Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex

Pénélope Martinelli,Stéphanie Lion,Jean François Meder,Isabelle Amado,Thierry Gallarda,Anne-Dominique Devauchelle,Sandrine Kalenzaga,Marco Sperduti,Pascale Piolino,Marion Delhommeau,Adèle Anssens,Catherine Oppenheim,Marie-Odile Krebs,Emmanuel Andreas Stamatakis

doi:10.1371/journal.pone.0082385

Abstract

Age-related changes in autobiographical memory (AM) recall are characterized by a decline in episodic details, while semantic aspects are spared. This deleterious effect is supposed to be mediated by an inefficient recruitment of executive processes during AM retrieval. To date, contrasting evidence has been reported on the neural underpinning of this decline, and none of the previous studies has directly compared the episodic and semantic aspects of AM in elderly. We asked 20 young and 17 older participants to recall specific and general autobiographical events (i.e., episodic and semantic AM) elicited by personalized cues while recording their brain activity by means of fMRI. At the behavioral level, we confirmed that the richness of episodic AM retrieval is specifically impoverished in aging and that this decline is related to the reduction of executive functions. At the neural level, in both age groups, we showed the recruitment of a large network during episodic AM retrieval encompassing prefrontal, cortical midline and posterior regions, and medial temporal structures, including the hippocampus. This network was very similar, but less extended, during semantic AM retrieval. Nevertheless, a greater activity was evidenced in the dorsal anterior cingulate cortex (dACC) during episodic, compared to semantic AM retrieval in young participants, and a reversed pattern in the elderly. Moreover, activity in dACC during episodic AM retrieval was correlated with inhibition and richness of memories in both groups. Our findings shed light on the direct link between episodic AM retrieval, executive control, and their decline in aging, proposing a possible neuronal signature. They also suggest that increased activity in dACC during semantic AM retrieval in the elderly could be seen as a compensatory mechanism underpinning successful AM performance observed in aging. These results are discussed in the framework of recently proposed models of neural reorganization in aging.

Highlights

The study of autobiographical memory (AM) constitutes an ecological approach to investigate long term declarative memory based on real-life events
It encompasses both episodic autobiographical memories (EAM), which consists of specific events in a particular spatio-temporal context, for which we can mentally travel back in time, and re-experience the encoding context, and semantic autobiographical memory (SAM), which stores general knowledge of the self as well as general events, information we are aware of in the absence of specific recollection [1–4]
We reported a correlation between the percent signal change in the dorsal anterior cingulate cortex (dACC), and autobiographical and neuropsychological scores, for each group and each condition

Summary

Introduction

The study of autobiographical memory (AM) constitutes an ecological approach to investigate long term declarative memory based on real-life events. The healthy elderly have a reduced capacity of recollection of specific events, regularly providing general events. We reported that the elderly showed increasing difficulty to access deeper levels of specificity of AM and that this effect was mediated by performance on executive functions (i.e. updating and inhibition) and working memory [20]. These findings are in keeping with the well established age-related deficits in prefrontal functions [21–22]

Objectives

Methods

Results

Conclusion