Table 1.
Structural MRI correlates of episodic memory
| Author, year | Study groups | Episodic memory test | Imaging analysis method | Imaging correlates of episodic memory |
|---|---|---|---|---|
| Preclinical AD | ||||
| Jagust, et al 2006 [8] | 60 CNC (6 dementia or MCI converters) (2-year follow-up) | Word list | HC and entorhinal cortex volumetry/FDG-PET | HC and entorhinal cortex volume predicted delayed recall decline over time. |
| Lind, et al 2006 [9] | 30 APOE ε4 carrier, 30 noncarrier CNC | Word categorization task | HC volumetry | R HC volume negatively correlated with number of false alarms in APOE ε4 carriers. |
| Westlye, et al 2012 [10] | 31 APOE ε4 carrier, 61 noncarrier CNC (3-4 year follow-up) | CVLT-II | Entorhinal cortex, parahippocampal gyrus thickness and WM volumetry, DTI | Entorhinal WM FA positively correlated with memory in the APOE ε4 carriers. |
| Zhuang, et al 2012 [11] | 193 CNC (20 aMCI converters in 2 years) | Logical Memory, RAVLT | VBM, DTI | Lower baseline L parahippocampal cingulum, inferior temporal lobe WM, parahippocampal gyrus, thalamus FA associated with worse verbal memory decline. L parahippocampal gyrus WM was predictive of subsequent memory decline. |
| Dowell, et al 2016 [12] | 21 APOE ε4 carrier, 20 noncarrier young CNC, and 17 APOE ε4 carrier, 20 noncarrier mid-age CNC | Word list | HC and parahippocampus thickness, WM volumetry | Parahippocampal thickness positively correlated with memory in young APOE ε4 carriers. |
| MCI | ||||
| Chetelat, et al 2003 [13] | 21 aMCI | Word list | VBM/FDG-PET | HC volume positively correlated with memory. |
| Stoub, et al 2006 [14] | 40 aMCI, 50 CNC | East Boston Story, WMS-R, CERAD-WL | HC and entorhinal cortex volumetry, WM VBM | Entorhinal cortex, HC and total parahippocampal WM were significant predictors of memory. |
| Goldstein, et al 2009 [15] | 14 aMCI, 9 CNC | CERAD-WL, Story A of Logical Memory, BVMT-R | DTI | Temporal and whole brain apparent diffusion coefficient negatively, whole brain FA positively correlated with verbal memory in aMCI. |
| Wang, et al 2009 [16] | 10 MCI (4 ADD converters in 3 years), 12 CNC | CERAD-WL, Logical Memory | HC, parahippocampal gyrus, amygdala volumetry, lobar masking method for frontal, lateral temporal, parietal occipital ROIs/SPECT | MTL volume positively correlated with memory. |
| Zhuang, et al 2012 [17] | 76 aMCI, 51 naMCI, 206 CNC | Logical Memory, RAVLT, Benton Visual Retention Test | HC DBM, fornix DTI | L fornix radial diffusivity negatively correlated with verbal memory. |
| Meyer, et al 2013 [18] | 25 aMCI | CERAD, CANTAB, WMS-R | VBM | Temporal WM volume positively correlated with pattern recognition. Parahippocampal gyrus and L precuneus WM volume positively correlated with story recall. |
| Fujishima, et al 2014 [19] | 186 MCI, 136 CNC | Logical Memory II | Cortical thickness, WMH probability map of the whole brain | L entorhinal cortex thickness positively; WMH volume in the posterior periventricular regions and near the R anterior horn of the lateral ventricle negatively correlated with memory. |
| Remy, et al 2015 [20] | 22 aMCI, 15 CNC | RCFT, DMS48 test | HC volumetry, DTI | L uncinate fasciculus FA positively correlated with recognition. |
| Peter, et al 2016 [21] | 20 MCI, 20 CNC | Verbal Learning and Memory Test | HC and basal forebrain cholinergic system volumetry | HC volume positively correlated with memory. |
