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Memory reactivation across distinct vigilance states: A multimodal neural decoding approach in humans

English title Memory reactivation across distinct vigilance states: A multimodal neural decoding approach in humans
Applicant Schwartz Sophie
Number 159862
Funding scheme Project funding (Div. I-III)
Research institution Dépt des Neurosciences Fondamentales Faculté de Médecine Université de Genève
Institution of higher education University of Geneva - GE
Main discipline Neurophysiology and Brain Research
Start/End 01.07.2015 - 30.06.2019
Approved amount 429'000.00
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All Disciplines (3)

Discipline
Neurophysiology and Brain Research
Psychology
Neurology, Psychiatry

Keywords (12)

Sleep; Neural reactivation; Neural decoding; MRI; Learning and Memory; Emotion; Neural plasticity; EEG; Reward; Synaptic downscaling; Homeostasis; Affective processes

Lay Summary (French)

Lead
Le but principal de ce projet est de mieux comprendre comment le sommeil contribue à notre bien-être émotionnel. Nous utilisons une approche de « décodage neuronal » pour montrer que l’activité cérébrale enregistrée lorsque nous vivons des événements émotionnels peuvent réémerger spontanément pendant que nous dormons. Les résultats de ce projet vont révéler les mécanismes cérébraux qui sous-tendent l’impact du sommeil (ou du manque de sommeil) sur la mémoire et les processus affectifs.
Lay summary

La recherche récente démontre que le sommeil favorise la réactivation et la consolidation de mémoire récentes. Cependant, on ne comprend toujours pas bien comment notre cerveau fait pour sélectionner et rejouer les informations les plus pertinentes. D’un point de vue évolutionniste, il est important que les individus se souviennent des informations qui assurent la survie ou la reproduction, comme trouver de la nourriture ou un partenaire sexuel, ou (surtout pour les humains) de l’argent ou des louages. Ainsi, des événements associés à des récompenses ont plus de chance d’être rejoués pendant le sommeil. Le but du présent projet est de tester cette hypothèse. Nous utilisons des méthodes avancées de décodage cérébral pour détecter des réactivations neuronal spontanées. Nos données nouvelles prouverons que des activations cérébrales correspondant à des comportements éveillés peuvent être réactivées pendant le sommeil, en particulier si ces comportements ont été récompensés (comme gagner à un jeu). Ce projet identifiera un mécanisme neuronal qui permet aux éléments les plus importants de notre vie de s’inscrire de manière permanente dans notre mémoire alors que nous dormons. 

En démontrant un rôle du sommeil dans la reactivation et la consolidation des mémoires émotionnelles, ce projet contribuera à une meilleure compréhension des troubles du sommeil et des émotions dans des pathologies comme les troubles anxieux, le stress post-traumatique, ou l’insomnie. De plus, en prouvant que les récompenses et le sommeil améliorent l’apprentissage, ce projet influencera le développement de stratégies éducatives ou de rééducation. Finalement, parce que les perturbations du sommeil émergent comme un problème de santé grandissant, associé à des conséquences socioéconomiques désastreuseuses, cette recherche pourra servir à sensibiliser les individus et les décideurs à se soucier du sommeil, qui représente (encore) environ un tiers de notre temps de vie.

 

Direct link to Lay Summary Last update: 05.07.2015

Lay Summary (English)

Lead
This project aims at a better understanding of the role of sleep in our emotional well-being. We use an advanced “neural decoding approach” to show for the first time that patterns of brain activity recorded while we experience emotional events spontaneously reemerge while we sleep. The results from this project will uncover the neural mechanisms underlying the impact of sleep (and lack of thereof) in memory and affective processes.
Lay summary

Recent research demonstrates that sleep favors the reactivation and consolidation of newly acquired memories. Yet, how our brain selects the noteworthy information that will be reprocessed during sleep remains largely unknown. From an evolutionary perspective, individuals must remember information leading to a positive outcome which promotes survival or reproduction, such as obtaining food or sexual partners, or (mostly in humans) money or praise. Thus, rewarded events are likely to be reactivated in priority during sleep. This project aims to tests this hypothesis. We will thus use advanced brain decoding methods to detect spontaneous neural replay. Our new data will provide evidence for the reactivation, during slow-wave sleep, of brain activation patterns corresponding to recent waking behavior. Critically, the expected results should also demonstrate a privileged replay of spatio-temporal patterns of neural activity associated with a rewarded action (i.e. winning a game). This project will thus uncover a neural mechanism whereby the most valuable elements of our lives are getting permanently engraved on our memory while we sleep.

