Neural evidence for age-related differences in representational quality and strategic retrieval processes

Alexandra N Trelle,Richard N Henson,Jon S Simons

doi:10.1016/j.neurobiolaging.2019.07.012

Abstract

Mounting behavioral evidence suggests that declines in both representational quality and controlled retrieval processes contribute to episodic memory decline with age. The present study sought neural evidence for age-related change in these factors by measuring neural differentiation during encoding of paired associates and changes in regional blood oxygenation level–dependent activity and functional connectivity during retrieval conditions that placed low (intact pairs) and high (recombined pairs) demands on controlled retrieval processes. Pattern similarity analysis revealed age-related declines in the differentiation of stimulus representations at encoding, manifesting as both reduced pattern similarity between closely related events and increased pattern similarity between distinct events. During retrieval, both groups increased recruitment of areas within the core recollection network when endorsing studied pairs, including the hippocampus and angular gyrus. In contrast, only younger adults increased recruitment of, and hippocampal connectivity with, lateral prefrontal regions during correct rejections of recombined pairs. These results provide evidence for age-related changes in representational quality and in the neural mechanisms supporting memory retrieval under conditions of high, but not low, control demand.

Highlights

Episodic memory declines in late adulthood; not all aspects of memory are affected to the same degree
We found that reducing demands on either the precision of representational content or recollection-based retrieval processes did not eliminate age-related memory deficits
We examined functional connectivity between the hippocampus and these cortical regions, which we predicted would vary as a function of strategic retrieval demand (Barredo et al, 2015; Bowman & Dennis, 2017)

Summary

Introduction

Episodic memory declines in late adulthood; not all aspects of memory are affected to the same degree. Age-related differences in behavioral measures of recall-to-accept are often smaller in magnitude compared to measures of recall-to-reject (Cohn et al, 2008; Trelle et al, 2017) This pattern suggests that instead of a generalized deficit in recollection-based retrieval processes, older adults’ ability to recall stored details may vary according to demands on strategic processes at test. If older adults’ ability to access stored details to support recognition varies as a function of strategic retrieval demand at test, we should observe an age-invariant neural signature associated with target recollection, that is, increased activity in the hippocampus and angular gyrus during hits relative to correct rejections, coupled with age-related reduction in the mechanisms associated with recall-to-reject, that is, a failure to increase recruitment of DLPFC and VLPFC, and hippocampal-VLPFC connectivity during correct rejections relative to hits. We examined the effects of age on: 1) the differentiation of event representations in ventral temporal cortex during encoding, and how this is modulated by stimulus relatedness, 2) the degree to which the recruitment of “retrieval success” regions (e.g., HIPP, ANG) and “retrieval control” regions (e.g. DLPFC, VLPFC) is modulated by strategic demand during retrieval, and 3) the degree to which HIPP connectivity with these lateral cortical regions (ANG, DLPFC, VLPFC) varies as a function of strategic demand at retrieval

Method Participants

Behavioural Results

31 Supplementary