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Cortical thickness in right frontal and left lingual gyri differentially mediate episodic memory for spatial contextual details across the adult lifespan

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Cortical thickness in right frontal and left lingual gyri differentially mediate episodic memory for spatial contextual details across the adult lifespan A. Swierkot* 1, 2and M. N. Rajah*2,3 RUNNING HEAD: Episodic memory and cortical thickness across the adult lifespan *Both authors contrib...

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bioRxiv preprint doi: https://doi.org/10.1101/289447. this version posted March 27, 2018. The copyright holder for this preprint (which was not
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

1

Cortical thickness in right frontal and left lingual gyri differentially mediate episodic memory for

spatial contextual details across the adult lifespan

A. Swierkot* 1, 2and M. N. Rajah*2,3

RUNNING HEAD: Episodic memory and cortical thickness across the adult lifespan

*Both authors contributed equally to this manuscript

1Graduate Program, Department of Psychiatry, McGill University

2Brain Imaging Centre, Douglas Mental Health University Institute

3Department of Psychiatry, McGill University

Corresponding author:

M. Natasha Rajah

Room 2114 CIC Pavilion

Douglas Mental Health University Institute

6875 LaSalle Blvd

Montreal, QC, Canada H4H 1R3

,bioRxiv preprint doi: https://doi.org/10.1101/289447. this version posted March 27, 2018. The copyright holder for this preprint (which was not
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

Changes in context memory and cortical thickness across the adult lifespan 2

Abstract

Healthy aging is associated with declines in episodic memory and with widespread cortical thinning.

These parallel declines suggest that age-related changes in cortical thickness may contribute to episodic

memory decline with age. The current study uses a cross-sectional study design to examine whether

regional cortical thickness mediates the relationship between age and episodic memory, as measured by

a context memory task for faces. Mediation and conditional mediation models were tested using

bootstrapping in order to determine how age-associated changes in regional cortical thickness mediated

age-associated changes in performance on the context memory task. We observed that right superior

frontal cortical thickness conditionally mediated spatial context memory only in middle-aged and older

adults; and right caudal middle frontal cortical thickness conditionally mediated context memory only

in older adults. Left lingual cortical thickness mediated spatial context memory across the adult

lifespan, but this effect was most evident at midlife. Right parahippocampal cortical thickness mediated

context memory, independent of age. We conclude that our cortical thickness results were generally

consistent with the posterior-to-anterior shift in aging hypothesis (Davis et al., 2008) for episodic

memory.

,bioRxiv preprint doi: https://doi.org/10.1101/289447. this version posted March 27, 2018. The copyright holder for this preprint (which was not
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

Changes in context memory and cortical thickness across the adult lifespan 3

1. Introduction

Healthy aging is associated with declines in the ability to remember an item or event in rich

contextual detail (episodic memory; Tulving, 1984). Studies have shown that episodic memory tasks

that assess one’s ability to encode and retrieve contextual details (item-context associative memory

tasks) are more sensitive at detecting age-associated episodic memory deficits, compared to item

recognition tasks (Cansino, 2009; Dulas & Duarte, 2012; Glisky, Polster, & Routhieaux, 1995;

Mattson, Wang, de Chastelaine, & Rugg, 2013; Rajah, Languay, & Valiquette, 2010; Schacter,

Kaszniak, Kihlstrom, & Valdiserri, 1991; Trott, Friedman, Ritter, & Fabiani, 1997). FMRI studies of

young adults have shown increased activity in medial temporal lobes (MTL) and prefrontal cortices

(PFC) during associative context memory tasks, compared to item recognition tasks (Davachi, 2006;

Maillet & Rajah, 2013; Shing et al., 2010; Staresina & Davachi, 2008). Moreover, it has been

hypothesized that successful encoding and retrieval of item-context associations in young adults relies

on the engagement of a distributed network of brain regions including sensory cortices, MTL, inferior

parietal cortex (IPC) and PFC (H. Kim, Daselaar, & Cabeza, 2010; Nyberg et al., 2000; Rugg &

Vilberg, 2013). Thus, it follows that age-related decrements in item-context associative memory tasks

may be mediated by structural changes in any (or all) of the brain regions implicated with successful

memory encoding and retrieval in young adults (Braskie, Small, & Bookheimer, 2009; Spencer & Raz,

1994).

Several studies have reported age-related volumetric decline in brain regions related to encoding

and/or retrieval of contextual details from episodic memory (Fjell et al., 2013; Hogstrom, Westlye,

Walhovd, & Fjell, 2013; Raz, Ghisletta, Rodrigue, Kennedy, & Lindenberger, 2010; Walhovd et al.,

2011). Salat et al (2004) reported reductions in cortical thickness with age in PFC, supramarginal

gyrus, and calcarine sulcus, with relative preservation of lateral temporal cortex thickness. Raz et al

, bioRxiv preprint doi: https://doi.org/10.1101/289447. this version posted March 27, 2018. The copyright holder for this preprint (which was not
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

Changes in context memory and cortical thickness across the adult lifespan 4

(2005) also reported a steady decline in PFC grey matter volumes with age, starting in young

adulthood. However, five year longitudinal follow-up data indicated there was notable individual

variability in how PFC volumes changed with age, with some subjects exhibiting volumetric decline,

and other subjects exhibiting either no change or increased PFC volume at five year follow-up (Raz et

al., 2005). In contrast to a general decrease in PFC volumes throughout adulthood, hippocampal

volume decline with age exhibits a non-linear pattern. For example, Walhovd et al (2011) have

reported changes in hippocampal volumes with age resembling an inverted-U shape, which was

suggestive of accelerated volume loss in this region in late midlife onwards. This observation was

corroborated by Fjell et al (2013). Therefore, there is significant evidence that aging is related to

structural decline in several brain regions associated with episodic memory.

However, fewer studies have examined whether age-related declines in brain volume and/or

cortical thickness directly relates to age-related decline in episodic memory tasks. In other words, do

age-related differences in regional cortical thickness or brain volume mediate the effect of age on

memory function? In one study, Walhovd et al. (2006) used a cross-sectional study design to examine

the relationship between cortical thickness and episodic memory, as measured by long-term recall on

the California Verbal Learning Task (CVLT), in a full lifespan sample. Through a whole-brain vertex-

wise analysis they found that after controlling for age, long-term recall was positively associated with

cortical thickness in bilateral gyrus rectus, bilateral medial frontal gyrus, bilateral parieto-occipital

sulcus, bilateral lingual gyri, right temporal and parietal lobes, and left precuneus throughout the adult

lifespan (Walhovd et al., 2006). Importantly, this analysis uncovered these brain-behaviour

relationships after controlling for age, meaning that this analysis explained how individual differences

in cortical thickness related to memory. However, it did not assess whether cortical thickness mediated

the effect of age on memory performance. Head, Rodrigue, Kennedy, & Raz (2008) aimed to answer

this question by conducting a path analysis to test the hypothesis that age-associated changes in

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