Hippocampal and Parahippocampal Gray Matter Structural Integrity Assessed by Multimodal Imaging Is Associated with Episodic Memory in Old Age

Ylva Köhncke,Myriam C Sander,Sandra Düzel,Andreas M Brandmaier,Simone Kühn,Ulman Lindenberger

doi:10.1093/cercor/bhaa287

Abstract

Maintained structural integrity of hippocampal and cortical gray matter may explain why some older adults show rather preserved episodic memory. However, viable measurement models for estimating individual differences in gray matter structural integrity are lacking; instead, findings rely on fallible single indicators of integrity. Here, we introduce multitrait–multimethod methodology to capture individual differences in gray matter integrity, based on multimodal structural imaging in a large sample of 1522 healthy adults aged 60–88 years from the Berlin Aging Study II, including 333 participants who underwent magnetic resonance imaging. Structural integrity factors expressed the common variance of voxel-based morphometry, mean diffusivity, and magnetization transfer ratio for each of four regions of interest: hippocampus, parahippocampal gyrus, prefrontal cortex, and precuneus. Except for precuneus, the integrity factors correlated with episodic memory. Associations with hippocampal and parahippocampal integrity persisted after controlling for age, sex, and education. Our results support the proposition that episodic memory ability in old age benefits from maintained structural integrity of hippocampus and parahippocampal gyrus. Exploratory follow-up analyses on sex differences showed that this effect is restricted to men. Multimodal factors of structural brain integrity might help to improve our biological understanding of human memory aging.

Highlights

Performance in episodic memory tasks typically declines after the age of 60 years (Schaie et al 1998; Rönnlund et al 2005), but there are pronounced age-related individual differences in levels and changes of performance (de Frias et al 2007; Josefsson et al 2012), with some older individuals displaying little or no performance decline
Structural integrity factors expressed the common variance of voxel-based morphometry, mean diffusivity, and magnetization transfer ratio for each of four regions of interest: hippocampus, parahippocampal gyrus, prefrontal cortex, and precuneus
In studies using magnetization transfer (MT) imaging, it could be shown that a higher MT ratio, indicating denser microstructure, is related to lower mean diffusivity (MD) (Düzel et al 2010), faster processing speed, and higher fluid intelligence (Aribisala et al 2014), but not better memory (Düzel et al 2010, 2008; Aribisala et al 2014). Taken together, these findings suggest that the macro- and micro-structural integrity of hippocampus might be critical for preserving its functionality for episodic memory in older age

Summary

Introduction

Performance in episodic memory tasks typically declines after the age of 60 years (Schaie et al 1998; Rönnlund et al 2005), but there are pronounced age-related individual differences in levels and changes of performance (de Frias et al 2007; Josefsson et al 2012), with some older individuals displaying little or no performance decline. Modern neuroimaging techniques allow us to better describe and understand various characteristics of brain tissue through the application of different imaging modalities such as structural and functional magnetic resonance imaging (MRI), diffusion tensor imaging (DTI), or positron-emission tomography (PET). It is unclear whether these measures converge on constructs that reflect the “integrity” of a given brain region. Longitudinal studies show that less decline over time in hippocampal volume in older adults is related to less decline in episodic memory performance (Persson et al 2012; Gorbach et al 2017). Similar results were found at the functional level, such that smaller decrements in activation were associated with better preservation of memory performance (Persson et al 2012)

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