| Gyebnar, et al 2018 [22] | 18 aMCI, 20 naMCI, 27 CNC | CANTAB, RAVLT | Voxel- and ROI-based DTI | Voxel-based: R inferior frontal gyrus pars triangularis FA negatively correlated with visual memory. L parahippocampal gyrus MD negatively correlated with verbal memory. ROI-based: Left cingulum MD negatively correlated with verbal memory, and L stria terminalis/crus of the fornix MD positively correlated with visual memory. |
| ADD | ||||
| Deweer, et al 1995 [23] | 18 ADD | WMS, CVLT, Grober and Buschke test | Hippocampal formation, amygdala, caudate nucleus, and ventricle volumetry | Hippocampal formation volume positively correlated with memory. |
| Kramer, et al 2005 [24] | 13 ADD, 11 frontotemporal dementia, 10 semantic dementia, 8 CNC | CVLT | HC, frontal, anterior temporal lobes, and posterior cortex volumetry | HC volume was the only predictor of delayed recall. |
| Sarazin, et al 2010 [25] | 35 ADD | The Free and Cued Selective Reminding Test | VBM, HC volumetry, and three-dimensional hippocampal surface-based shape analysis | VBM: L MTL, and thalamus volume positively correlated with total recall. Automatic hippocampal volumetry: L HC volume positively correlated with total recall. Three-dimensional hippocampal surface-based shape analysis: HC CA1 field volume positively correlated with free and total recall. |
| Yakushev, et al 2010 [26] | 20 ADD, 18 CNC | CERAD | HC volumetry and diffusivity | L body-tail volume positively correlated with recall in ADD. L head diffusivity negatively correlated with delayed verbal recall. |
| Wolk, et al 2011 [27] | 146 ADD | RAVLT, Logical Memory, ADAS-Cog-Word list | Rostral MTL, rostral inferior temporal gyrus, temporal pole, angular gyrus, supramarginal gyrus, superior parietal lobule, precuneus, superior frontal gyrus, inferior frontal sulcus/caudal middle frontal gyrus thickness | HC, MTL, caudal middle frontal gyrus, temporal pole thickness positively correlated with memory. |
| Irish, et al 2012 [28] | 11 ADD, 11 semantic dementia, 10 CNC | Modified version of the past–future task | VBM | R frontal pole, R PCG and precuneus, L inferior temporal and L middle frontal gyri volume positively correlated with past retrieval in ADD and CNC. |
| Kerchner, et al 2012 [29] | 9 ADD | HVLT-R, BVMT-R, Logical Memory | CA1-SP, CA1-SRLM, and entorhinal cortex thickness; DG/CA3 and hippocampal cross-sectional area (proxy for total HC volume) volumetry | CA1- SRLM and entorhinal cortex width, HC volume positively correlated with recall. |
| Dore, et al 2013 [30] | 40 ADD, 93 CNC | CVLT-II, Logical Memory II | HC, temporal lobe, precuneus and PCG thickness combined with a voxel-based approach/PiB PET | R temporal lobe and R precuneus/PCG thickness positively correlated with memory in CNC with high PiB retention. HC thickness positively correlated with memory in both CNC groups. |
| Irish, et al 2013 [31] | 10 ADD, 10 frontotemporal dementia, 10 CNC | Modified version of the past–future task | VBM | L PCG volume positively correlated with past retrieval in ADD and CNC. |
| MCI and ADD | ||||
| Fellgiebel, et al 2005 [32] | 17 aMCI, 25 ADD, 21 CNC | Delayed verbal recall test | DTI | PCG bundle FA positively, MD negatively correlated with memory. |
| Leube, et al 2008 [33] | 21 MCI, 12 ADD, 29 CNC | Verbal learning and memory test | VBM | HC, L perirhinal cortex, L parahippocampal gyrus, L ventral anterior cingulate and R posterior entorhinal cortex, R middle temporal gyrus volume positively correlated with memory. |
