study was to investigate the altered neurophysiological processing mechanism of motor imagery and to examine the relationships between this knowledge and the altered structural basis of motor imagery with impaired cognition in aMCI. A hand mental rotation paradigm was used to manipulate the processing of motor imagery while event-related brain potentials (ERPs) were recorded and gray matter (GM) voxel-based morphometry was performed in 20 aMCI and 29 healthy controls. Compared with controls, aMCI exhibited lower ERP amplitudes in parietal cortex and higher ERP amplitudes in frontal cortex during motor imagery. In addition, aMCI showed reduced GM volumes in cerebellum posterior lobe, insula and hippocampus/parahippocampal gyrus, and increased GM volumes in middle cingulate gyrus and superior frontal gyrus. Most importantly, increased ERP amplitude significantly mediated the association between increased GM and cognition. This study provided a novel evidence for the relationships between the electrophysiological processing mechanism and structural basis of motor imagery with impaired cognition in aMCI. It suggests that improving neural activity by stimulating the frontal lobe can potentially contribute to acquire motor imagery skills for neurological rehabilitation in aMCI subjects.
KeywordsAmnestic mild cognitive impairment Motor imagery Event-related brain potential MRI Structural equation model Mediating effect
This study was supported by the National Natural Science Foundation of China (Nos. 81420108012, 81500919, 81671046, and 81701675), the Disciplinary group of Psychology and Neuroscience, Xinxiang Medical University (No. 2016PNKFKT-01), the Nanjing Medical Science and Technology Development Foundation-Nanjing Outstanding Youth Fund Projects (No. JQX18005), the Cooperative Research Project of Southeast University-Nanjing Medical University (No. 2018DN0031), the Key Research and Development Plan (Social Development) Project of Jiangsu Province (No. BE2018608), and Humanities and Social Science Research Project of Henan Colleges and Universities (2017-ZZJH-423).
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Conflict of interest
All authors have made substantial intellectual contribution to this paper in one or more of the following areas that included design or conceptualization of the study, analysis or interpretation of the data, or drafting or revising the manuscript. All authors contributed to the work, agree with the presented findings, and declare that they have no conflicts of interest, financial or otherwise, directly or indirectly related to this work.
- Albers MW, Gilmore GC, Kaye J, Murphy C, Wingfield A, Bennett DA, Boxer AL, Buchman AS, Cruickshanks KJ, Devanand DP, Duffy CJ, Gall CM, Gates GA, Granholm AC, Hensch T, Holtzer R, Hyman BT, Lin FR, McKee AC, Morris JC, Petersen RC, Silbert LC, Struble RG, Trojanowski JQ, Verghese J, Wilson DA, Xu S, Zhang LI (2015) At the interface of sensory and motor dysfunctions and Alzheimer’s disease. Alzheimers Dement 11:70–98PubMedCrossRefGoogle Scholar
- Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:270–279PubMedPubMedCentralCrossRefGoogle Scholar
- Chen J, Wei D, Yang L, Wu X, Ma W, Fu Q, Wang H, Liu G, Deng Z, Ye M, Zhang Y, Zhang Z (2015b) Neurocognitive impairment on motor imagery associated with positive symptoms in patients with first-episode schizophrenia: evidence from event-related brain potentials. Psychiatry Res 231:236–243PubMedCrossRefGoogle Scholar
- Cronin-Golomb A, Amick MM (2001) Spatial abilities in aging, Alzheimer’s disease, and Parkinson’s disease. Elsevier, AmsterdamGoogle Scholar
- Jack CR Jr, Wiste HJ, Vemuri P, Weigand SD, Senjem ML, Zeng G, Bernstein MA, Gunter JL, Pankratz VS, Aisen PS, Weiner MW, Petersen RC, Shaw LM, Trojanowski JQ, Knopman DS, Alzheimer’s Disease Neuroimaging I (2010) Brain beta-amyloid measures and magnetic resonance imaging atrophy both predict time-to-progression from mild cognitive impairment to Alzheimer’s disease. Brain 133:3336–3348PubMedPubMedCentralCrossRefGoogle Scholar
- Morra JH, Tu Z, Apostolova LG, Green AE, Avedissian C, Madsen SK, Parikshak N, Toga AW, Jack CR Jr, Schuff N, Weiner MW, Thompson PM, Alzheimer’s Disease Neuroimaging I (2009) Automated mapping of hippocampal atrophy in 1-year repeat MRI data from 490 subjects with Alzheimer’s disease, mild cognitive impairment, and elderly controls. Neuroimage 45:S3–15PubMedCrossRefGoogle Scholar
- Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8:4049–4068PubMedPubMedCentralCrossRefGoogle Scholar
- Spearman C (1932) The abilities of man: their nature and measurement. Macmillan & Co, LondonGoogle Scholar
- Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Wagster MV, Phelps CH (2011) Toward defining the preclinical stages of Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:280–292PubMedPubMedCentralCrossRefGoogle Scholar