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Precise slow oscillation-spindle coupling promotes memory consolidation in younger and older adults
(2018)
Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO) and sleep spindles (SP) and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that the fine-tuned SO–SP coupling that is present in younger adults diffuses with advanced age and shifts both in time and frequency. Crucially, we show that the tight precision of SO–SP coupling promotes memory consolidation in younger and older adults, and that brain integrity in source regions for the generation of SOs and SPs reinforces this beneficial SO–SP coupling in old age. Our results reveal age-related differences in SO–SP coupling in healthy elderly individuals. Furthermore, they broaden our understanding of the conditions and the functional significance of SO–SP coupling across the entire adult lifespan.
From early to middle childhood, brain regions that underlie memory consolidation undergo profound maturational changes. However, there is little empirical investigation that directly relates age-related differences in brain structural measures to the memory consolidation processes. The present study examined system-level memory consolidations of intentionally studied object-location associations after one night of sleep (short delay) and after two weeks (long delay) in normally developing 5-to-7-year-old children (n = 50) and young adults (n = 39). Behavioural differences in memory consolidation were related to structural brain measures. Our results showed that children, in comparison to young adults, consolidate correctly learnt object-location associations less robustly over short and long delay. Moreover, using partial least squares correlation method, a unique multivariate profile comprised of specific neocortical (prefrontal, parietal, and occipital), cerebellar, and hippocampal subfield structures was found to be associated with variation in short-delay memory consolidation. A different multivariate profile comprised of a reduced set of brain structures, mainly consisting of neocortical (prefrontal, parietal, and occipital), and selective hippocampal subfield structures (CA1-2 and subiculum) was associated with variation in long-delay memory consolidation. Taken together, the results suggest that multivariate structural pattern of unique sets of brain regions are related to variations in short- and long-delay memory consolidation across children and young adults.
RESEARCH HIGHLIGHTS
* Short- and long-delay memory consolidation is less robust in children than in young adults
* Short-delay brain profile comprised of hippocampal, cerebellar, and neocortical brain regions
* Long-delay brain profile comprised of neocortical and selected hippocampal brain regions.
* Brain profiles differ between children and young adults.
Memory consolidation tends to be less robust in childhood than adulthood. However, little is known about the corresponding functional differences in the developing brain that may underlie age-related differences in retention of memories over time. This study examined system-level memory consolidation of object-scene associations after learning (immediate delay), one night of sleep (short delay), as well as two weeks (long delay) in 5-to-7-year-old children (n = 49) and in young adults (n = 39), as a reference group with mature consolidation systems. Particularly, we characterized how functional neural activation and reinstatement of neural patterns change over time, assessed by functional magnetic resonance imaging combined with representational similarity analysis (RSA). Our results showed that memory consolidation in children was less robust and strong (i.e., more forgetting) compared to young adults. Contrasting correctly retained remote versus recent memories across time delay, children showed less upregulation in posterior parahippocampal gyrus, lateral occipital cortex, and cerebellum than adults. In addition, both children and adults showed decrease in scene-specific neural reinstatement over time, indicating time-related decay of detailed differentiated memories. At the same time, we observed more generic gist-like neural reinstatement in medial-temporal and prefrontal brain regions uniquely in children, indicating qualitative difference in memory trace in children. Taken together, 5-to-7-year-old children, compared to young adults, show less robust memory consolidation, possibly due to difficulties in engaging in differentiated neural reinstatement in neocortical mnemonic regions during retrieval of remote memories, coupled with relying more on gist-like generic neural reinstatement.
Age-related memory decline is associated with changes in neural functioning but little is known about how aging affects the quality of information representation in the brain. Whereas a long-standing hypothesis of the aging literature links cognitive impairments to less distinct neural representations in old age, memory studies have shown that high similarity between activity patterns benefits memory performance for the respective stimuli. Here, we addressed this apparent conflict by investigating between-item representational similarity in 50 younger (19–27 years old) and 63 older (63–75 years old) human adults (male and female) who studied scene-word associations using a mnemonic imagery strategy while electroencephalography was recorded. We compared the similarity of spatiotemporal frequency patterns elicited during encoding of items with different subsequent memory fate. Compared to younger adults, older adults’ memory representations were more similar to each other but items that elicited the most similar activity patterns early in the encoding trial were those that were best remembered by older adults. In contrast, young adults’ memory performance benefited from decreased similarity between earlier and later periods in the encoding trials, which might reflect their better success in forming unique memorable mental images of the joint picture–word pair. Our results advance the understanding of the representational properties that give rise to memory quality as well as how these properties change in the course of aging.
