Memory consolidation in typical and atypical development

Lead Research Organisation: University of York
Department Name: Psychology

Abstract

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.

Planned Impact

This research is fundamental science and its primary impact is scientific. However, we envisage societal impact in several areas, with the time-scale medium to long-term.

Educational sector - The research will enhance understanding of the conditions that lead to initially fragile memories becoming more robust over time. This should have practical benefits for all ages in terms of defining optimal learning sessions (e.g., for 1st and 2nd language learning or university education). Given the focus on children there should be particular interest in the educational ramifications. Previous research on pedagogical methods for enhancing learning in school has focused on the factors that benefit encoding rather than retention. We address questions such as: "How do we learn and retain new information?", "How does sleep influence the ability to retain information?","What is the role of sleep in language learning?", "Is there an optimal time span between encoding and sleep for consolidation?", and "How does knowledge advantage sleep-dependent consolidation?". Addressing such questions may facilitate better educational practice (e.g., how best to structure the day for the most effective retention), realistic expectations about the effects of learning, and when best to assess retention.

Clinical sector - The research will directly contribute to understanding of the link between sleep and language development in ASD and LI. Current estimates of the annual cost of supporting adults with ASD in the UK exceed £34 billion. Language outcomes are one of strongest predictors of academic, social and emotional outcomes. If we can better understand the contributing factors associated with language problems then we can better support individuals with such problems (e.g., by informing teachers, carers, therapists), and potentially pursue new treatments or intervention in the longer term. The findings would be of relevance to charities associated with ASD (e.g., NAS, Autistica) and LI (e.g., Afasic, RALLI, of which Norbury is a founding member), who may wish to raise awareness and support. More broadly, the findings may be relevant to the understanding of the implications of a range of disorders involving sleep problems (e.g., dyslexia, ADHD, Landau-Kleffner syndrome, sleep apnoea, insomnia).

Wider public - Our research has lesser implications for the general public by highlighting the value of sleep for cognition and learning. This has potential benefits in terms of discouraging damaging practices amongst children such as minimising sleep, use of media devices before bed, or "cramming" before exams and is of particular relevance to shift workers.

Staff on the project - The postdoctoral researcher and research assistants will gain valuable experience in the full range of academic tasks required for a career in academic research. Bursary students and casual student workers will also gain experience in research and the lab environment, which is becoming almost a prerequisite for PhD funding. The opportunities and experiences gained by the staff will also be applicable to an array of non-academic employment sectors (e.g., public liaison, communication and social awareness; problem solving; creativity and innovation; application of IT and numeracy).

The following activities will work to maximise impact: Articles and presentations to target practitioner audiences (e.g., Children's Sleep Charity, National Autistic Society, RALLI; Association for Science Education) and public audiences (e.g., British Science Festival); workshops and research symposia; communication with established contacts in educational and clinical settings (e.g., educational/clinical psychologists, child psychiatrists, special educational needs coordinators, teachers and head teachers) and advice from colleagues at the Institute for Effective Education in York; press releases, publications on our website, via Twitter and through our annual research lab newsletters.