By supporting a role for the neurobiology of sleep in the spontaneous reemergence and consolidation of emotional human memories, this project may make a significant contribution to the understanding of altered sleep and emotional functions in clinical disorders, such as anxiety disorder, post-traumatic stress disorder, depression, and insomnia. Moreover, the demonstration that rewards and sleep improve learning will have repercussions on the development of educational and clinical rehabilitation strategies. Finally, because sleep disturbances constitute a growing and pervasive health problem, with disastrous socioeconomic and public safety consequences, this research is expected to encourage individuals and decision makers to care about sleep, which (still) represents about a third of our entire lifetime.

Direct link to Lay Summary Last update: 05.07.2015

Responsible applicant and co-applicants

Employees

Publications

Publication
Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis
Sterpenich Virginie, Perogamvros Lampros, Tononi Giulio, Schwartz Sophie (2019), Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis, in Human Brain Mapping, hbm.24843-hbm.24843.
Increased heartbeat-evoked potential during REM sleep in nightmare disorder
Perogamvros Lampros, Park Hyeong-Dong, Bayer Laurence, Perrault Aurore A., Blanke Olaf, Schwartz Sophie (2019), Increased heartbeat-evoked potential during REM sleep in nightmare disorder, in NeuroImage: Clinical, 22, 101701-101701.
Reward-enhanced encoding improves relearning of forgotten associations
Miendlarzewska Ewa A., Ciucci Sara, Cannistraci Carlo V., Bavelier Daphne, Schwartz Sophie (2018), Reward-enhanced encoding improves relearning of forgotten associations, in Scientific Reports, 8(1), 8557-8557.
Interactions Between Large-Scale Functional Brain Networks are Captured by Sparse Coupled HMMs
Bolton Thomas A. W., Tarun Anjali, Sterpenich Virginie, Schwartz Sophie, Van De Ville Dimitri (2018), Interactions Between Large-Scale Functional Brain Networks are Captured by Sparse Coupled HMMs, in IEEE Transactions on Medical Imaging, 37(1), 230-240.
Sleep deprivation disrupts the contribution of the hippocampus to the formation of novel lexical associations
Sterpenich Virginie, Ceravolo Leonardo, Schwartz Sophie (2017), Sleep deprivation disrupts the contribution of the hippocampus to the formation of novel lexical associations, in Brain and Language, 167, 61-71.
Sleep does not facilitate insight in older adults
Debarnot Ursula, Rossi Marta, Faraguna Ugo, Schwartz Sophie, Sebastiani Laura (2017), Sleep does not facilitate insight in older adults, in Neurobiology of Learning and Memory, 140, 106-113.
Linking Individual Learning Styles to Approach-Avoidance Motivational Traits and Computational Aspects of Reinforcement Learning
Carl Aberg Kristoffer, Doell Kimberly C., Schwartz Sophie (2016), Linking Individual Learning Styles to Approach-Avoidance Motivational Traits and Computational Aspects of Reinforcement Learning, in PLOS ONE, 11(11), e0166675-e0166675.
The “Creative Right Brain” Revisited: Individual Creativity and Associative Priming in the Right Hemisphere Relate to Hemispheric Asymmetries in Reward Brain Function
Aberg Kristoffer Carl, Doell Kimberly C., Schwartz Sophie (2016), The “Creative Right Brain” Revisited: Individual Creativity and Associative Priming in the Right Hemisphere Relate to Hemispheric Asymmetries in Reward Brain Function, in Cerebral Cortex, 27(10), 4946-4959.
The left hemisphere learns what is right: Hemispatial reward learning depends on reinforcement learning processes in the contralateral hemisphere
Aberg Kristoffer Carl, Doell Kimberly Crystal, Schwartz Sophie (2016), The left hemisphere learns what is right: Hemispatial reward learning depends on reinforcement learning processes in the contralateral hemisphere, in Neuropsychologia, 89, 1-13.
Influence of reward motivation on human declarative memory
Miendlarzewska Ewa A., Bavelier Daphne, Schwartz Sophie (2016), Influence of reward motivation on human declarative memory, in Neuroscience & Biobehavioral Reviews, 61, 156-176.
Hemispheric Asymmetries in Striatal Reward Responses Relate to Approach-Avoidance Learning and Encoding of Positive-Negative Prediction Errors in Dopaminergic Midbrain Regions
Aberg K. C., Doell K. C., Schwartz S. (2015), Hemispheric Asymmetries in Striatal Reward Responses Relate to Approach-Avoidance Learning and Encoding of Positive-Negative Prediction Errors in Dopaminergic Midbrain Regions, in Journal of Neuroscience, 35(43), 14491-14500.

