Sleep and Cognition in Children with
Down Syndrome and Williams Syndrome
Anna Fiona Ashworth
Thesis submitted for the degree of Doctor of Philosophy
Institute of Education, University of London
Prepared under the supervision of Dr. Dagmara Dimitriou,
Dr. Cathy M. Hill and Professor Annette Karmiloff-Smith
March 2013
Leading education and social research KT Institute of Education University of London
1 "It is a common experience that a problem difficult at night is resolved in the morning after the committee of sleep has worked on it."
—John Steinbeck, 1902 — 1968, American writer
2 Abstract
This thesis provides a novel contribution to cognitive and developmental psychology by investigating the relationship between sleep, behaviour and cognition in 41 healthy typically developing (TD) children, 22 children with Down syndrome (DS) and 22 with Williams syndrome (WS). In addition, developmental changes in sleep and cognition, and the importance of sleep for consolidation of new memories were assessed in these groups. Finally, the influence of children's sleep and behaviour on their mothers' sleep and wellbeing were examined. The research used a battery of standardised and novel cognitive tasks, objective measures of sleep, and questionnaires.
Sleep problems were syndrome-specific, with poor sleep quality and oxyhaemoglobin desaturation occurring more frequently in DS, suggestive of breathing difficulties during sleep, and long sleep latencies in the WS group. TD children performed well on cognitive tasks of short term memory, working memory and sustained attention compared to children with DS and WS, and their performance generally improved with increasing age, which tended not to be the case for the clinical groups. In the TD group, improved sleep quality and higher, less variable oxyhaemoglobin saturation related to better performance on cognitive tasks and fewer behavioural problems. Few associations between sleep, cognition and behaviour were found in the DS and WS groups. TD children and children with WS showed evidence of sleep-dependent memory consolidation for explicitly learnt material on two tasks. Mothers of children with DS had the poorest sleep and most daytime sleepiness, though not related to children's sleep or daytime behaviour.
The findings indicate that sleep problems should be assessed and managed in clinical groups.
Educational strategies should be implemented to reinforce sleep-related learning gains. Future research could examine whether sleep-dependent learning occurs in relation to specific aspects of sleep architecture in children with DS and WS, as it does in adults and TD children.
Declaration
I, Anna Fiona Ashworth, confirm that the work presented in this thesis is entirely my own. Where
information has been derived from other sources, explicit attribution is made.
Word count (exclusive of appendices, list of references and bibliography): 68,330 words.
3 Acknowledgements
Without a doubt, completing this PhD has been my most challenging yet rewarding accomplishment.
I am eternally grateful to both of my supervisors, Dr Dagmara Dimitriou and Dr Cathy Hill for giving me the opportunity to undertake this project and for their support, guidance and encouragement throughout. I also thank Professor Annette Karmiloff-Smith for being such an inspiring mentor, as well as providing such valuable advice and feedback.
I sincerely thank the Williams Syndrome Foundation UK and the Down Syndrome Education
International for kindly funding this project. Thank you also to all the families and children who took part, and to their teachers who allowed me to visit them in school; I am indebted to all of them, as without them this project would not have been possible.
I thank my family and friends for their support and confidence in me, in particular my parents, Jan and Allan for always cheering me up, calming me down and believing in me. Particular thanks go to
Dr Tessa Dekker, Lucy Irving and Dr Jo Van Herwegan for always providing kind and sound advice on
PhD and other related (and unrelated) issues. Finally, special thanks to my amazing fiancé, Xabi
Joyce, and Nieves, for your encouragement, emotional support, for looking after me and putting up with me. Xabi, you remind me that there is more to life than work.
4
Table of Contents
Abstract 3
Declaration 3
Acknowledgements 4
Table of Contents 5
List of Figures 11
List of Tables 12
List of Terms and Abbreviations 14
Thesis Overview 15
1. Sleep and Learning 16
1.1 Introduction 16
1.2 Sleep Physiology 17
1.2.1 History of sleep research 17
1.2.2 Adult sleep architecture 17
1.2.3 The development of sleep architecture from infancy to old age 20
1.2.4 Physiological regulation of sleep 21
1.2.5 Functional neuroanatomy during sleep 22
1.2.6 Ethnic and cultural differences in sleep 23
1.3 Sleep Problems in Typical Development 23
1.3.1 Insomnias 24
1.3.2 Sleep-disordered breathing 24
1.3.3 Parasomnias 25
1.3.4 Periodic limb movement disorder 26
1.3.5 Daytime sleepiness 26
1.4 Functions of Sleep 26
1.4.1 Executive functions 27
1.4.2 Attention 30
1.4.3 Behaviour 33
5 1.4.4 Mood 34
1.4.5 School performance 35
1.4.6 Speech and language 36
1.4.7 Physiological functions of sleep 37
1.5 Sleep-Dependent Memory Consolidation 39