| Sexton, et al 2010 [34] | 8 MCI, 7 ADD, 8 CNC | HVLT-R, RCFT | HC volumetry, cingulum and fornix DTI | HC volume, L crus of the fornix FA positively; cingulate gyrus MD negatively correlated with memory. |
| Molinuevo, et al 2011 [35] | 24 aMCI, 27 MCI (ADD converters in 2 years), 31 ADD, 27 CNC | CERAD-recall of constructional praxis, delayed text memory, memory alteration tests | VBM | L lateral, medial, inferior, and R medial, inferior gyri volume positively correlated with memory over time. L medial temporal gyrus positively correlated with delayed text memory. |
| Bosch, et al 2012 [36] | 16 aMCI, 15 ADD, 15 CNC | CERAD-recall of constructional praxis, Grober and Buschke test | DTI | Whole brain FA positively correlated with memory. |
| Kerchner, et al 2013 [37] | 15 aMCI, 11 ADD, 9 young CNC, 18 old CNC | HVLT-R, BVLT-R, Logical Memory | CA1-SP, CA1-SRLM, and entorhinal cortex thickness; DG/CA3 and hippocampal cross-sectional area volumetry | CA1-SRLM width positively correlated with recall in aMCI. |
| Defrancesco, et al 2014 [38] | 14 MCI, 13 MCI (ADD converters), 28 CNC | CERAD-WL, CERAD-figural memory | GM and WM VBM, MD reflected by apparent diffusion coefficient maps | L putamen and inferior frontal gyrus volume positively correlated with verbal memory in ADD converters. |
| Bonner-Jackson, et al 2015 [39] | 82 aMCI, 13 naMCI, 72 other neurological disorders, 34 ADD, 25 CNC | HVLT-R, BVMT-R | HC volumetry | Bilateral HC volume positively correlated with memory. HC volume positively correlated with non-verbal memory in aMCI. |
| Gomar, et al 2017 [40] | 9 aMCI, 9 ADD, 44 CNC | Relational and item-specific encoding task | Entorhinal, perirhinal, parahippocampal cortices thickness, HC volumetry | HC volume, perirhinal and parahippocampal thickness predicted encoding performance. |
| Reas, et al 2017 [41] | 12 MCI, 13 ADD, 31 CNC | WMS-R, CVLT, CERAD | Restriction spectrum imaging in fiber tracts, HC and entorhinal cortex GM; DTI | Fornix, uncinated, inferior fronto-occipital, inferior longitudinal and arcuate fasciculi neurite density positively correlated with recall. HC and entorhinal cortex isotropic free water diffusion negatively correlated with memory. |
Abbreviations: MCI, mild cognitive impairment; APOE ε4, apolipoprotein E ε4; CNC, cognitively normal control; aMCI, amnestic mild cognitive impairment; ADD, Alzheimer's disease dementia; naMCI, nonamnestic mild cognitive impairment; CVLT, California Verbal Learning Test; RAVLT, Rey Auditory Verbal Learning Test; WMS-R, Wechsler Memory Scale-Revised; CERAD, Consortium to Establish a Registry for Alzheimer's Disease; CERAD-WL, CERAD-Word list; BVMT-R, Brief Visuospatial Memory Test-Revised; CANTAB, Cambridge Neuropsychological Test Automated Battery; RCFT, Rey Complex Figure Test; DMS48, delayed matching to sample-48 items; ADAS-Cog, Alzheimer's Disease Assessment Scale-cognitive subscale; HVLT-R, Hopkins Verbal Learning Test-Revised; HC, hippocampus; FDG-PET, fluorodeoxyglucose positron emission tomography; WM, white matter; DTI, diffusion tensor imaging; VBM, voxel-based morphometry; ROI, region of interest; SPECT, single-photon emission computed tomography; DBM, deformation based morphometry; WMH, white matter hyperintensity; MTL, medial temporal lobe; CA, cornu ammonis; CA1-SP, CA1-stratum pyramidale; CA1-SRLM, CA1-stratum radiatum/stratum lacunosum-moleculare; DG/CA3, dentate gyrus/CA3; PCG, posterior cingulate gyrus; PiB PET, Pittsburgh compound B PET; GM, gray matter; MD, mean diffusivity; R, right; L, left; FA, fractional anisotropy.