Age-related alterations of default mode network in autobiographical memory: Recent versus remote events
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.
References (58)
- et al.
Constructive episodic simulation of the future and the past: Distinct subsystems of a core brain network mediate imagining and remembering
Neuropsychologia
(2009) - et al.
Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration
Neuropsychologia
(2007) - et al.
Association between precuneus volume and autobiographical memory impairment in posterior cortical atrophy: Beyond the visual syndrome
Neuroimage Clin
(2018) A fast diffeomorphic image registration algorithm
NeuroImage
(2007)- et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends in Cognitive Sciences
(2000) - et al.
The space for memory in posterior parietal cortex: Re-analyses of bottom-up attention data
Neuropsychologia
(2020) - et al.
A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI
NeuroImage
(2014) - et al.
Neural correlates of envisioning emotional events in the near and far future
NeuroImage
(2008) - et al.
Functional connectivity change across multiple cortical networks relates to episodic memory changes in aging
Neurobiology of Aging
(2015) - et al.
“Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician
Journal of Psychiatric Research
(1975)
Age-related differences in the neural correlates of vivid remembering
NeuroImage
Validating the independent components of neuroimaging time series via clustering and visualization
NeuroImage
Extraversion is encoded by scale-free dynamics of default mode network
NeuroImage
Association between prefrontal activity and volume change in prefrontal and medial temporal lobes in aging and dementia: A review
Ageing Research Reviews
The mind's eye—precuneus activation in memory-related imagery
NeuroImage
Measuring functional connectivity during distinct stages of a cognitive task
NeuroImage
The functional neuroanatomy of autobiographical memory: A meta-analysis
Neuropsychologia
Brain structural, functional, and cognitive correlates of recent versus remote autobiographical memories in amnestic Mild Cognitive Impairment
NeuroImage: Clinical
Nonmonotonic recruitment of ventromedial prefrontal cortex during remote memory recall
PLoS Biology
Detecting representations of recent and remote autobiographical memories in vmPFC and hippocampus
Journal of Neuroscience
The neural bases of the constructive nature of autobiographical memories studied with a self-paced fMRI design
Memory
The brain's default network: Anatomy, function, and relevance to disease
Annals of the New York Academy of Sciences
A method for making group inferences from functional MRI data using independent component analysis
Human Brain Mapping
Life span changes in autobiographical memory
Phenomenal characteristics of autobiographical memories for emotional and neutral events in older and younger adults
Experimental Aging Research
Differentiating location- and distance-based processes in memory for time: An ERP study
Psychonomic Bulletin & Review
Functional connectivity tracks clinical deterioration in Alzheimer's disease
Neurobiology of Aging
Age-dependent differences in the neural mechanisms supporting long-term declarative memories
Archives of Clinical Neuropsychology
Comparison of multi-subject ICA methods for analysis of fMRI data
Human Brain Mapping
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2021, CortexCitation Excerpt :Notably, the angular gyrus and the posterior cingulate cortex are key nodes of the default mode network (Raichle, 2015), which has been linked already to self-referential processing and autobiographical memory (for a review, see Molnar-Szakacs & Uddin, 2013). Interestingly, age-related alterations of the default mode network have been recently reported for normal elderly adults during autobiographical memory retrieval (Xu et al., 2021). The increased activity of these regions during memory access in GC appears then to suggest that the default mode network might contribute to promote the retrieval of autobiographical information in an elderly individual with HSAM.