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Emotional relevance and sleep shape neural plasticity: A multimodal neuroimaging investigation in humans

English title Emotional relevance and sleep shape neural plasticity: A multimodal neuroimaging investigation in humans
Applicant Schwartz Sophie
Number 135653
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 01.09.2011 - 30.06.2015
Approved amount 331'000.00
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All Disciplines (2)

Discipline
Neurophysiology and Brain Research
Psychology

Keywords (8)

Sleep; Emotion; Perceptual Learning; Neural Plasticity; Functional MRI; EEG; Individual differences; Dreaming

Lay Summary (English)

Lead
Lay summary

Sleep boosts learning and underlying neural plasticity. Yet the factors that govern the selection of information to be further consolidated in sleep remain largely unknown. Here, we hypothesize that the affective relevance of a stimulus affects its subsequent reprocessing during sleep, at both the cognitive and neural levels. Specifically, the proposed experiments will test whether sleep and emotion interact to foster a shift in memory representations, and may thus influence subsequent decision making.

Our main goal is to investigate the role of the affective significance of a stimulus on offline memory processes, particularly during sleep, both at the behavioral and neural levels in healthy adult humans. We also test ask whether the strength of the emotional effects on memory and neural responses varies across individuals and correlates with individual differences in emotions in dreams. We use functional magnetic resonance imaging and electroencephalography to measure changes in neural activity and connectivity during sleep after emotional learning.

