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Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults.

ABSTRACT: Memory consolidation occurs via reactivation of a hippocampal index during non-rapid eye movement slow-wave sleep (NREM SWS) which binds attributes of an experience existing within cortical modules. For memories containing emotional content, hippocampal-amygdala dynamics facilitate consolidation over a sleep bout. This study tested if modularity and centrality-graph theoretical measures that index the level of segregation/integration in a system and the relative import of its nodes-map onto central tenets of memory consolidation theory and sleep-related processing. Findings indicate that greater network integration is tied to overnight emotional memory retention via NREM SWS expression. Greater hippocampal and amygdala influence over network organization supports emotional memory retention, and hippocampal or amygdala control over information flow are differentially associated with distinct stages of memory processing. These centrality measures are also tied to the local expression and coupling of key sleep oscillations tied to sleep-dependent memory consolidation. These findings suggest that measures of intrinsic network connectivity may predict the capacity of brain functional networks to acquire, consolidate, and retrieve emotional memories.

SUBMITTER: Chappel-Farley MG

PROVIDER: S-EPMC10634911 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults.

Chappel-Farley Miranda G MG Adams Jenna N JN Betzel Richard F RF Janecek John C JC Sattari Negin S NS Berisha Destiny E DE Meza Novelle J NJ Niknazar Hamid H Kim Soyun S Dave Abhishek A Chen Ivy Y IY Lui Kitty K KK Neikrug Ariel B AB Benca Ruth M RM Yassa Michael A MA Mander Bryce A BA

bioRxiv : the preprint server for biology 20231101

Memory consolidation occurs via reactivation of a hippocampal index during non-rapid eye movement slow-wave sleep (NREM SWS) which binds attributes of an experience existing within cortical modules. For memories containing emotional content, hippocampal-amygdala dynamics facilitate consolidation over a sleep bout. This study tested if modularity and centrality-graph theoretical measures that index the level of segregation/integration in a system and the relative import of its nodes-map onto cent ...[more]

PMID: 37961192

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Project description:Background and objectivesSleep disordered breathing (SDB) has been related to amyloid deposition and an increased dementia risk. However, how SDB relates to medial temporal lobe neurodegeneration and subsequent episodic memory impairment is unclear. Our objective was to investigate the impact of amyloid positivity on the associations between SDB severity, medial temporal lobe subregions, and episodic memory performance in cognitively unimpaired older adults.MethodsData were acquired between 2016 and 2020 in the context of the Age-Well randomized controlled trial of the Medit-Aging European project. Participants older than 65 years who were free of neurologic, psychiatric, or chronic medical diseases were recruited from the community. They completed a neuropsychological evaluation, in-home polysomnography, a Florbetapir PET, and an MRI, including a specific high-resolution assessment of the medial temporal lobe and hippocampal subfields. Multiple linear regressions were conducted to test interactions between amyloid status and SDB severity on the volume of MTL subregions, controlling for age, sex, education, and the ApoE4 status. Secondary analyses aimed at investigating the links between SDB, MTL subregional atrophy, and episodic memory performance at baseline and at a mean follow-up of 20.66 months in the whole cohort and in subgroups stratified according to amyloid status.ResultsWe included 122 cognitively intact community-dwelling older adults (mean age ± SD: 69.40 ± 3.85 years, 77 women, 26 Aβ+ individuals) in baseline analyses and 111 at follow-up. The apnea-hypopnea index interacted with entorhinal (β = -0.81, p < 0.001, pη2 = 0.19), whole hippocampal (β = -0.61, p < 0.001, pη2 = 0.10), subiculum (β = -0.56, p = 0.002, pη2 = 0.08), CA1 (β = -0.55, p = 0.002, pη2 = 0.08), and DG (β = -0.53, p = 0.003, pη2 = 0.08) volumes such that a higher sleep apnea severity was related to lower MTL subregion volumes in amyloid-positive individuals, but not in those who were amyloid negative. In the whole cohort, lower whole hippocampal (r = 0.27, p = 0.005) and CA1 (r = 0.28, p = 0.003) volumes at baseline were associated with worse episodic memory performance at follow-up.DiscussionOverall, we showed that SDB was associated with MTL atrophy in cognitively asymptomatic older adults engaged in the Alzheimer continuum, which may increase the risk of developing memory impairment over time.Trial registration informationClinicalTrials.gov Identifier: NCT02977819.

Dataset Information

Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults.

Publications

Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults.

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