Healthy ageing reduces the precision of episodic memory retrieval

Abstract

Episodic memory declines with older age, but it is unresolved whether this decline reflects reduced probability of successfully retrieving information from memory, or decreased precision of the retrieved information. Here, we used continuous measures of episodic memory retrieval in combination with computational modelling of participants' retrieval errors to distinguish between these two potential accounts of age-related memory deficits. In three experiments, young and older participants encoded stimuli displays consisting of everyday objects varying along different perceptual features (e.g., location, colour and orientation) in a circular space. At test, participants recreated the features of studied objects using a continuous response dial. Across all three experiments, we observed age-related declines in the precision of episodic memory retrieval, whereas age differences in retrieval success were limited to the most challenging task condition. Reductions in mnemonic precision were evident for retrieval of both item-based and contextual information, and persisted after controlling for age-related decreases in the fidelity of perception and working memory. The findings highlight impoverished precision of memory representations as one factor contributing to age-related episodic memory loss, and suggest that the cognitive and neural changes associated with older age can differentially affect distinct aspects of episodic retrieval.

Hippocampal and cortical mechanisms at retrieval explain variability in episodic remembering in older adults

“…Although we observed robust group-level cortical reinstatement effects during associative hits, reinstatement strength declined with age, and partially mediated the relationship between age and episodic memory. These data provide neuroimaging evidence in support of proposals that age-related episodic memory decline is driven, in part, by a loss of specificity or precision in mnemonic representations, a possibility that has been well-supported by behavioural evidence (56–58). Importantly, the effect of age on reinstatement strength, and the relationship between reinstatement strength and memory performance, was observed after accounting for variance in encoding classifier performance, a putative assay of cortical differentiation (i.e., the ability to establish distinct neural patterns associated with different visual stimulus categories) during memory encoding.…”

Memory precision of object-location binding is unimpaired inAPOEε4-carriers with spatial navigation deficits

“…Older adults, individuals with mild cognitive impairment (MCI) and preclinical individuals with positive AD biomarkers exhibit significant deficits in mnemonic discrimination of novel and studied targets under conditions of high feature overlap (Trelle et al ., n.d.; Yassa et al ., 2010, 2011; Ally et al ., 2013; Stark et al ., 2013; Reagh et al ., 2014; Stark and Stark, 2017; Berron et al ., 2018, 2019; Leal and Yassa, 2018; Gellersen et al ., 2020; Webb et al ., 2020). Similarly, cognitively healthy preclinical adults (defined by APOE genotype or AD pathologies), as well as MCI and AD patients, also perform significantly worse in tests of feature binding, showing a marked decline in representational fidelity (Atienza et al ., 2011; Rentz et al ., 2011; Troyer et al ., 2012; Della Sala et al ., 2012; Hampel, 2013; Bastin et al ., 2014; Oedekoven et al ., 2015; Parra et al ., 2015, 2019; Van Geldorp et al ., 2015; Koppara et al ., 2015; Mowrey et al ., 2016; Pietto et al ., 2016; Chen and Chang, 2016; Liang et al ., 2016; Polcher et al ., 2017; Zokaei et al ., 2019; Delhaye et al ., 2019; Konijnenberg et al ., 2019; Pavisic et al ., 2020; Valdés et al ., 2020; Korkki et al ., 2020).…”

“…A longer study-test delay may be able to index such faster forgetting. We hypothesised that our task design may detect ε4-dependent differences because 1) the task involves entorhinal and hippocampal mediated relational binding of objects and locations, which is impaired in prodromal AD (Charles et al ., 2004; Reagh et al ., 2014; Hampstead et al ., 2018; McIlvain et al ., 2018; Weigard et al ., 2020), 2) a continuous metric may be a more sensitive index than categorical measures of retrieval (Zokaei et al ., 2015; Korkki et al ., 2020), and 3) memory fidelity relies on communication between hippocampus and cortical regions, which exhibit altered connectivity in the early course of AD (Buckner et al ., 2005; Sperling et al ., 2011; Jack et al ., 2015; Richter et al ., 2016; Xie, 2018; Stevenson et al ., 2018; Cooper and Ritchey, 2019; Harrison et al ., 2019; Sullivan et al ., 2019; Berron et al ., 2020; Foo et al ., 2020).…”

Hippocampal-cortical encoding activity predicts the precision of episodic memory

“…To distinguish the likelihood of successful memory retrieval from the precision of the retrieved information, we fitted a two-component mixture model (Bays et al, 2009; Zhang & Luck, 2008) to each participant’s retrieval error data using maximum likelihood estimation (code available at: https://www.paulbays.com/code/JV10/index.php). This mixture model has previously been shown to characterize long-term memory performance in similar tasks (e.g., Brady et al, 2013; Korkki et al, 2020; Richter et al, 2016), and has been employed to gain insights about the neural basis of the precision of episodic recollection (Cooper & Ritchey, 2019; Richter et al, 2016; Stevenson et al, 2018). The model assumes that two distinct sources of error contribute to participants’ retrieval performance across trials: variability, that is, noise, in successful retrieval of target features, and the presence of random guess responses where memory retrieval has failed to bring any diagnostic information about the target to mind.…”