Age-related alterations of default mode network in autobiographical memory: Recent versus remote events

https://doi.org/10.1016/j.nlm.2020.107341Get rights and content

Highlights

  • Older adults’ vividness ratings were less sensitive to temporal distance.

  • The age-by-temporal distance effect was located in the left precuneus.

  • Young adults had more precuneus activation for recent than for remote events.

  • Young adults’ precuneus activation correlated with vividness ratings for recent AMs.

  • Older adults’ temporal distance effect was reflected in the aDMN-pDMN coupling.

Abstract

Previous studies have shown that the vividness of autobiographical memory decreases over time, and older adults often retrieve fewer details than young adults. However, the age-by-temporal distance (i.e., recent versus remote events) effect on autobiographical memory and underlying neural mechanisms are less understood. We recruited 25 young adults and 27 older adults to perform an fMRI-adapted autobiographical memory task with different temporal distances. The results showed that older adults’ vividness ratings were generally higher than that of young adults, but were less sensitive to temporal distances. For neural imaging, an age-by-temporal distance effect was found in the left precuneus, manifested as young adults had more activation for recent events than for remote events, whereas no temporal distance effect was found in older adults. Interestingly, for older adults, the temporal distance effect was reflected by functional connectivity within the default mode network (DMN), with a stronger anterior DMN-posterior DMN coupling for remote events than for recent events, whereas no temporal distance difference on functional connectivity was found in young adults. The results suggest that older adults exhibit age-related neural differences in both activation and functional connectivity during the processing of autobiographical memory with different temporal distances, shedding new light for the understanding of the relationship between the DMN, autobiographical memory, and aging.

Introduction

Autobiographical memory refers to our ability to recall and re-experience the lifetime we have experienced at a specific moment and place in the past (Tulving, 1983). This ability is likely to be unique to humans, as it is related to the self-consciousness in subjective time (Tulving, 2002). Meanwhile, the richness of details of autobiographical memory decreases with time passes (Levine et al., 2002), and recent autobiographical memories (AMs) are more vivid than remote AMs (Barry et al., 2018, Janssen et al., 2011). With advanced age, older adults retrieve fewer details of autobiographical memory than young adults (Gaesse et al., 2011, Levine et al., 2002), whereas their subjective vividness ratings of past events are similar to or even higher than that of young adults (Comblain et al., 2005, Folville et al., 2020, Janssen et al., 2011). However, the age-by-temporal distance (i.e., recent versus remote) effect on autobiographical memory and underlying neural mechanisms are less understood.

Neuroimaging studies have found that brain regions involved in autobiographical memory have a large overlap with the default mode network (DMN; Philippi et al., 2015, Spreng et al., 2009). The DMN has been found to be activated during resting-state, but is deactivated in tasks that have cognitive requirements (Buckner et al., 2008, Gusnard et al., 2001). The DMN consists of two subsystems (Xu et al., 2016), i.e., the anterior default mode network (aDMN) and posterior default mode network (pDMN). The aDMN, including the medial prefrontal cortex (mPFC), dorsal medial prefrontal cortex (dmPFC), anterior cingulate cortex, anterior temporal lobe, inferior frontal gyrus, and anterior lateral parietal cortex, functions in self-referential thinking and decision making. The pDMN, consisting of the posterior cingulate cortex (PCC), precuneus, posterior inferior parietal lobule, angular, and temporal lobe, is more relevant to familiarity and autobiographical memory processing (Damoiseaux et al., 2012, Lei et al., 2014, Lei et al., 2013). Specifically, the precuneus in the pDMN is considered to be the functional core of DMN (Utevsky et al., 2014), which has been identified as a key brain region contributing to psychological representation of retrieved visual details, and has been found to be associated with subjective vividness ratings (Richter et al., 2016, St-Laurent et al., 2015). For example, a recent study administrated autobiographical interviews with patients with atrophy of posterior cortical (including precuneus), patients with Alzheimer's disease (AD), and healthy controls. The results showed that patients with atrophy of posterior cortical exhibited a striking loss of internal episodic details relative to controls and as disrupted as patients with AD, indicating the function role of precuneus on imagery and autobiographical memory (Ahmed et al., 2018). Moreover, the DMN activity is also moderated by temporal distance in autobiographical memory processing. For example, the study of Botzung et al. (2008) required participants to recall from four temporal periods of life (0–9 years, 10–19 years, 20–29 years, and 30 years to the date of the test). The results showed that recent AMs (30 years to the date of the test) elicited more activation of the left precuneus, bilateral posterior cingulate gyrus, and left superior frontal gyrus than remote AMs (0–9 years). However, as far as we know, there is no research has explored whether this temporal effect of autobiographical memory could be moderated by age.

Here, we used an fMRI-adapted autobiographical memory task to first explore the age-by-temporal distance effect on the vividness ratings of autobiographical memory. Second, we conducted an age-by-temporal distance full-factorial analysis to examine the activation of DMN. Then, we used region-of-interest (ROI) analysis to further explore the interrelationship between precuneus activation and vividness ratings. Third, on top of the activation, we compared functional connectivity within the DMN in autobiographical memory processing between young and older adults.

Section snippets

Participants

Twenty-five young adults and 27 older adults were recruited for the current study. Due to excessive head movements (i.e., translation > 3 mm or rotation > 3°), data recording errors, and missing structural images, fifteen participants were excluded from the following analyses. The data exclusion procedure is shown in Fig. 1A. As a result, we included 38 healthy right-handed participants, with 19 young adults (8 male, aged 19 ~ 26 years, 20.6 ± 2.6 years) and 19 older adults (6 male, aged

The vividness ratings

The 2 age (young versus old) × 2 temporal distance (recent versus remote) repeated-measure ANOVA revealed a significant main effect of age (F(1,36) = 11.03, p < 0.01, ηp2 = 0.23) with higher vividness ratings in older adults, a main effect of temporal distance (F(1,36) = 7.33, p < 0.01, ηp2 = 0.17) with higher vividness rating for recent AMs, and an interaction of age × temporal distance (F (1,36) = 5.47, p < 0.05, ηp2 = 0.13). The simple effect analysis showed that young adults rated the

Discussion

The age-by-temporal distance effect was found for both subjective vividness ratings and neural activities of DMN in autobiographical memory processing. Specifically, young adults rated the vividness of recent AMs higher than that of remote AMs, whereas there was no temporal distance effect in older adults. Of note, the vividness ratings of older adults were generally higher than that of young adults regardless of temporal distances. For neural imaging, the full-factorial analysis revealed an

Conclusion

To conclude, the present study is the first to explore age-related alterations of DMN neural activities in autobiographical memory processing with different temporal distances. The vividness ratings of older adults were generally higher than that of young adults and were less sensitive to temporal distances. Neurally, aging not only impacted the DMN activation but also its functional connectivity. The results suggest that older adults exhibit age-related neural differences in both activation

Funding

This work was supported by the National Natural Science Foundation of China (31971007, 31971028), the Ministry of Education of Humanities and Social Science project (17YJA190015), nd the CAS Key Laboratory of Mental Health, Institute of Psychology (KLMH2019K02).

CRediT authorship contribution statement

Hong-Zhou Xu: Conceptualization, Methodology, Formal analysis, Software, Writing - original draft, Visualization, Writing - review & editing. Xiao-Xiao Xu: Conceptualization, Investigation, Data curation. Xu Lei: Funding acquisition, Writing - review & editing. Jing Yu: Conceptualization, Supervision, Visualization, Project administration, Writing - review & editing, Funding acquisition.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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