Dataset Information

Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer's disease.

ABSTRACT: Successful episodic memory calls upon a number of different cognitive processes that are supported by the coordination of several large-scale cortical networks. Previous work from our group has demonstrated dissociable anatomic substrates at different stages of memory in patients with dementia due to Alzheimer's disease (AD). The aim of the current study was to extend the understanding of brain-behavior associations underlying a commonly administered neuropsychological assessment of verbal episodic memory (Rey Auditory Verbal Learning Test; RAVLT) by determining the cortical network contributions to the performance at early vs. late stages of list learning, delayed recall, and retention, in 235 very mild biomarker positive (A+/T+/N+) individuals diagnosed with amnestic mild cognitive impairment (aMCI; MMSE = 27.7). We measured cortical atrophy in four large-scale cortical networks impacted by AD: default mode (DMN), dorsal attention (DAN), frontoparietal (FPN), and language (LN) networks. We also evaluated the role of hippocampal atrophy at each stage of memory performance. Partial correlation analyses controlling for age, sex, and education and corrected for multiple comparisons revealed that early learning was most strongly associated with cortical thickness in the DAN, while late learning was most strongly associated with hippocampal volume, but also related to cortical thickness in the DAN, FPN, DMN, and LN. Delayed recall was associated most strongly with hippocampal volume, but was also related to cortical thickness in the FPN and DMN, while retention was associated only with hippocampal volume. These findings are consistent with prior models of the neural substrates of different stages of verbal list learning and retrieval, provide new insights into the cortical networks undergoing neurodegeneration even at very mild stages of prodromal AD, and inform our thinking about the networks and regions being interrogated by this kind of neuropsychological assessment of episodic memory.

SUBMITTER: Putcha D

PROVIDER: S-EPMC6571167 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer's disease.

Putcha Deepti D Brickhouse Michael M Wolk David A DA Dickerson Bradford C BC

Neuropsychologia 20190328

Successful episodic memory calls upon a number of different cognitive processes that are supported by the coordination of several large-scale cortical networks. Previous work from our group has demonstrated dissociable anatomic substrates at different stages of memory in patients with dementia due to Alzheimer's disease (AD). The aim of the current study was to extend the understanding of brain-behavior associations underlying a commonly administered neuropsychological assessment of verbal episo ...[more]

PMID: 30930301

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Project description:The aim of this study was to determine the neural correlates of different stages of episodic memory function and their modulation by Alzheimer's disease (AD). Several decades of work has supported the role of the medial temporal lobes (MTL) in episodic memory function. However, a more recent work, derived in part from functional neuroimaging studies, has suggested that other brain structures make up a large-scale network that appears to support successful encoding and retrieval of episodic memories. Furthermore, controversy exists as to whether dissociable MTL regions support qualitatively different aspects of memory (hippocampus: contextual memory or 'recollection'; perirhinal/lateral entorhinal cortex: item memory or 'familiarity'). There is limited neuropsychological support for these models and most work in AD only has examined free recall memory measures. We studied the relationship between performance on different stages of the Rey Auditory Verbal Learning Test (AVLT), a 15-item word list learning task, and structural MRI measures in mild AD patients. Structural measures included hippocampal volume and cortical thickness of several ROIs known to undergo atrophy in AD. Correlation and multiple regression analyses, controlling for age, education, and gender, were performed in 146 mild AD patients (MMSE 23.3±2.0). To evaluate the robustness of these relationships, similar analyses were performed with additional standardized verbal memory measures. Early immediate recall trials (e.g. Trial 1 of the AVLT) were not associated with the size of MTL regions, but correlated most strongly with inferior parietal, middle frontal gyrus, and temporal pole ROIs. After repeated exposure (e.g. Trial 5 of the AVLT), immediate recall was correlated with both MTL and a similar distribution of isocortical structures, but most strongly the temporal pole. For delayed recall, only the hippocampus correlated with performance. In contrast, for delayed recognition discrimination, the perirhinal/entorhinal cortex correlated more strongly than the hippocampus; no other isocortical regions were strongly associated with performance. Convergent results were found for immediate and delayed trials of other memory tests. The current results suggest that a richer understanding of the memory deficits in AD can be gained by examining multiple measures, which tap different aspects of memory function. Furthermore, the present findings are consistent with models hypothesizing different stages of verbal list learning map onto dissociable brain regions. These data have implications for understanding the anatomic basis of processes underlying episodic memory, particularly related to a division of labor within the medial temporal lobes and within the large-scale MTL-cortical memory network.

Project description:Network-sensitive neuroimaging methods have been used to characterize large-scale brain network degeneration in Alzheimer's disease and its prodrome. However, few studies have investigated the combined effect of Alzheimer's disease and cerebrovascular disease on brain network degeneration. Our study sought to examine the intrinsic functional connectivity and structural covariance network changes in 235 prodromal and clinical Alzheimer's disease patients with and without cerebrovascular disease. We focused particularly on two higher-order cognitive networks-the default mode network and the executive control network. We found divergent functional connectivity and structural covariance patterns in Alzheimer's disease patients with and without cerebrovascular disease. Alzheimer's disease patients without cerebrovascular disease, but not Alzheimer's disease patients with cerebrovascular disease, showed reductions in posterior default mode network functional connectivity. By comparison, while both groups exhibited parietal reductions in executive control network functional connectivity, only Alzheimer's disease patients with cerebrovascular disease showed increases in frontal executive control network connectivity. Importantly, these distinct executive control network changes were recapitulated in prodromal Alzheimer's disease patients with and without cerebrovascular disease. Across Alzheimer's disease patients with and without cerebrovascular disease, higher default mode network functional connectivity z-scores correlated with greater hippocampal volumes while higher executive control network functional connectivity z-scores correlated with greater white matter changes. In parallel, only Alzheimer's disease patients without cerebrovascular disease showed increased default mode network structural covariance, while only Alzheimer's disease patients with cerebrovascular disease showed increased executive control network structural covariance compared to controls. Our findings demonstrate the differential neural network structural and functional changes in Alzheimer's disease with and without cerebrovascular disease, suggesting that the underlying pathology of Alzheimer's disease patients with cerebrovascular disease might differ from those without cerebrovascular disease and reflect a combination of more severe cerebrovascular disease and less severe Alzheimer's disease network degeneration phenotype.

Dataset Information

Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer's disease.

Publications

Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer's disease.

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