Memory Consolidation in Typical and Atypical Development, 2016-2021

DOI

This project comprises a number of studies examining memory consolidation over sleep in different populations. Each have their own Open Science Framework record, complete with data, analysis scripts and methods, with the links to these records (and respective publications) all provided under Related Resources below. The abstract for each dataset is provided as follows: TITLE: Sleep-dependent memory consolidation in children with vocabulary weaknesses BACKGROUND: Vocabulary is crucial for an array of life outcomes and is frequently impaired in developmental disorders. Notably, 'poor comprehenders' (children with reading comprehension deficits but intact word reading) often have vocabulary deficits, but underlying mechanisms remain unclear. Prior research suggests intact encoding but difficulties consolidating new word knowledge. We test the hypothesis that poor comprehenders' sleep-associated vocabulary consolidation is compromised by their impoverished lexical-semantic knowledge. METHODS: Memory for new words was tracked across wake and sleep to assess encoding and consolidation in 8-to-12-year-old good and poor comprehenders. Each child participated in two sets of sessions, one beginning in the morning (AM-encoding) and the other in the evening (PM-encoding). In each case, they were taught 12 words and were trained on a spatial memory task. Memory was assessed immediately, 12- and 24-hr later via stem-completion, picture-naming, and definition tasks to probe different aspects of word knowledge. Long-term retention was assessed 1-2 months later. RESULTS: Recall of word-forms improved over sleep and postsleep wake, as measured in both stem-completion and picture-naming tasks. Counter to hypotheses, deficits for poor comprehenders were not observed in consolidation but instead were seen across measures and throughout testing, suggesting a deficit from encoding. Variability in vocabulary knowledge across the whole sample predicted sleep-associated consolidation, but only when words were learned early in the day and not when sleep followed soon after learning. CONCLUSIONS: Poor comprehenders showed weaker memory for new words than good comprehenders, but sleep-associated consolidation benefits were comparable between groups. Sleeping soon after learning had long-lasting benefits for memory and may be especially beneficial for children with weaker vocabulary. These results provide new insights into the breadth of poor comprehenders' vocabulary weaknesses, and ways in which learning might be better timed to remediate vocabulary difficulties. TITLE: Learning to live with interference neighbours ABSTRACT: New vocabulary is consolidated offline, particularly during sleep; however, the parameters that influence consolidation remain unclear. Two experiments investigated effects of exposure level and delay between learning and sleep on adults' consolidation of novel competitors (e.g. BANARA) to existing words (e.g. BANANA). Participants made speeded semantic decisions (i.e. a forced choice: natural versus man-made) to the existing words, with the expectation that novel word learning would inhibit responses due to lexical competition. This competition was observed, particularly when assessed after sleep, for both standard and high exposure levels (10 and 20 exposures per word; Experiment 1). Using a lower exposure level (five exposures; Experiment 2), no post-sleep enhancement of competition was observed, despite evidence of consolidation when explicit knowledge of novel word memory was tested. Thus, when encoding is relatively weak, consolidation-related lexical integration is particularly compromised. There was no evidence that going to bed soon after learning is advantageous for overnight consolidation; however, there was some preliminary suggestion that longer gaps between learning and bed-onset were associated with better explicit memory of novel words one week later, but only at higher levels of exposure. These findings suggest that while lexical integration can occur overnight, weaker lexical traces may not be able to access overnight integration processes in the sleeping brain. Furthermore, the finding that longer-term explicit memory of stronger (but not weaker) traces benefit from periods of wake following learning deserves examination in future research. TITLE: Growing up with interfering neighbours: the influence of time of learning and vocabulary knowledge on written word learning in children ABSTRACT: Evidence suggests that new vocabulary undergoes a period of strengthening and integration offline, particularly during sleep. Practical questions remain, however, including whether learning closer to bedtime can optimize consolidation, and whether such an effect varies with vocabulary ability. To examine this, children aged 8–12-years-old (n 59) were trained on written novel forms (e.g. BANARA) in either the morning (long delay) or the evening (short delay). Immediately after training and the next day, lexical competition (a marker of integration) was assessed via speeded semantic decisions to neighbouring existing words (e.g. BANANA); explicit memory was measured via recognition and recall tasks. There were no main effects indicating performance changes across sleep for any task, counter to studies of spoken word learning. However, a significant interaction was found, such that children with poorer vocabulary showed stronger lexical competition on the day after learning if there was a short delay between learning and