Distinct resting-state functional connections associated with episodic and visuospatial memory in older adults

Sana Suri, Anya Topiwala, Nicola Filippini, Enikő Zsoldos, Abda Mahmood, Claire E Sexton, Archana Singh-Manoux, Mika Kivimäki, Clare E Mackay, Stephen Smith, Klaus P Ebmeier, Sana Suri, Anya Topiwala, Nicola Filippini, Enikő Zsoldos, Abda Mahmood, Claire E Sexton, Archana Singh-Manoux, Mika Kivimäki, Clare E Mackay, Stephen Smith, Klaus P Ebmeier

Abstract

Episodic and spatial memory are commonly impaired in ageing and Alzheimer's disease. Volumetric and task-based functional magnetic resonance imaging (fMRI) studies suggest a preferential involvement of the medial temporal lobe (MTL), particularly the hippocampus, in episodic and spatial memory processing. The present study examined how these two memory types were related in terms of their associated resting-state functional architecture. 3T multiband resting state fMRI scans from 497 participants (60-82 years old) of the cross-sectional Whitehall II Imaging sub-study were analysed using an unbiased, data-driven network-modelling technique (FSLNets). Factor analysis was performed on the cognitive battery; the Hopkins Verbal Learning test and Rey-Osterreith Complex Figure test factors were used to assess verbal and visuospatial memory respectively. We present a map of the macroscopic functional connectome for the Whitehall II Imaging sub-study, comprising 58 functionally distinct nodes clustered into five major resting-state networks. Within this map we identified distinct functional connections associated with verbal and visuospatial memory. Functional anticorrelation between the hippocampal formation and the frontal pole was significantly associated with better verbal memory in an age-dependent manner. In contrast, hippocampus-motor and parietal-motor functional connections were associated with visuospatial memory independently of age. These relationships were not driven by grey matter volume and were unique to the respective memory domain. Our findings provide new insights into current models of brain-behaviour interactions, and suggest that while both episodic and visuospatial memory engage MTL nodes of the default mode network, the two memory domains differ in terms of the associated functional connections between the MTL and other resting-state brain networks.

Keywords: Connectomics; Hippocampus; Network modelling; Resting-state fMRI; Verbal memory; Visuospatial memory.

Copyright © 2017 The Authors. Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
The resting-state functional connectome estimated for 497 participants of the Whitehall II Imaging sub-study. High-dimensionality group ICA and network modelling were performed using the FSL-MELODIC and FSLNETS tools respectively. Z statistics for the full correlation (below the diagonal) and partial correlation (above the diagonal) were computed for the 58 nodes visualized at the top of each column. The nodes were reordered according to a hierarchical clustering of the full correlation matrix. Five clusters representing commonly observed resting-state networks are highlighted in black boxes and labelled at the top of the figure. The partial correlation netmats were used in the linear regression with memory.
Fig. 2
Fig. 2
Distinct resting-state connections representing episodic and visuospatial memory. (a) Verbal memory was significantly negatively correlated with temporal-frontal anticorrelation. Visuospatial memory was significantly positively correlated with (b) motor-parietal connectivity and (c) motor-hippocampal connectivity. The colour of the bar connecting the two nodes represents the sign of the group-average partial correlation (red: positive, blue: negative). Each subject's partial correlation edge strengths are plotted against the corresponding memory factor on the right. All images are thresholded at z > 4 for visualisation.

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