The Role of Sleep in the Formation of Semantic Memory A thesis submitted to the University of Manchester for the degree of Doctor of Philosophy in the Faculty of Medical and Human Sciences 2014 Nora Hennies School of Psychological Sciences Contents List of Figures6 List of Tables7 List of Abbreviations8 Abstract 9 Declaration 10 Copyright Statement 10 Acknowledgements 11 Chapter 1 Introduction: Semantic Memory, Sleep and Consolidation 13 1.1 Overview ..................................... 13 1.2 Semantic memory................................. 14 1.2.1 Semantic memory representations: The hub-and-spoke model . 15 1.2.2 Formation of new conceptual knowledge................ 18 1.3 Memory consolidation .............................. 22 1.3.1 Standard model for systems memory consolidation.......... 22 1.3.2 Semanticisation as a product of memory reorganisation . 24 1.3.3 Schema theory .............................. 26 1.3.4 Schema assimilation model ....................... 27 1.3.5 Relationship between semantic memory and schemas......... 28 1.4 Sleep physiology ................................. 29 1.4.1 Sleep stages................................ 29 1.4.2 Synchrony of sleep-related rhythms................... 32 1.4.3 Synaptic plasticity during sleep..................... 33 1.5 The role of sleep in systems memory consolidation and semanticisation . 34 1.5.1 Active systems consolidation model................... 34 1.5.2 Evidence that memories are processed during sleep.......... 35 1.5.3 Evidence that sleep supports systems memory consolidation . 38 1.6 Summary ..................................... 42 1.7 Research objectives................................ 42 3 Contents Chapter 2 Time- but not sleep-dependent memory consolidation pro- motes the emergence of conceptual knowledge 45 2.1 Abstract...................................... 46 2.2 Introduction.................................... 46 2.3 Methods...................................... 48 2.3.1 Participants................................ 48 2.3.2 Stimuli and stimulus generation..................... 48 2.3.3 Experimental tasks............................ 49 2.3.4 Procedure................................. 52 2.3.5 Statistical analysis............................ 52 2.4 Results....................................... 53 2.4.1 Experiment A............................... 53 2.4.2 Experiment B............................... 55 2.5 Discussion..................................... 57 Chapter 3 Cued memory reactivation during SWS abolishes the benefi- cial effect of sleep on abstraction 61 3.1 Abstract...................................... 62 3.2 Introduction.................................... 62 3.3 Methods...................................... 64 3.3.1 Participants................................ 64 3.3.2 Stimuli .................................. 64 3.3.3 Experimental task and design...................... 66 3.3.4 Equipment ................................ 68 3.3.5 Behavioural data analysis........................ 68 3.3.6 PSG data acquisition and analysis ................... 69 3.4 Results....................................... 70 3.4.1 Auditory recall task ........................... 70 3.4.2 Visual recall task............................. 70 3.4.3 Alertness and response times ...................... 71 3.4.4 N-back task................................ 71 3.4.5 Association between overnight performance change and SWS . 72 3.4.6 Differences between groups in sleep structure............. 73 3.4.7 Differences between groups in sleep quality .............. 74 3.5 Discussion..................................... 75 Chapter 4 Sleep spindles mark hippocampal to neocortical consolidation of schema-related memories 79 4.1 Abstract...................................... 80 4.2 Introduction.................................... 80 4.3 Results....................................... 82 4.4 Discussion..................................... 88 4.5 Methods...................................... 90 4.5.1 Participants................................ 90 4 Contents 4.5.2 Stimuli .................................. 90 4.5.3 Procedure................................. 91 4.5.4 PSG data acquisition and analysis ................... 91 4.5.5 Statistical analyses............................ 92 4.5.6 fMRI data acquisition and analysis................... 93 4.6 Supplemental material.............................. 