Publications

10 25 50
 
Description The findings of this award can be split into three broad themes: (i) developmental differences in the role that sleep plays in the consolidation of new language, (ii) the impact of individual differences in sleep on language learning, (iii) the impact of poor sleep on mental health.
(i) Developmental differences.
This award was based a foundation of research showing that sleep plays an active role in strengthening and refining adults' memory for newly learned language. We extended these findings by revealing that these mechanisms change over development. Specifically, we observed that children can show larger benefits of nocturnal sleep on memory for new language than compared to adults (as reflected by larger increases in memory for newly learned words over sleep), likely as a consequence of increased time spent in NREM sleep. We also found that children and adults were more likely to maintain memories of new words over a daytime nap (but forget them after an equivalent period of wake), but again that this protective benefit was larger for children than adults. This suggests that there are developmental differences in the active and passive benefits of sleep. Advancing our neurological understanding of the word learning process, this same nap study also utilised diffusion weighted imaging to identify white matter tracts in the brain that are associated with the consolidation of new words. Indeed, for children, white matter integrity in the superior longitudinal fasciculus and uncinate fasciculus predicts their ability to initially learn and also consolidate new words over the nap.
We went on to show that the enhanced benefit of sleep in childhood even outweighs the benefits of prior knowledge during learning, such that for children (but not adults) consolidation processes can supersede the effects of prior knowledge in the days following initial learning. We also revealed developmental differences in the benefits of learning closer to sleep. Namely, adults' explicit memory one week after learning benefitted from increased time spent awake after learning (i.e., they showed better long-term memory if they learned in the morning), but children (particularly those with weaker vocabulary) benefit from sleeping sooner after learning. We have replicated this latter effect with younger children utilizing a more naturalistic bedtime story paradigm, in which parents were given materials to read to their children.
In summary, this strand of research has strengthened our theoretical knowledge of word learning in development, and also has the potential to feed into practical solutions for optimizing the word learning process (e.g., by timing learning closer to sleep for some children).
(ii) Individual differences
We have used two key atypical populations, to examine how variability in language development relates to developing sleep architecture: autism and developmental language disorder. We have identified key differences in the sleep architecture of children with autism relative to typical peers. Specifically, lower power in the sleep spindle frequency range and less time in NREM (particularly the deepest stage of sleep). Such sleep atypicalities appear to have knock on effects for longer-term retention of new language material, such that children with autism show increased forgetting of new semantic features of words over multiple nights. For children with autism, we also found that sleep plays a more general role in supporting memory for general task performance, rather than being specifically associated with enhancing memory for novel information, counter to typically developing children. However, for other aspects of language consolidation - fine tuning of existing lexical representations to understand a new accent - are intact in autism. More research is needed to understand why only some aspects of memory consolidation are impaired in autism. We have also been running studies to examine the presence of sleep difficulties in children with developmental language disorder, showing that parents (and practitioners) are highly likely to report sleep onset difficulties in this population and that the maturation of sleep patterns in infancy predict vocabulary knowledge at school entry, raising the hypothesis that children with developmental language disorder may have an early history of sleep difficulties that impact on language development.
(iii) Sleep and mental health.
The pandemic offered us the opportunity to focus on two studies to examine relationships between sleep and mental health, in developing and atypical populations. Firstly, we used the UK Biobank Database to examine relationships between sleep, cognition and mental health in an aging autism and neurotypical population. Here, we found significantly stronger associations between objective measures sleep and mental health in adults with autism than adults from the general population. Second, in an online survey study of parents during the first lockdown period in the UK, we examined how childhood sleep changed during lockdown and how these changes were associated with child mental health (symptoms of anxiety and depression). Bedtime anxiety predicted how long it took children to fall asleep at night at the start of the first lockdown, and later in the year when many restrictions had been lifted. Bedtime and wake-up time shifted at the onset of lockdown, but interestingly total sleep time was resilient (likely owing to an absence of early school start times) and was not predicted by child anxiety. Together, these findings further support calls for sleep to be taken as a key indicator of mental health in adults and children.
Exploitation Route There are a large number of questions that could be further explored: (i) refining developmental differences in neurocognitive mechanisms of memory, (ii) capitalising on the pedagogically relevant findings, to better understand how to optimize learning in the classroom, (iii) feeding the findings into sleep-based interventions for children with autism/language difficulties, (iv) larger/longitudinal efforts to better understand the influence of early sleep patterns on later cognitive, brain and mental health development across a transdiagnostic sample.
Sectors Education,Healthcare

 
Description Sleep Manifesto
Geographic Reach National 
Policy Influence Type Contribution to a national consultation/review
 
Description Child Development
Amount £60,000 (GBP)
Organisation The Waterloo Foundation 
Sector Charity/Non Profit
Country United Kingdom
Start 05/2018 
End 04/2019
 
Description Collaboration Fund
Amount £10,749 (GBP)
Organisation White Rose University Consortium 
Sector Academic/University
Country United Kingdom
Start 07/2016 
End 07/2017
 
Description Collaborative Award
Amount £78,282 (GBP)
Organisation Economic and Social Research Council 
Sector Public
Country United Kingdom
Start 09/2017 
End 08/2021
 