Collaboration

Group / person Country
Types of collaboration
R. Khatami/Klinik Barmelweid, Aarau Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
D. Sander/NCCR science affective/University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
P. Franken/University of Lausanne Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
C. Michel/Neuroscience/University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
G. Vandewalle/Cyclotron Center/University of Liege Belgium (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
M. Tafti/University of Lausanne Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
D. Van De Ville/HUG-EPFL Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
P. Vuilleumier/Neuroscience/University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
- Industry/business/other use-inspired collaboration
M. Muhlethaler/Neuroscience/University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
G.Pourtois/University of Ghent, Belgium Belgium (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
K. Rauss/University of Tuebingen Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
M. Seeck/Epilepsy/University Hospital Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
I. Arnulf/Pitié-Salpétrière, Paris France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Annual Meeting of the Swiss Society for Neuroscience Poster Sleep deprivation increases the motivational value of high calorie food, but not in uncontrollable eaters. 01.02.2019 Geneva, Switzerland Riontino Laura;
Comment naissent les bonnes idées Talk given at a conference Sommeil, rêve et créativité 18.01.2019 Lausanne, Switzerland Schwartz Sophie;
Sleep and Consciousness meeting Individual talk Emotional memory (re)processing in sleep and dreams 03.10.2018 Lyon, France Schwartz Sophie;
Congress of the European Sleep Research Society (ESRS) Poster Sleep deprivation alters affective and neural responses to erotic stimuli in heterosexual males. 25.09.2018 Basel, Switzerland Riontino Laura;
EPS Conference Talk given at a conference Acute physical exercise improves memory consolidation in humans via BDNF and endocannabinoid signaling 18.04.2018 Leicester, Great Britain and Northern Ireland Igloi Kinga;
Swiss Society for Neuroscience Poster Acute physical exercise improves declarative and motor memory consolidation in humans 09.02.2018 Zurich, Switzerland Igloi Kinga;
ARF annual research forum 2018 Talk given at a conference Acute physical exercise improves memory consolidation in humans via BDNF and endocannabinoid signaling 07.02.2018 Genève, Switzerland Igloi Kinga;
ABIM 2017 Poster Acute physical exercise improves memory consolidation in humans via BDNF and endocannabinoid signaling 08.01.2018 Champéry, Switzerland Igloi Kinga;
Society for Neuroscience Annual Meeting Poster Acute physical exercise improves memory consolidation in humans via BDNF and endocannabinoid signaling 11.11.2017 Washington, United States of America Igloi Kinga;
ICOM conference Individual talk What factors influence hippocampal-prefrontal interactions to optimize memory consolidation? 17.07.2017 Budapest, Hungary Montagrin Alison;
BBL-CIBM day 2017 Talk given at a conference Acute physical exercise improves memory consolidation in humans via BDNF and endocannabinoid signaling 21.06.2017 Genève, Switzerland Igloi Kinga;
NCCR phasing out Talk given at a conference Sleep ...& Emotions 18.05.2017 Geneva, Switzerland Schwartz Sophie;
International Association for the Study of Dreams – online conference Talk given at a conference Processing emotionally-relevant memories in sleep and dreams 11.11.2016 Online conference, Finland Schwartz Sophie;
Symposium of the Clinical Research Priority Program «Sleep and Health» Talk given at a conference Sleep modulates affective and reward functions in humans 07.10.2016 Zurich, Switzerland Schwartz Sophie;
Swiss Society for Neuroscience Talk given at a conference The interplay between social and physical pain in borderline personality disorder 08.01.2016 Lausanne, Switzerland Doell Kimberly;
Society for Neuroscience Individual talk Sleep benefits reward brain functions 17.10.2015 Chicago, United States of America Schwartz Sophie;
Society for Neuroscience Annual Meeting Talk given at a conference A nap to recap or how reward regulates hippocampal-prefrontal memory networks during daytime sleep in humans 17.10.2015 Chicago, United States of America Igloi Kinga;


Self-organised

Title Date Place
Swiss Society for Neuroscience 01.02.2019 Geneva, Switzerland
European Sleep Research Society 25.09.2018 Basel, Switzerland

Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
Series of climate seminars Workshop 04.02.2019 Geneva, Switzerland Igloi Kinga;
Brainhack Geneva Talk Talk 19.11.2018 Geneva, Switzerland Igloi Kinga;