The project addresses fundamental and timely questions about the role of sleep in cognitive and affective processes. The expected results will establish emotional relevance as a key component of sleep-related memory consolidation and dreaming. It will also show that specific neural mechanisms mediate these emotional effects on brain plasticity, therefore clarifying the physiological links between the regulation of sleep-wake states and affective processes that serve the optimization of waking behavior. Because sleep disturbances constitute a major and pervasive health problem, our results are also expected to substantially improve awareness about the important socioeconomical consequences of sleep curtailment on education and well-being.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Influence of reward motivation on human declarative memory
Miendlarzewska E. A., Bavelier D., Schwartz S. (2016), Influence of reward motivation on human declarative memory, in Neuroscience and biobehavioral reviews, 61, 156-76.
A nap to recap or how reward regulates hippocampal-prefrontal memory networks during daytime sleep in humans
Igloi K., Gaggioni G., Sterpenich V., Schwartz S. (2015), A nap to recap or how reward regulates hippocampal-prefrontal memory networks during daytime sleep in humans, in eLife, 4, 0.
Disrupted Sleep: From Molecules to Cognition
Van Someren E. J., Cirelli C., Dijk D. J., Van Cauter E., Schwartz S., Chee M. W. (2015), Disrupted Sleep: From Molecules to Cognition, in The Journal of neuroscience : the official journal of the Society for Neuroscience, 35, 13889-95.
Dreaming, Neural Basis of
Perogamvros L., Schwartz S. (2015), Dreaming, Neural Basis of, in Wright J. (ed.), 650-656.
Emotion, Motivation, and Reward in Relation to Dreaming
Schwartz S., Perogamvros L. (2015), Emotion, Motivation, and Reward in Relation to Dreaming, in Kryger M. H. (ed.), 567-570.
Increased Reward-Related Behaviors during Sleep and Wakefulness in Sleepwalking and Idiopathic Nightmares
Perogamvros L., Aberg K., Gex-Fabry M., Perrig S., Cloninger C. R., Schwartz S. (2015), Increased Reward-Related Behaviors during Sleep and Wakefulness in Sleepwalking and Idiopathic Nightmares, in PloS one, 10, 0134504-0134504.
Sleep and emotional functions
Perogamvros L., Schwartz S. (2015), Sleep and emotional functions, in Current topics in behavioral neurosciences, 25, 411-31.
Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning
Sterpenich V., Piguet C., Desseilles M., Ceravolo L., Gschwind M., Van De Ville D., Vuilleumier P., Schwartz S. (2014), Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning, in NeuroImage, 100, 608-18.
Le rêve, une forme de thérapie: Le retour du refoulé dans le rêve à la lumière de la recherche empirique
Schmidt R., Schwartz S. (2013), Le rêve, une forme de thérapie: Le retour du refoulé dans le rêve à la lumière de la recherche empirique, in Psychoscope, 12, 12.
Dissociating learning-induced changes in fMRI signal from structural modifications: a comment on Dorjee and Bowers (2012)
Rauss K., Schwartz S. (2012), Dissociating learning-induced changes in fMRI signal from structural modifications: a comment on Dorjee and Bowers (2012), in Cortex; a journal devoted to the study of the nervous system and behavior, 48, 515.
Sommeil, rêves et régulation des émotions
Desseilles M., Mikolajczak M., Schwartz S. (2012), Sommeil, rêves et régulation des émotions, in Mikolajczak M. Desseilles M. (ed.), 87.
The roles of the reward system in sleep and dreaming.
Perogamvros Lampros, Schwartz Sophie (2012), The roles of the reward system in sleep and dreaming., in Neuroscience and biobehavioral reviews, 36(8), 1934-51.
Decoding brain states from fMRI connectivity graphs
Richiardi J., Eryilmaz H., Schwartz S., Vuilleumier P., Van De Ville D. (2011), Decoding brain states from fMRI connectivity graphs, in NeuroImage, 56, 616-26.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Society for Neuroeconomics Annual Meeting 2013, Lausanne, Switzerland Poster Separate influences of phasic and tonic reward delivery schemes on associative memory 27.09.2013 Lausanne, Switzerland Miendlarzewska Ewa; Schwartz Sophie; Doell Kimberly;
CISA conference, Geneva Talk given at a conference Sleep, emotion, and brain plasticity 24.09.2013 Geneva, Switzerland Schwartz Sophie; Miendlarzewska Ewa; Sander David;
Exploratory Workshop on ‘Dream, Sleep, Emotion’ Talk given at a conference Sleep, dreams, and emotions 12.09.2013 Geneva, Switzerland Schwartz Sophie; Miendlarzewska Ewa;
Congress of the European Association for Behavioral and Cognitive Therapies (EABC), Geneva, Switzerland Poster Sleep, dreams and the reward system 20.08.2013 Geneva, Switzerland Schwartz Sophie;
19th Annual Meeting of the Organization for Human Brain Mapping (OHBM), 16-20 Jun. 2013 Seattle, WA, USA Poster A nap to recap: Reward strengthens relational memory during daytime sleep 16.06.2013 Seattle, United States of America Igloi Kinga; Schwartz Sophie;
Annual meeting of the Swiss Society for Sleep Research, Sleep Medicine and Chronobiology, Aarau, Switzerland Talk given at a conference A nap to recap: Reward strengthens relational memory during daytime sleep 23.05.2013 Aarau, Switzerland Igloi Kinga; Schwartz Sophie;
11ème Colloque de la Société des neurosciences, Lyon, France Talk given at a conference What is the role of sleep in the consolidation of emotional memory? 23.04.2013 Lyon, France Schwartz Sophie;
24th Annual Meeting of the American Neuropsychiatric Association, Boston, USA Poster Active reward processing during sleep: insights from dreaming and parasomnias 16.04.2013 Boston, United States of America Schwartz Sophie;
8th Alpine Brain Imaging Meeting (ABIM) 6-10 Jan. 2013, Champéry, Switzerland Talk given at a conference A nap to recap: Reward strengthens relational memory during daytime sleep 06.01.2013 Champéry, Switzerland Schwartz Sophie; Igloi Kinga;
Society for Neuroeconomics Annual Meeting 2012, Miami, USA Poster Dual role of the reward-system in reinforcement learning styles and creativity 28.09.2012 Miami, United States of America Schwartz Sophie;
“What does human intra-cerebral recording tell us about emotions?” Geneva, Switzerland, scientific committee Talk given at a conference What does human intra-cerebral recording tell us about emotions? 19.09.2012 Geneva, Switzerland Schwartz Sophie; Igloi Kinga; Van De Ville Dimitri; Miendlarzewska Ewa;
Congress of the European Sleep Research Society, Paris, France. Invited talk. “Emotions in dreams relate to emotional brain reactivity during wakefulness”. Talk given at a conference Emotions in dreams relate to emotional brain reactivity during wakefulness 05.09.2012 Paris, France Schwartz Sophie;
“Behind and beyond the brain” meeting, Bial Foundation, Porto (Portugal). Invited talk: “Dreams, emotions, and brain plasticity” Talk given at a conference Dreams, emotions, and brain plasticity 28.03.2012 Porto, Portugal Schwartz Sophie;
Société Française de Recherche et Médecine du Sommeil, Strasbourg (France). Invited inaugural talk: “Sommeil, émotion et mémoire” Talk given at a conference Sommeil, émotion et mémoire 23.11.2011 Strassbourg, France, France Schwartz Sophie;
Swiss Neurological Society and the Swiss Society for Sleep Research, Sleep Medicine and Chronobiology (SSSSC), St. Gallen (Switzerland). Invited talk: “Sleep, dreams, and emotions” Talk given at a conference Sleep, dreams, and emotions 03.11.2011 St-Gallen, Switzerland Schwartz Sophie;