Description ASD-UK 
Organisation Autism Spectrum Database - UK
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution ASD-UK is a UK research family database of children with an autism spectrum disorder (ASD). The aim of ASD-UK is to provide accurate data about children with an ASD to facilitate research and give families the opportunity to take part in research studies. The project is funded by Autistica (www.autistica.org.uk). We submitted an application for ASD-UK to aid recruitment for our grant experiments. This was successful and ASD-UK are now distributing information to families on their database.
Collaborator Contribution This collaboration required us to submit a proposal, including ethical details, and provide information sheets and consent forms to distribute to relevant families. This collaboration came at a small cost of £250
Impact n.a
Start Year 2017
 
Description Born in Bradford: Early sleep and language 
Organisation Bradford Institute for Health Research (BIHR)
Department Born in Bradford
Country United Kingdom 
Sector Public 
PI Contribution We have been collaborating with Born in Bradford to examine the impact of early sleep maturation on vocabulary at school entry, in the Born in Bradford 1000 cohort.
Collaborator Contribution They supplied the data.
Impact KNOWLAND, V., BERENS, S., GASKELL, M., WALKER, S., & HENDERSON, L. (2021). Does the maturation of early sleep patterns predict language ability at school entry? A Born in Bradford study. Journal of Child Language, 1-23. doi:10.1017/S0305000920000677
Start Year 2019
 
Description The bedtime story effect 
Organisation University of Sussex
Country United Kingdom 
Sector Academic/University 
PI Contribution This was a collaborative project between the team of researchers involved in the current grant and Dr Jessica Horst at the University of Sussex. We carried out a project examining the advantages of exposing 3-5-year-old children to new words in bedtime stories (i.e., immediately before going to sleep) in comparison to exposing them to new words 2 hours before bed for memory consolidation. Parallel studies in the grant are examining similar questions at school age and adulthood. This enabled us to test theoretical hypotheses about the changing role of wake-based interference across development, in addition to raising practical implications for optimising word learning in childhood.
Collaborator Contribution The study was designed collaboratively with Dr Horst with data collection driven from York. Unfortunately, the materials used for this collaborative project (taken from Horst's lab) were not suited to the purpose of examining consolidation in the ways intended, and hence we abandoned this project, switching to existing in-house materials.
Impact An invited external seminar at the University of Sussex: Henderson, L.M. What role does sleep play in vocabulary acquisition? Perspectives from typical and atypical development. University of Sussex, February 2016
Start Year 2016
 
Description UK Bioank 
Organisation UK Biobank
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution We are working with UK Biobank to analyse data accelerometer and subjective sleep data from adults diagnosed with autism, examining relationships between sleep, cognition, mental health and sleep variables.
Collaborator Contribution n/a
Impact In progress
Start Year 2019
 
Description Annual sleep lecture University of York 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact A talk to raise awareness of the importance of sleep for cognitive and mental health. Lead to a question and answer session. We have delivered this annually for the previous three years.
Year(s) Of Engagement Activity 2018
 
Description Parent talk at Lighthouse School 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Talk to parents and teachers of children with autism spectrum disorders, raising awareness of the importance of monitoring and treating sleep difficulties.
Year(s) Of Engagement Activity 2018
 
Description Radio Interview (BBC Radio York) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact A radio interview on the importance of sleep for memory development in children, and and opportunity to advertise our grant project.
Year(s) Of Engagement Activity 2016
 
Description Radio interview (BBC Radio Humberside) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact This interview provided an opportunity to advertise our grant experiments in an effort to inform the general public on the importance of sleep and aid recruitment to our studies.
Year(s) Of Engagement Activity 2016
 
Description Series of School Assemblies 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact We have delivered many assemblies to local schools on the purpose of sleep. The aims have been two-fold: (1) to increase public awareness of the importance of sleep and inform schools/students on our research, and (2) to aid recruitment to our studies
Year(s) Of Engagement Activity 2016,2017
 
Description York Autism Awareness day 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Patients, carers and/or patient groups
Results and Impact Presentation to parents and general public to raise awareness of sleep difficulties, sleep associated problems and how to improve sleep, in the context of autism spectrum conditions. This worked to communicate our research goals and outcomes to a wide audience, and initiated further engagement events.
Year(s) Of Engagement Activity 2019