1.5.1 Sleep-dependent declarative memory consolidation 40
1.5.2 Sleep-dependent procedural memory consolidation 45
1.6 Measurements of Sleep 49
1.6.1 Polysomnography 49
1.6.2 Video recording 50
1.6.3 Actigraphy 50
1.6.4 Pulse oximetry 51
1.6.5 Questionnaires 52
1.7 Chapter summary 52
2. Down Syndrome and Williams Syndrome 55
2.1 Introduction 55
2.2 Down Syndrome 56
2.2.1 Clinical features 57
2.2.2 Cognitive features 59
2.2.3 Behavioural characteristics 64
2.2.4 Sleep 65
2.2.5 Sleep and cognition 68
2.3 Williams Syndrome 69
2.3.1 Clinical features 70
2.3.2 Cognitive features 72
2.3.1 Behaviour 79
2.3.2 Sleep 80
2.3.3 Sleep and cognition 83
6 2.4 Problems for Parents of Children with Developmental Disorders 85
2.5 Chapter summary 87
2.6 Aims and Hypotheses 88
3. Pilot Studies 91
3.1 Introduction 91
3.2 Declarative Memory Task 91
3.2.1 Associated word pairs task 91
3.2.2 Unrelated word pairs task 93
3.2.3 Novel Animal Names task 94
3.3 Procedural memory task 96
3.3.1 Don't Buzz the Wire! 96
3.3.2 Contour integration task 98
3.3.3 Tower of Hanoi 99
3.3.4 Continuous Performance Task 101
3.4 Chapter Summary 103
4. Methodology 104
4.1 Ethical approval 104
4.2 Participants 104
4.2.1 Exclusion criteria 104
4.2.2 Recruitment 104
4.2.3 Sample 105
4.3 Materials 105
4.3.1 Sleep measures 106
4.3.2 Experimental tasks 109
4.3.3 Animal Names declarative learning task 110
4.3.4 Tower of Hanoi cognitive procedural learning task 111
4.3.5 Continuous performance task 111
4.3.6 Raven's Coloured Progressive Matrices 111
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4.3.7 Short term and working memory span 112
4.4 Questionnaires 113
4.4.1 Children's Sleep Habits Questionnaire 113
4.4.2 Temperament in Middle Childhood Questionnaire 114
4.4.3 Strengths and Difficulties Questionnaire 114
4.4.4 Pittsburgh Sleep Quality Index (for parents) 115
4.4.5 Epworth Sleepiness Scale (for parents) 115
4.4.6 Major Depression Inventory (for parents) 116
4.5 General Procedure Summary 116
4.6 Statistical analysis 117
4.6.1 Group means 117
4.6.2 Age-related effects 118
4.6.3 Sleep-related effects 118
5. Results 120
5.1 Sleep Measures 120
5.1.1 Actigraphy 120
5.1.2 Pulse oximetry 124
5.2 Standardised Tests 125
5.2.1 Raven's Coloured Progressive Matrices 125
5.2.2 Short-Term and working memory span 130
5.3 Experimental Tasks 139
5.3.1 Animal Names declarative learning task 139
5.3.2 Tower of Hanoi procedural learning task 143
5.3.3 Continuous Performance Task 152
5.4 Questionnaires 157
5.4.1 Children's Sleep Habits Questionnaire 158
5.4.2 Temperament in Middle Childhood Questionnaire 162
5.4.3 Strengths and Difficulties Questionnaire 165
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5.4.4 Parent questionnaires 168
6. Discussion 173
6.1 Summary 173
6.2 Sleep 173
6.2.1 Actigraphy and pulse oximetry 173
6.2.2 Children's Sleep Habits Questionnaire 177
6.2.3 Comparison of parent report, actigraphy and pulse oximetry 178
6.3 Sleep-dependent learning 179
6.3.1 Animal Names task 180
6.3.2 Tower of Hanoi 181
6.3.3 General comments on sleep-dependent learning 184
6.4 Continuous Performance Task 185
6.5 Short term and working memory 188
6.5.1 Sleep, short term and working memory 189
6.6 Behavioural questionnaires 190
6.6.1 Sleep and behaviour 192
6.7 Parent questionnaires 192
6.8 Developmental effects 193
6.9 Implications 195
6.10 Future directions 197
6.11 Conclusions 199
References 201
Appendix A. Pilot study materials 237
Al. Related word pairs 237
A2. Unrelated word pairs 237
A3. Animal Names 237
Appendix B. Recruitment material 238
B1. Consent form 238
9 B2. Invitation letter to parents 239
B3. Participant information sheet 240
Appendix C. Questionnaires 243
C1. Children's Sleep Habits Questionnaire (CSHQ) 243
C2. Temperament in Middle Childhood Questionnaire (TMCQ) 246
C3. Definitions of TMCQ subscales 252
C4. Strengths and Difficulties Questionnaire (SDQ) 253
C5. Pittsburgh Sleep Quality Index (PSQI) 255
C6. Epworth Sleepiness Scale (ESS) 258
C7. Major Depression Inventory (MDI) 259
10 List of Figures
Figure 1.1. Showing EEG signal of wakefulness and sleep stages 18
Figure 1.2. Hypnogram showing typical adult sleep architecture (adapted from Hill, Hogan, &
Karmiloff-Smith, 2007). 19
Figure 1.3. Developmental changes to duration of daytime and night-time sleep 20
Figure 1.4. Graph showing time (minutes) spent in each sleep stage, sleep latency and wake after
sleep onset over the lifespan. Source: Carskadon & Dement (2005) 21
Figure 2.1. Images of children with Down syndrome. 57
Figure 2.2. Images of children with Williams syndrome 71
Figure 3.1. Example of Animal Names Flashcard Images: Basco the Cat and Jaala the Pig 95
Figure 3.2. Image of Don't Buzz the Wire steady-hand game. 97
Figure 3.3. Example of Contour Integration Stimuli: Levels 1 to 6. 98
Figure 3.4. Image of Tower of Hanoi Task. 99
Figure 3.5. Target Images in the Continuous Performance Task. 101
Figure 4.1. Actiwatch mini. 106
Figure 4.2. Screen shot of Sleep Analysis 7 (CamNTech, Cambridge, UK) 107
Figure 4.3. Example actigram. Black bars indicate movement during each epoch. 107
Figure 4.4. Masimo Pulse Oximetry Rad 8 Device. 108
Figure 4.5. Screen shot from Visi-Download software (Stowood Scientific Instruments, Oxford, UK).