Episodic memory across the lifespan: The contributions of associative and strategic components

The structural and functional brain circuitries supporting episodic memory undergo profound reorganization in childhood and old age. We propose a two-component framework that combines and integrates evidence from child development and aging. It posits that episodic memory builds on two interacting components: (a) the strategic component, which refers to memory control operations, and (b) the associative component, which refers to mechanisms that bind different features of a memory episode into a compound representation. We hypothesize that: (a) children's difficulties in episodic memory primarily originate from low levels of strategic operations, and reflect the protracted development of the prefrontal cortex (PFC); (b) deficits in episodic memory performance among older adults originate from impairments in both strategic and associative components, reflecting senescent changes in the PFC and the medio-temporal lobes (MTL). Initial behavioral and neural evidence is consistent with both hypotheses. The two-component framework highlights the specificities of episodic memory in different age periods, helps to identify and dissociate its components, and contributes to understanding the interplay among maturation, learning, and senescence

Dopamine and memory dedifferentiation in aging.

The dedifferentiation theory of aging proposes that a reduction in the specificity of neural representations causes declines in complex cognition as people get older, and may reflect a reduction in dopaminergic signaling. The present pharmacological fMRI study investigated episodic memory-related dedifferentiation in young and older adults, and its relation to dopaminergic function, using a randomized placebo-controlled double-blind crossover design with the agonist Bromocriptine (1.25mg) and the antagonist Sulpiride (400mg). We used multi-voxel pattern analysis to measure memory specificity: the degree to which distributed patterns of activity distinguishing two different task contexts during an encoding phase are reinstated during memory retrieval. As predicted, memory specificity was reduced in older adults in prefrontal cortex and in hippocampus, consistent with an impact of neural dedifferentiation on episodic memory representations. There was also a linear age-dependent dopaminergic modulation of memory specificity in hippocampus reflecting a relative boost to memory specificity on Bromocriptine in older adults whose memory was poorer at baseline, and a relative boost on Sulpiride in older better performers, compared to the young. This differed from generalized effects of both agents on task specificity in the encoding phase. The results demonstrate a link between aging, dopaminergic function and dedifferentiation in the hippocampus.This research was funded mainly by a Fellowship to AMM from Research into Ageing, UK, and by an RCUK Academic Fellowship at the University of Edinburgh. Some of the research was conducted by Hunar Abdulrahman as part of a dissertation for the MSc in Neurosciences at the University of Edinburgh. The research was also supported by a Human Brain Project grant from the National Institute of Mental Health and the National Institute of Biomedical Imaging & Bioengineering. PCF was supported by a Wellcome Trust Senior Fellowship in Clinical Science, and by the Bernard Wolfe Health Neuroscience Fund. ETB is a part-time (50%) employee and shareholder of GSK. AMM is a member of the University of Edinburgh Centre for Cognitive Ageing and Cognitive Epidemiology, part of the cross-council Lifelong Health and Wellbeing Initiative, Grant number G0700704/84698.This is the accepted manuscript. The final version is available at http://dx.doi.org/10.1016/j.neuroimage.2015.03.03

Free recall test experience potentiates strategy-driven effects of value on memory.

People tend to show better memory for information that is deemed valuable or important. By one mechanism, individuals selectively engage deeper, semantic encoding strategies for high value items (Cohen, Rissman, Suthana, Castel, & Knowlton, 2014). By another mechanism, information paired with value or reward is automatically strengthened in memory via dopaminergic projections from midbrain to hippocampus (Shohamy & Adcock, 2010). We hypothesized that the latter mechanism would primarily enhance recollection-based memory, while the former mechanism would strengthen both recollection and familiarity. We also hypothesized that providing interspersed tests during study is a key to encouraging selective engagement of strategies. To test these hypotheses, we presented participants with sets of words, and each word was associated with a high or low point value. In some experiments, free recall tests were given after each list. In all experiments, a recognition test was administered 5 minutes after the final word list. Process dissociation was accomplished via remember/know judgments at recognition, a recall test probing both item memory and memory for a contextual detail (word plurality), and a task dissociation combining a recognition test for plurality (intended to probe recollection) with a speeded item recognition test (to probe familiarity). When recall tests were administered after study lists, high value strengthened both recollection and familiarity. When memory was not tested after each study list, but rather only at the end, value increased recollection but not familiarity. These dual process dissociations suggest that interspersed recall tests guide learners' use of metacognitive control to selectively apply effective encoding strategies. (PsycINFO Database Recor

Ageing and episodic retrieval: using event-related potentials to compare the neural correlates of item and associative recognition in young and older adults.