Self-organised

Title Date Place
Alpine Brain Imaging Meeting 11.01.2015 Champery, Switzerland
Alpine Brain Imaging Meeting 12.01.2014 Champéry, Switzerland
Annual Meeting Swiss Society for Sleep Research, Sleep Medicine and Chronobiology SSSSC 23.05.2013 Aarau, Switzerland
Alpine Brain Imaging Meeting 06.01.2013 Champery, Switzerland
What does human intra-cerebral recording tell us about emotions? 19.09.2012 Paris, France
Alpine Brain Imaging Meeting 08.01.2012 Champery, Switzerland

Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
FENS-IBRO European Neuroscience School ‘Imaging Training Center 2013: Imaging Human Brain Structure and Function’ Workshop 02.09.2013 Geneva, Switzerland Schwartz Sophie; Miendlarzewska Ewa; Van De Ville Dimitri; Sander David; Igloi Kinga;
Pulsation Junior: A quoi ca sert de dormir? Performances, exhibitions (e.g. for education institutions) 02.05.2013 Geneva, Switzerland Schwartz Sophie;
Parcours sommeil-cerveau Performances, exhibitions (e.g. for education institutions) 12.03.2013 Geneva, Switzerland Bayer Laurence; Schwartz Sophie; Miendlarzewska Ewa;
Semaine du cerveau (chaque année les membres de mon laboratoire contribue activement à animer des activités) Performances, exhibitions (e.g. for education institutions) 12.03.2012 Geneva, Switzerland Doell Kimberly; Bayer Laurence; Van De Ville Dimitri; Schwartz Sophie; Miendlarzewska Ewa; Igloi Kinga; Sander David;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions Sommeil et apprentissage (semaine du cerveau) Western Switzerland 2015
Media relations: print media, online media A quoi ça sert de dormir? UNIGE-HUG, Pulsation Junior Western Switzerland 2014
Media relations: radio, television “36.9” interview on the negative impact of the lack of sleep on cognition and emotion RTS Rhaeto-Romanic Switzerland 2013
Media relations: radio, television Dreaming: a historical view New Scientist International 2013
Media relations: print media, online media Interview about M. Jouvet Science & Avenir International 2013
Media relations: print media, online media Interview with S. Schwartz on dreaming Science & Vie International 2013
Media relations: print media, online media La face cachée du sommeil RTS, UNIGE, HUG Western Switzerland 2013
Media relations: print media, online media Rêver Revue de Sciences Humaines International 2013
Media relations: print media, online media Mémoire émotionnelle et sommeil paradoxal Cerveau & Psycho International Western Switzerland 2011

Awards

Title Year
Best Oral Communication Prize from the Swiss Society for Sleep Research, Sleep Medicine and Chronobiology. 2013