sleep. Furthermore, while poorer vocabulary was associated with slower novel word recognition speed before and after sleep for the long delay group, this association was only present before sleep for the short delay group. Thus, weak vocabulary knowledge compromises novel word acquisition, and when there is a longer period of post-learning wake, this disadvantage remains after a consolidation opportunity. However, when sleep occurs soon after learning, consolidation processes can compensate for weaker encoding and permit lexical integration. These data provide preliminary suggestion that children with poorer vocabulary may benefit from learning new words closer to bedtime. TITLE: Offline consolidation supersedes prior knowledge benefits in childrens but not adults word learning ABSTRACT: Prior linguistic knowledge is proposed to support the acquisition and consolidation of new words. Adults typically have larger vocabularies to support word learning than children, but the developing brain shows enhanced neural processes that are associated with offline memory consolidation. This study investigated contributions of prior knowledge to initial word acquisition and consolidation at different points in development, by teaching children and adults novel words (e.g., ballow) that varied in the number of English word-form "neighbours" (e.g., wallow, bellow). Memory for the novel word-forms was tested immediately after training, the next day and 1 week later, to assess the time-course of prior knowledge contributions. Children aged 7-9 years (Experiments 1, 3) and adults (Experiment 2) recalled words with neighbours better than words without neighbours when tested immediately after training. However, a period of offline consolidation improved overall recall and reduced the influence of word-form neighbours on longer term memory. These offline consolidation benefits were larger in children than adults, supporting theories that children have a greater propensity for consolidating phonologically distinctive language information. Local knowledge of just a single word-form neighbour was enough to enhance learning, and this led to the individual differences in word recall that were related to adults' global vocabulary ability. The results support the proposal that the relative contributions of different learning mechanisms change across the lifespan, and highlight the importance of testing theoretical models of word learning in the context of development. TITLE: Atypicalities in sleep and semantic processing in autism ABSTRACT: Sleep is known to support the neocortical consolidation of declarative memory, including the acquisition of new language. Autism spectrum disorder (ASD) is often characterized by both sleep and language learning difficulties, but few studies have explored a potential connection between the two. Here, 54 children with and without ASD (matched on age, nonverbal ability and vocabulary) were taught nine rare animal names (e.g., pipa). Memory was assessed via definitions, naming and speeded semantic decision tasks immediately after learning (pre‐sleep), the next day (post‐sleep, with a night of polysomnography between pre‐ and post‐sleep tests) and roughly 1 month later (follow‐up). Both groups showed comparable performance at pre‐test and similar levels of overnight change on all tasks; but at follow‐up children with ASD showed significantly greater forgetting of the unique features of the new animals (e.g., pipa is a flat frog). Children with ASD had significantly lower central non‐rapid eye movement (NREM) sigma power. Associations between spindle properties and overnight changes in speeded semantic decisions differed by group. For the TD group, spindle duration predicted overnight changes in responses to novel animals but not familiar animals, reinforcing a role for sleep in the stabilization of new semantic knowledge. For the ASD group, sigma power and spindle duration were associated with improvements in responses to novel and particularly familiar animals, perhaps reflecting more general sleep‐associated improvements in task performance. Plausibly, microstructural sleep atypicalities in children with ASD and differences in how information is prioritized for consolidation may lead to cumulative consolidation difficulties, compromising the quality of newly formed semantic representations in long‐term memory. TITLE: Sleep promotes phonological learning in children across language and autism spectra PURPOSE: Establishing stable and flexible phonological representations is a key component of language development and one which is thought to vary across children with neurodevelopmental disorders affecting language acquisition. Sleep is understood to support the learning and generalization of new phonological mappings in adults, but this remains to be examined in children. This study therefore explored the time course of phonological learning in childhood and how it varies by structural language and autism symptomatology. METHOD: Seventy-seven 7- to 13-year-old children, 30 with high autism symptomatology, were included in the study; structural language ability varied across the sample. Children learned new phonological mappings based on synthesized speech tokens in the morning; performance was then charted via repetition (without feedback) over 24 hr and followed up 4 weeks later. On the night following learning, children's sleep was monitored with polysomnography. RESULTS: A period of sleep but not wake was associated with improvement on the phonological learning task in childhood. Sleep was