UNIVERSIDAD COMPLUTENSE DE MADRID FACULTAD DE PSICOLOGÍA TESIS DOCTORAL Cognitive and neural mechanisms of episodic memory reactivation: from consolidation to retrieval Mecanismos cognitivos y neurales de la reactivación de la memoria episódica: de la consolidación a la recuperación MEMORIA PARA OPTAR AL GRADO DE DOCTORA PRESENTADA POR María del Carmen Martín-Buro García de Dionisio DIRECTORES Bernhard P. Staresina Fernando Maestú Unturbe Madrid Ed. electrónica 2019 © María del Carmen Martín-Buro García de Dionisio, 2019 UNIVERSIDAD COMPLUTENSE DE MADRID FACULTAD DE PSICOLOGÍA Cognitive and neural mechanisms of episodic memory reactivation: from consolidation to retrieval Mecanismos cognitivos y neurales de la reactivación de la memoria episódica: de la consolidación a la recuperación MEMORIA PARA OPTAR AL GRADO DE DOCTOR PRESENTADA POR: María del Carmen Martín-Buro García de Dionisio BAJO LA DIRECCIÓN DE LOS DOCTORES Bernhard P. Staresina Y Fernando Maestú Unturbe MADRID, 2019 Cognitive and neural mechanisms of episodic memory reactivation: from consolidation to retrieval A doctoral thesis submitted by María del Carmen Martín-Buro García de Dionisio for partial fulfilment of the requirements for the degree of Doctor with International mention under the direction of Dr. Bernhard P. Staresina and Dr. Fernando Maestú at the Faculty of Psychology of the Complutense University of Madrid. Madrid, 2019 A Emilio A mis padres y hermanas A todos los que alguna vez me han enseñado To all those who have ever taught me Contents ACKNOWLEDGEMENTS / AGRADECIMIENTOS ........................ XI LIST OF ABBREVIATIONS ........................................................ XV LIST OF FIGURES ................................................................. XVII LIST OF TABLES ................................................................. XVIII Chapter 1. Summary and outline .................................. 1 SUMMARY .............................................................................. 3 Introduction .................................................................................... 3 Objective ......................................................................................... 3 Experimental study I: Consolidation ................................................ 4 Experimental study II: Retrieval ...................................................... 5 Conclusion ...................................................................................... 5 OUTLINE OF THE THESIS ......................................................... 6 RESUMEN .............................................................................. 9 Introducción ................................................................................... 9 Objetivo .......................................................................................... 9 Estudio experimental I: Consolidación ........................................... 10 Estudio experimental II: Recuperación .......................................... 11 Conclusión .................................................................................... 11 ESTRUCTURA DE LA TESIS ..................................................... 12 vii Chapter 2. Episodic memory: a brief review from psychology and cognitive neuroscience ...................... 15 1. INTRODUCTION ................................................................. 17 2. DEFINITION OF EPISODIC MEMORY .................................... 20 3. COGNITIVE AND NEUROBIOLOGICAL MODELS OF EPISODIC MEMORY ........................................................................... 22 3.1. Encoding .............................................................................. 23 3.2. Consolidation ....................................................................... 27 3.3. Retrieval ............................................................................... 30 4. NEURAL SIGNALS OF EPISODIC MEMORY: FROM EVENT- RELATED RESPONSES TO OSCILLATIONS .............................. 33 4.1. Electrophysiological techniques ............................................. 33 4.2. Electrophysiological signatures of episodic memory ............... 34 5. THE KNOWLEDGE GAPS ..................................................... 38 Chapter 3. Purpose statement .................................... 41 1. GENERAL PURPOSE ........................................................... 43 2. RESEARCH QUESTIONS: OBJECTIVES AND HYPOTHESES ........ 43 2.1. Consolidation: Can consolidation be tracked by the reactivation of specific oscillatory patterns during waking rest? .................. 43 2.2. Retrieval: Can alpha rhythms unite ERP/ERFs and BOLD- fMRI recollection signatures to simultaneously track its temporal and spatial dynamics? ............................................................ 44 3. SIGNIFICANCE OF THE THESIS ............................................ 45 Chapter 4. Experimental study I: Consolidation ......... 47 HIGHLIGHTS ......................................................................... 49 1. INTRODUCTION ................................................................. 49 2. MATERIALS AND METHODS ............................................... 52 2.1. Participants ........................................................................... 52 viii 2.2. Behavioural analysis .............................................................. 52 2.3. Experimental procedure ........................................................ 53 2.4. MEG Recordings .................................................................. 55 2.5. MEG preprocessing ............................................................... 55 2.6. Quantification and statistical analysis .................................... 56 2.6.1. Power analysis ......................................................................... 56 2.6.2. Topography of power oscillatory entrainment during encoding . 57 2.6.3. Encoding conditions specificity: Multivariate pattern analysis (MVPA) .................................................................................. 58 2.6.4. Evidence for sensor-space offline reactivation ........................... 59 2.6.5. Control analysis: specificity of the offline reactivation ............... 61 2.6.6. Source reconstruction .............................................................. 61 2.6.7. Evidence for source-space offline reactivation ........................... 61 2.6.8. Relationship between reactivation and behavioural performance ............................................................................................... 62 3. RESULTS ........................................................................... 62 3.1. Behavioural results ................................................................ 62 3.2. Encoding reaction times (RTs) ............................................... 62 3.3. Subsequent memory performance .......................................... 63 3.4. Topography of the power entrainment during encoding .......... 63 3.5. Cognitive and perceptual representations can be decoded from the power spectrum during the encoding phase ...................... 64 3.6. Evidence for sensor-space offline reactivation ......................... 66 3.7. Prefrontal and mediotemporal regions track the reactivation of deeply encoded items. ........................................................... 67 3.8. Post-encoding offline reactivation is related to subsequent associative memory performance ........................................... 68 4. DISCUSSION ...................................................................... 70 5. CONCLUSION .................................................................... 74 Chapter 5. Experimental study II: Retrieval ................ 75 HIGHLIGHTS ........................................................................ 77 1. INTRODUCTION ................................................................ 77 2. MATERIALS AND METHODS .............................................. 78 ix 2.1. Experimental procedure ........................................................ 79 2.2. MEG preprocessing ............................................................... 80 2.3. Quantification and statistical analysis..................................... 80 2.3.1. Sensor space time-frequency analysis and statistics ................... 80 2.3.2. Source reconstruction .............................................................. 81 2.3.3. Source space time-frequency and statistics ............................... 81 3. RESULTS ........................................................................... 82 3.1. Behavioural results ................................................................ 82 3.2. Alpha rhythms track time courses of familiarity and recollection …………………………………………………………………….83 3.3. Alpha rhythms track engagement of the core recollection network …………………………………………………………...85 4. DISCUSSION ...................................................................... 86 5. CONCLUSION .................................................................... 89 Chapter 6. General discussion ................................... 91 1. GENERAL DISCUSSION ....................................................... 93 2. CONCLUSIONS ................................................................. 100 References .............................................................. 103 x “The heart is hard to translate” Florence and the Machine Acknowledgements / Agradecimientos I can tell that there have been two turning points in my research