Associated projects

Number Title Start Funding scheme
124763 Interactions of dopamine and hypocretin in sleep-wake functions: Vigilance, emotional processing, and learning in patients with narcolepsy, restless legs syndrome, Parkinson’s disease and healthy controls 01.08.2009 Project funding (Div. I-III)
149731 Influence of rocking on sleep and memory: A multidisciplinary investigation in people and mice with good or poor sleep 01.01.2014 Interdisciplinary projects
159862 Memory reactivation across distinct vigilance states: A multimodal neural decoding approach in humans 01.07.2015 Project funding (Div. I-III)
114008 Sleep-related changes in cerebral activity underlying perceptual and emotional learning 01.05.2007 Project funding (Div. I-III)
104100 Pathophysiology of narcolepsy - a multimodal approach 01.08.2004 Project funding (Div. I-III)

Abstract

Background: Recent data has accumulated to suggest that sleep boosts learning and underlying neural plasticity. Yet the factors that govern the selection of information to be further consolidated in sleep remain largely unknown. Here, we hypothesize that the affective relevance of a stimulus affects its subsequent reprocessing during sleep, at both the cognitive and neural levels. Specifically, the proposed experiments will test whether sleep and emotion interact to foster a shift in memory representations, and may thus influence subsequent decision making. Several lines of evidence suggest interactions between sleep and affective processes: a) sleep disorders are frequently associated with emotion disorders; b) limbic, mesolimbic, and ventral medial prefrontal regions, all involved in the processing of emotional relevance, are activated during human rapid eye movement sleep; c) consistent with an activation of emotion circuits during sleep, subjective experiences during sleep (i.e. dreams) can be highly emotional; d) waking neuronal activation associated with a rewarded task is replayed during sleep in hippocampus and ventral striatal regions in rodents. Furthermore, our recent fMRI work on narcoleptic patients shows that brain circuits involved in the stabilization of sleep-wake states (hypocretin/orexin system) exert a strong influence on emotional learning and reward-related responses in mesolimbic dopamine regions and in the amygdala. Together these findings provide new and converging support for substantial functional interactions between sleep and emotion brain circuits. We believe that this emerging view is promising both for fundamental research and for its implications for understanding diseases and promoting public health.Aims/hypotheses: Our main goal is to investigate the role of the affective significance of a stimulus on offline memory processes, particularly during sleep, both at the behavioral and neural levels in healthy adult humans. The following hypotheses are tested. a) The emotional value or relevance of a stimulus guides the selection of memories that will be subsequently consolidated. b) Sleep represents a permissive period for memory reprocessing and neural remodeling to occur. c) Sleep and emotion interact to induce changes in memory representations. d) The neural mechanisms underlying these effects involve influences of emotional circuits (limbic and mesolimbic networks) onto sensory and/or memory systems. e) The strength of the emotional effects on memory and neural responses varies across individuals and correlates with individual differences in emotions in dreams. Methods: To experimentally manipulate the emotional relevance of a stimulus, we use two paradigms that involve distinct brain structures: aversive conditioning (amygdala, insula) and reward learning (striatum, ventral tegmental area). To test for the effects of sleep on memory, we measure behavioral performance and whole-brain fMRI activity after a delay that includes sleep or not. With simultaneous EEG and fMRI, we directly assess changes in neural activity and connectivity during sleep after emotional learning, and use dedicated methods to detect any reactivation of patterns of brain activity corresponding to emotionally-relevant material. Correlations with individual dream data are performed.Potential value of the project: The project addresses fundamental and timely questions about the role of sleep in cognitive and affective processes. It involves innovative cognitive tasks, a unique combination of methodological approaches, as well as outstanding technical facilities and scientific expertise, which together guarantee the success of this ambitious project. The expected results (based on our preliminary findings) will establish emotional relevance as a key component of sleep-related memory consolidation and dreaming. It will also show that specific neural mechanisms mediate these emotional effects on brain plasticity, therefore clarifying the physiological links between the regulation of sleep-wake states and affective processes that serve the optimization of waking behavior. Because sleep disturbances constitute a major and pervasive health problem, our results are also expected to substantially improve awareness about the important socioeconomical consequences of sleep curtailment on education and well-being.
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