associated with improved performance for both trained items and novel items. Structural language ability predicted overall task performance, though language ability did not predict degree of change from one session to the next. By contrast, autism symptomatology did not explain task performance. With respect to sleep architecture, rapid eye movement features were associated with greater phonological generalization. CONCLUSIONS: Children's sleep was associated with improvement in performance on both trained and novel items. Phonological generalization was associated with brain activity during rapid eye movement sleep. This study furthers our understanding of individual differences in the acquisition of new phonological mappings and the role of sleep in this process over childhood.Sleep is known to affect the consolidation process that takes fragile memories and makes them robust. Components of sleep such as slow oscillations influence this consolidation process. However, little is known about how children's sleep may influence consolidation. This is important: children's sleep has more of the components that are crucial for consolidation of memory, and may show more substantial effects. Given that children encounter new information at a dramatic rate, it is important to understand what factors influence consolidation to ensure that learning is optimal. Furthermore, sleep difficulties are common in childhood, particularly in neurodevelopmental disorders characterised by language learning impairments (e.g., autism spectrum disorder; ASD), but little progress has been made in examining whether learning and sleep difficulties are related in these groups. Comparisons across ages, as well as between typical and atypical groups of the same age, offer an opportunity to test theories of consolidation in terms of whether they can explain the substantial variability across and within development. Our plans provide a comprehensive evaluation of the influence of sleep on consolidation of memory in development. Strand 1 focuses on typical development, using children aged 10-12 (when slow-oscillation activity peaks), as well as adults, and in some cases younger children. Strand 2 focuses on atypical development, comprising the first systematic evaluation of whether atypical sleep relates to language learning difficulties in children with ASD with varying language phenotypes and in children with language impairment (LI) without ASD. This enables us to separate learning mechanisms associated with ASD from those attributable to language impairment. Our experiments involve learning of new materials, followed by a delay. For sleep conditions, participants' brain activity is recorded at home. Later tests determine the strength and nature of the new memory. For example, one study addresses whether sleep facilitates stabilisation of new memories, and looks at the optimal delay between learning and sleep (which may be particularly pertinent for children). Another examines the influence of prior knowledge on consolidation during sleep. Adults and children differ in terms of the prior knowledge that they bring to a learning situation and it is possible that this can mask the stronger consolidation ability of children. Furthermore, children with language impairments have impoverished vocabularies which may lead to a 'Matthew Effect' (i.e., the rich get richer and the poor get poorer) in the consolidation of new words; our studies will test this hypothesis directly. Many studies focus on the role of sleep in language learning. We track the timecourse of learning spoken words and their meanings, and the extent to which this new information is strengthened over time, integrated with existing knowledge, and generalised to new exemplars. Such studies permit a thorough examination of whether language learning difficulties are associated with differences in sleep architecture in ASD and LI. We will exploit data collected from the same children over a 2-year period to examine whether sleep variables predict vocabulary outcomes over a longer period. Finally, in a cross-cutting study we examine the generality of any effects of sleep across both typical and atypical development by examining the influence of sleep in a rather different type of memory that is nonetheless dependent on consolidation: spatial location. We aim to create a comprehensive theory of typical and atypical consolidation and forgetting across wake and sleep, and advance theories of typical language acquisition and language heterogeneity in ASD and LI. The theoretical applications of the planned research have the potential to improve our practical understanding of how to make memories stick in children and adults, and ultimately improve outcomes.

Information about the sample and methods used in data collection are all provided in full in the attached published papers.

Identifier
DOI https://doi.org/10.5255/UKDA-SN-854772
Metadata Access https://datacatalogue.cessda.eu/oai-pmh/v0/oai?verb=GetRecord&metadataPrefix=oai_ddi25&identifier=9a82ceb8ae8b0117b5101342ee43954bb80a7390a51d4150515d5a026ab2f011
Provenance
Creator Henderson, L, University of York
Publisher UK Data Service
Publication Year 2021
Funding Reference Economic and Social Research Council
Rights Lisa Henderson, University of York; The Data Collection is available from an external repository. Access is available via Related Resources.
OpenAccess true
Representation
Language English
Resource Type Numeric; Text; Audio; Other
Discipline Psychology; Social and Behavioural Sciences
Spatial Coverage United Kingdom