Older people commonly report problems with remembering, and behavioural studies have confirmed that memory does decline with age. Age-related deficits are particularly evident in episodic memory; however, the degree of impairment appears to be task-dependent. Compared to young adults, older adults generally perform reasonably well on simple item recognition tasks, but are markedly compromised on more complex tasks, such a s those that require memory for context. Dual process theory suggests that this pattern of ageing deficits results from an age-related decline in recollection, whilst familiarly remains relatively intact. This thesis reports a series of event-related potential (ERP) studies conducted to examine the effect of ageing on the neural correlates of simple item recognition and more complex associative recognition. Behaviourally, as anticipated, the young outperformed the elderly, particularly in associative recognition. Electrophysiologically, the age-related reduction of the left parietal effect in item recognition appeared to support the dual process view that recollection becomes compromised as people grow older. Likewise, an early right frontal component, evident in both item and associative recognition, may reflect the preservation of familiarity in elderly adults. However, the ERP data also suggest that dual process theory may represent an oversimplification of episodic memory age decline. While the presence of a left parietal sam e/rearranged difference in young adults was interpreted as evidence of the adoption of a target-specific recollection strategy in associative recognition, the modulation's absence in older adults suggests that they are unable to similarly inhibit the retrieval of goal-irrelevant information. Moreover, the older participants also demonstrated widespread left-sided negative activations that may represent two components: First, the fronto-central negativities elicited by both tasks may index the compensatory operations recruited by older adults to maximise their performance. Second, a central/posterior negativity in item recognition, which strongly resembled a modulation that had been previously observed in source memory ageing studies, was interpreted as reflecting the task-irrelevant retrieval of contextual information

Remembering out-of-context: a developmental perspective.

Contextual influences on memory retrieval are of theoretical and e~pirical importance in infant memory research. Early in infancy, memory is strongly constrained by contextual congruency at encoding and retrieval. Contextual constraints appear to progressively loosen over the infancy period (Hayne, 2004), but little is known about the nature and extent of this change. The present studies revealed that age-related decreases in contextual constraints on memory retrieval extend to both physical and social context, and to recall and recognition memory (Experiments 1-4). Specifically, for 9-month-olds both recognition and recall memory were less affected by a change of social context than for 6-month- . olds, and for 12-month-olds, recognition memory was less influenced by a change of global physical context than for 6-month-olds. At 12-months, memory retrieval appeared to be particularly constrained by intrinsic contextual details, a constraint that was robust across procedural variations that alleviate context-shift effects in other age-groups (Experiment 5). Nonetheless, providing infants with a unique environment for learning and retrieval helped them to retrieve memory across an intrinsic contextual change, indicating that extrinsic context may perform a disambiguating function later in infancy (Experiment 6). Finally, Experiments 7 to 9 used an EEG study to explore the processes underlying contextual influences on memory retrieval with adults. A change ofioom selectively impaired the purported neural correlates ofrecollective-based recognition memory, indicating that investigating the development ofrecollection in infancy may be an important step towards understanding contextual influences on memory in development. Taken together, these studies show that sirililar contextual features are encoded in memory from infancy to adulthood. Contextual details exert progressively less influence over memory retrieval over the first year of life, likely through a combination ofboth the maturation ofbrain regions involved in memory, and experience oflearning and remembering in a variety of settings

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

Age-related episodic memory decline is characterized by striking heterogeneity across individuals. Hippocampal pattern completion is a fundamental process supporting episodic memory. Yet, the degree to which this mechanism is impaired with age, and contributes to variability in episodic memory, remains unclear. We combine univariate and multivariate analyses of fMRI data from a large cohort of cognitively normal older adults (N=100) to measure hippocampal activity and cortical reinstatement during retrieval of trial-unique associations. Trial-wise analyses revealed that (a) hippocampal activity scaled with reinstatement strength, (b) cortical reinstatement partially mediated the relationship between hippocampal activity and associative retrieval, (c) older age weakened cortical reinstatement and its relationship to memory behaviour. Moreover, individual differences in the strength of hippocampal activity and cortical reinstatement explained unique variance in performance across multiple assays of episodic memory. These results indicate that fMRI indices of hippocampal pattern completion explain within-and across-individual memory variability in older adults