95 Chapter 5 A weak schema link is sufficient to trigger the schema benefit and the association with sleep spindles 109 5.1 Abstract......................................110 5.2 Introduction....................................110 5.3 Methods......................................111 5.3.1 Participants................................111 5.3.2 Stimuli ..................................112 5.3.3 Pilot study ................................113 5.3.4 Procedure.................................113 5.3.5 Equipment ................................118 5.3.6 PSG data acquisition and analysis ...................118 5.3.7 Statistical analyses............................119 5.4 Results.......................................119 5.4.1 Subjective ratings ............................119 5.4.2 Behavioural memory performance ...................119 5.4.3 Reaction time results...........................120 5.4.4 Polysomnography results ........................121 5.5 Discussion.....................................124 Chapter 6 General Discussion 127 6.1 The impact of sleep on processes of abstraction and integration . 127 6.1.1 Summary of findings (Chapters 2 and 3) . 127 6.1.2 Relation to semantic memory......................128 6.1.3 Benefit of consolidation on the formation of semantic memory . 129 6.1.4 What determines which memories are processed during sleep? . 130 6.1.5 What determines how memories are processed during sleep? . 131 6.1.6 Underlying mechanisms of memory reorganisation during sleep . 133 6.1.7 Function of sleep versus wakefulness ..................135 6.2 Sleep and the integration of new information with semantic memory . 136 6.2.1 Summary of findings (Chapters 4 & 5) . 136 6.2.2 Schema benefit on memory .......................137 6.2.3 Association between sleep and the schema benefit . 137 6.2.4 Schema-related differences during memory acquisition . 139 6.3 Future directions.................................139 6.4 Conclusions....................................140 Word count: 55,966 5 List of Figures 1.1 Models of conceptualisation........................... 17 1.2 Standard model for systems memory consolidation.............. 24 1.3 Schema assimilation model ........................... 28 1.4 Sleep physiology ................................. 30 1.5 Active systems consolidation model....................... 35 2.1 Category structure and CMCL-task trial structure .............. 50 2.2 Schematic illustration of the experimental procedures............. 53 2.3 Reaction time results for Experiment A and Experiment B ......... 54 3.1 Generation of structured and unstructured sequences............. 65 3.2 Experimental design ............................... 67 3.3 Behavioural results................................ 71 3.4 Relationship between SWS and behavioural performance........... 73 4.1 Experimental design ............................... 82 4.2 Behavioural results................................ 83 4.3 Overnight change in hippocampal activity................... 84 4.4 Spindle-modulated hippocampal activity for the interaction......... 86 4.5 SM: Illustration of the schema structure.................... 95 4.6 SM: Spindle-related hippocampal activity ...................105 5.1 Schema structure.................................113 5.2 Experimental design ...............................114 5.3 Encoding and recall trials ............................117 5.4 Response accuracy................................121 5.5 Reaction time results...............................122 5.6 Spindle density predicts the overnight change in the schema effect . 123 6 List of Tables 2.1 Parameters for the stimulus generation..................... 49 2.2 Results of the explicit memory tasks of Experiment A ............ 55 2.3 Results of the explicit memory tasks of Experiment B ............ 56 3.1 Polysomnography results............................. 72 3.2 Power spectral density during slow wave sleep................. 74 3.3 Overall sleep quality............................... 74 3.4 Sleep quality of slow wave sleep......................... 75 4.1 SM: Examples of schema-related facts ..................... 96 4.2 SM: Schema-learning procedure......................... 98 4.3 SM: Polysomnography results..........................100 4.4 SM: Activation clusters for the contrast recent > remote . 102 4.5 SM: Activation clusters for the interaction contrast . 103 4.6 SM: Activation clusters for the interaction contrast modulated by spindle density.......................................104 4.7 SM: Activation cluster for the overnight change of schema-related facts, modulated by spindle density..........................104 4.8 SM: Polysomnography results of the control group . 106 4.9 SM: Activation clusters for the interaction contrast modulated by the SWS spindle density ..................................107 5.1 Examples of schema-related facts........................112 5.2 Procedure and tasks involved in the schema-learning . 116 5.3 Polysomnography results.............................124 7 Abbreviations ANOVA Analysis of variance BBSRC Biological Sciences Research Council EEG Electroencephalography fMRI functional magnetic resonance imaging KSS Karolinska