Sleep's Role on Episodic Memory Consolidation
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SLEEP ’S ROLE ON EPISODIC MEMORY CONSOLIDATION IN ADULTS AND CHILDREN Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften der Mathematisch-Naturwissenschaftlichen Fakultät und der Medizinischen Fakultät der Eberhard-Karls-Universität Tübingen vorgelegt von Jing-Yi Wang aus Shijiazhuang, Hebei, Volksrepublik China Dezember, 2016 Tag der mündlichen Prüfung: February 22 , 2017 Dekan der Math.-Nat. Fakultät: Prof. Dr. W. Rosenstiel Dekan der Medizinischen Fakultät: Prof. Dr. I. B. Autenrieth 1. Berichterstatter: Prof. Dr. Jan Born 2. Berichterstatter: Prof. Dr. Steffen Gais Prüfungskommission: Prof. Manfred Hallschmid Prof. Dr. Steffen Gais Prof. Christoph Braun Prof. Caterina Gawrilow I Declaration: I hereby declare that I have produced the work entitled “Sleep’s Role on Episodic Memory Consolidation in Adults and Children”, submitted for the award of a doctorate, on my own (without external help), have used only the sources and aids indicated and have marked passages included from other works, whether verbatim or in content, as such. I swear upon oath that these statements are true and that I have not concealed anything. I am aware that making a false declaration under oath is punishable by a term of imprisonment of up to three years or by a fine. Tübingen, the December 5, 2016 ........................................................ Date Signature III To my beloved parents – Hui Jiao and Xuewei Wang, Grandfather – Jin Wang, and Frederik D. Weber 致我的父母:焦惠和王学伟 爷爷王金,以及 爱人王敬德 V Content Abbreviations .................................................................................................................................................... 1 List of publications in the cumulative thesis ........................................................................................ 3 Summary ............................................................................................................................................................. 5 Zusammenfassung .......................................................................................................................................... 7 Synopsis .............................................................................................................................................................. 9 Introduction .................................................................................................................................................. 9 1. Memory in general ............................................................................................................................................ 9 2. Episodic memory and related brain structures .................................................................................. 11 Experimental paradigms to assess episodic memory .......................................................................................... 15 Developmental trajectories of episodic memory ................................................................................................... 17 Interdependency of semantic memory and episodic memory ........................................................................ 19 3. Sleep ...................................................................................................................................................................... 22 Sleep and memory consolidation .................................................................................................................................. 23 Sleep stages and specific features in memory consolidation ........................................................................... 24 Developmental evidence on sleep and memory consolidation ....................................................................... 26 Objectives and expected output of the doctoral research ......................................................... 28 Conclusion and general discussion .................................................................................................... 31 Forgetting curves differences over sleep and comparing related memory types between children and adults ................................................................................................................................................................................ 32 Limited capacity of sleep on memory consolidation ............................................................................................ 33 Sleep for vivid episodic remembering, episodic forgetting and the relation to semantic memory 35 The candidates of sleep parameters that support episodic memory consolidation .............................. 36 Limitations and outlook ........................................................................................................................ 39 References .................................................................................................................................................. 41 Description of personal contribution ................................................................................................... 53 Acknowledgements ..................................................................................................................................... 55 Appendix .......................................................................................................................................................... 57 VII Abbreviations ANCOVA – Analysis of Covariance ANOVA - Analysis of variance EEG – Electroencephalography HPC – Hippocampus LTD – Long-term depression LTP – Long-term potentiation MTL – Medial temporal lobe PFC – Prefrontal cortex REM – Rapid eye movement SEM – Standard error of the mean SOs – Slow oscillations SWA – Slow-wave activity SW-Rs – Sharp wave ripples SWS – Slow-wave sleep WWWhen – What-Where-When paradigm WWWhich – What-Where-Which paradigm 1 2 List of publications in the cumulative thesis Weber, FD.*, Wang, JY. *, Born, J. & Inostroza, M. (2014). Sleep benefits in parallel implicit and explicit measures of episodic memory. Learning & Memory . 2014. 21: 190-198 (*equal contribution) Wang, JY. *, Weber, FD.*, Zinke, K., Inostroza, M., & Born, J. More effective consolidation of episodic long-term memory in children than adults - Unrelated to sleep (accepted by Child Development ) (*equal contribution) Wang, JY., Weber, FD., Zinke, K., Noack, H., & Born, J. Effects of sleep on word-pair memory in children – separating item and source memory aspects. (Submitted) 3 4 Summary Episodic memory is an essential cognitive function to support our everyday life. It depends on the hippocampus to bind the experienced events into their spatiotemporal contexts, i.e. giving us information about what has happened, where and when. Sleep is vital for declarative memory. Broad evidence suggests sleep as an optimal state to transfer a hippocampus-dependent memory from a temporary short-term representation into its stable neocortical long-term storage, i.e. its consolidation. This sleep-mediated consolidation process is thought to happen especially during deeper slow-wave sleep, i.e. a sleep stage most abundant in children before puberty. It is unclear how sleep consolidates particularly episodic memory, and how sleep-mediated consolidation changes during development. This dissertation aimed to establish new behavioral paradigms and study sleep’s effect on episodic memory in adults and children. We hypothesized that sleep benefits specifically the consolidation of episodic aspects of memory, especially in children. To explore sleep’s effect on episodic memory consolidation in human adults (18-37 years) and children (8-12 years) we established a new episodic task to assess “What-Where-When” memory by explicit (oral report) and implicit (eye-tracking) measures. Additionally, we changed a word-pair learning task to an item–source paradigm, in which word pairs (items) were learned in temporal contexts (source) separated by two lists. This task allowed the assessment of episodic aspects of word-pair learning, i.e. the binding of item and source memory. Using the same tasks, children and adults encoded two episodes and learned two lists of word pairs, with each episode and list being separated by an hour. Memory was then tested on short-term (1-hour delay) prior to sleep as well as after long-term retention (~10-h delay) with either a night of sleep or a day of wakefulness. In adults, explicit and implicit measures of episodic memory were positively associated with each other, and both benefitted from sleep, thus linking this sleep benefit to previous rodent studies and opening the possibility to apply this paradigm to a broader age range (study I). 5 Comparing adults with children, both ages showed a two-fold benefit for episodic memory after sleep than after wakefulness, even though children had superior amounts of slow-wave sleep. Surprisingly, children started at a much lower episodic memory level on the short-term before sleep than adults, suggesting children had less capacity to encode or retain episodic memories. However, children did not forget the episodes any further over the any long-term retention interval as the adults did, suggesting the consolidation of episodic memory in children to be more efficient, and unrelated to sleep (study II). Replicating previous studies, we also found that children benefit from sleep for the explicitly learned word-pair memory over sleep. Unlike the weak temporal memory effect in the episodic task, we found a