From early to middle childhood, brain regions that underlie memory consolidation undergo profound maturational changes. However, there is little empirical investigation that directly relates age-related differences in brain structural measures to the memory consolidation processes. The present study examined system-level memory consolidations of intentionally studied object-location associations after one night of sleep (short delay) and after two weeks (long delay) in normally developing 5-to-7-year-old children (n = 50) and young adults (n = 39). Behavioural differences in memory consolidation were related to structural brain measures. Our results showed that children, in comparison to young adults, consolidate correctly learnt object-location associations less robustly over short and long delay. Moreover, using partial least squares correlation method, a unique multivariate profile comprised of specific neocortical (prefrontal, parietal, and occipital), cerebellar, and hippocampal subfield structures was found to be associated with variation in short-delay memory consolidation. A different multivariate profile comprised of a reduced set of brain structures, mainly consisting of neocortical (prefrontal, parietal, and occipital), and selective hippocampal subfield structures (CA1-2 and subiculum) was associated with variation in long-delay memory consolidation. Taken together, the results suggest that multivariate structural pattern of unique sets of brain regions are related to variations in short- and long-delay memory consolidation across children and young adults.
RESEARCH HIGHLIGHTS
Short- and long-delay memory consolidation is less robust in children than in young adults
* Short-delay brain profile comprised of hippocampal, cerebellar, and neocortical brain regions
* Long-delay brain profile comprised of neocortical and selected hippocampal brain regions.
* Brain profiles differ between children and young adults.
Mnemonic but not contextual feedback signals defy dedifferentiation in the aging early visual cortex
(2024)
Perception is an intricate interplay between feedforward visual input and internally generated feedback signals that comprise concurrent contextual and time-distant mnemonic (episodic and semantic) information. Yet, an unresolved question is how the composition of feedback signals changes across the lifespan and to what extent feedback signals undergo age-related dedifferentiation, that is, a decline in neural specificity. Previous research on this topic has focused on feedforward perceptual representation and episodic memory reinstatement, suggesting reduced fidelity of neural representations at the item and category levels. In this fMRI study, we combined an occlusion paradigm that filters feedforward input to the visual cortex and multivariate analysis techniques to investigate the information content in cortical feedback, focusing on age-related differences in its composition. We further asked to what extent differentiation in feedback signals (in the occluded region) is correlated to differentiation in feedforward signals. Comparing younger (18–30 years) and older female and male adults (65–75 years), we found that contextual but not mnemonic feedback was prone to age-related dedifferentiation. Semantic feedback signals were even better differentiated in older adults, highlighting the growing importance of generalized knowledge across ages. We also found that differentiation in feedforward signals was correlated with differentiation in episodic but not semantic feedback signals. Our results provide evidence for age-related adjustments in the composition of feedback signals and underscore the importance of examining dedifferentiation in aging for both feedforward and feedback processing.
Childhood is a period when memory consolidation and knowledge base undergo rapid changes. The present study examined short-delay (overnight) and long-delay (after a 2-week period) consolidation of new information either congruent or incongruent with prior knowledge in typically developing 6- to 8-year-old children (n = 32), 9- to 11-year-old children (n = 33), and 18- to 30-year-old young adults (YA; n = 39). Both memory accessibility (cued recall of objects) and precision (precision of object placement) of initially well-learned object–scene pairs were measured. Our results showed that overnight, memory accessibility declined similarly in all age groups; memory precision improved more in younger children (YC) compared to older children (OC) and even declined in YA. After a 2-week period, both memory accessibility and precision became worse. Specifically, while age groups showed similar decline in memory accessibility, precision decline was less in YC than in OC and YA. The accessibility and precision of congruent and incongruent information changed similarly with consolidation in all age groups. Taken together, our results showed that, for initially well-learned information, YC have robust memory consolidation, despite their overall lower mnemonic performance compared to OC and YA, which is potentially crucial for stable and precise knowledge accumulation early on in development.
Generating predictions about environmental regularities, relying on these predictions, and updating these predictions when there is a violation from incoming sensory evidence are considered crucial functions of our cognitive system for being adaptive in the future. The violation of a prediction can result in a prediction error (PE) which affects subsequent memory processing. In our preregistered studies, we examined the effects of different levels of PE on episodic memory. Participants were asked to generate predictions about the associations between sequentially presented cue-target pairs, which were violated later with individual items in three PE levels, namely low, medium, and high PE. Hereafter, participants were asked to provide old/new judgments on the items with confidence ratings, and to retrieve the paired cues. Our results indicated a better recognition memory for low PE than medium and high PE levels, suggesting a memory congruency effect. On the other hand, there was no evidence of memory benefit for high PE level. Together, these novel and coherent findings strongly suggest that high PE does not guarantee better memory.