Communication with the public

Communication Title Media Place Year
Media relations: print media, online media Après 21 heures, les adolescents ne devraient plus regarder d’écrans Le Temps Western Switzerland 2019
Media relations: print media, online media Le cauchemar, miroir de notre cerveau Le Temps Western Switzerland 2019
Media relations: print media, online media Comment la musique influence nos rêves et notre sommeil Le Figaro International 2017
Talks/events/exhibitions Discussion avec public au Théatre AmStramGram Western Switzerland 2017
Talks/events/exhibitions Embassy of Foreign Artists (EoFA) - talk Western Switzerland 2017
Media relations: print media, online media Pour bien dormir, il faut éloigner les écrans Pulsations_Junior Western Switzerland 2017
Talks/events/exhibitions Semaine du Cerveau - talk Western Switzerland 2016
Talks/events/exhibitions La Nuit de la Science Western Switzerland 2015

Associated projects

Number Title Start Funding scheme
182589 Deciphering the neural impact of sleep loss on metacognition and empathic judgments for pain in others 01.07.2019 Project funding (Div. I-III)
135653 Emotional relevance and sleep shape neural plasticity: A multimodal neuroimaging investigation in humans 01.09.2011 Project funding (Div. I-III)

Abstract

Recent research provides evidence for memory reactivation during both wakefulness and sleep. The spontaneous reactivation of recent memory traces may contribute to their consolidation. We hypothesize that this mechanism enhances the neural integration and representation of the most important information to optimize future behavior. The overarching aim of the project is to test this hypothesis by using a combination of advanced high-density EEG (hdEEG), functional MRI (fMRI) measurements, and neural decoding. This approach offers an unprecedented opportunity to study the spontaneous reemergence of patterns of neural activity corresponding to specific past experience across distinct vigilance states in humans. A first main goal of the present project is to test whether information with a high relevance for future behavior is favored in the competition for reactivation. We and others recently showed that stimuli or behaviors with an affective relevance (e.g., aversively conditioned or rewarded information) reach improved memory representation at both the cognitive and neural levels after a period of sleep, suggesting that they undergo privileged offline reprocessing during sleep. However, to our knowledge, there is no direct evidence for such selectivity in spontaneous neural replay and its causal role in memory consolidation processes. In the present project, we propose to experimentally manipulate the affective relevance of a task and assess the reactivation of associated brain activity patterns by using neural decoding methods. Applied to activity and connectivity neuroimaging measures with a high spatial and temporal resolution (i.e., fMRI and hdEEG), this approach offers unique insights into the type of neural information that may be reactivated. A second main goal of the project is to decipher how neural reactivation operates across wakefulness and distinct stages of sleep, and how it affects the integration of new information into existing networks of representation. Ruminations and counter-factual thoughts are often reported at sleep onset, whereas the replay of rewarded memories may predominate during slow-wave sleep (SWS). Yet, these phenomena have never been investigated in the same experiment, their neural underpinnings remain unclear, and how they differentially contribute to memory processes is unsettled. We also expect to observe inter-individual differences since, for example, anxious individuals often report ruminations at sleep-onset, which may cause insomnia. A third goal of the project is to investigate another major indicator of experience-dependent local neural plasticity, namely synaptic homeostasis, which can be measured by slow-wave activity (SWA). Whether the emotional relevance of a learning task may also influence the spatial and temporal distribution of SWA during subsequent sleep is unknown. Importantly, while neural replay and synaptic homeostasis may both predominate during SWS, their possible cooperation and respective contributions to overnight brain changes need to be better understood. This project proposal is designed to optimally address each of these goals. The methodological approach proposed is original, reliable, and timely. In particular, it exploits some recent developments in the domain of neural decoding that uniquely allow the study and interpretation of spontaneous brain activity. Moreover, based on concomitant measures of neural reactivation and local SWA, this project seeks to offer an integrative view on these distinct mechanisms of neural plasticity. Finally, by clarifying how emotionally-significant events are selected for offline memory reprocessing, our experimental proposal may provide new insights into the role of sleep (and lack of thereof) in the development, maintenance but also management of some affective disorders. This work may have several important implications. At a theoretical level, by showing how distinct vigilance states contribute to the adaptive and ever-changing nature of memory representations. At a clinical level, by propounding that a healthy emotional balance involves a form of neural reverberation, which helps our brains learn from our daily failures and accomplishments.
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