Changes in Emotional Responses to Aversive Pictures Across Periods Rich in Slow-Wave Sleep Versus Rapid Eye Movement Sleep
Abstract
Objective Since Freud's "Interpretation of Dreams," sleep has been related to emotional functions, where dreams were assumed to play a cathartic role. In psychophysiological research, this role was attributed mainly to rapid eye movement (REM) sleep. The present study compared processing pictures with negative emotional impact over intervals covering either early sleep dominated by slow-wave sleep (SWS) or late REM sleep-dominated sleep. Method Emotional reactions were assessed by a nonverbal rating procedure along the two emotional dimensions valence (positive vs. negative) and arousal (low vs. high). Two groups of healthy men were tested across 3-hour periods of early and late nocturnal sleep (sleep group) or corresponding intervals filled with wakefulness (wake group). After the intervals, subjects rated new pictures together with old pictures already presented before the interval. Sleep was recorded polysomnographically. Results As expected, the amount of REM sleep was about three times greater during late than early nocturnal sleep, whereas a reversed distribution was observed for SWS (p Conclusions Indicating a priming-like enhancement of emotional reactivity after periods rich in REM sleep, results do not confirm a cathartic function of REM sleep or sleep in general.
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Declarative memory for neutral materials is enhanced by SWS.
“While these studies quite compellingly showed that declarative memory for neutral materials is enhanced by SWS, emotional declarative memories appear to additionally benefit from REM-rich late sleep (1273, 1274).”
From About Sleep's Role in Memory (2013) · cites this paper as [1273]
Emotional declarative memories additionally benefit from REM-rich late sleep.
“While these studies quite compellingly showed that declarative memory for neutral materials is enhanced by SWS, emotional declarative memories appear to additionally benefit from REM-rich late sleep (1273, 1274).”
From About Sleep's Role in Memory (2013) · cites this paper as [1273]
REM sleep-rich sleep amplifies subjectively experienced aversion to previously viewed emotional pictures.
“With respect to emotional reactivity, one study showed that REM sleep-rich sleep amplified subjectively experienced aversion to previously viewed emotional pictures (1273).”
From About Sleep's Role in Memory (2013) · cites this paper as [1273]
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Wassing, R., Schalkwijk, F. W., Lakbila‐Kamal, O., Ramautar, J. R., Stoffers, D., Mutsaerts, H. J. M. M., Talamini, L. M., & Someren, E. J. W. V. (2019) · Brain · doi:10.1093/brain/awz089 · Cited by 72 · see citing works
“2012), or both before and after a period of sleep either in early or late in the night (Wagner et al., 2002; Groch et al., 2013).”
BackgroundChanges in Cardiac Variability after REM Sleep Deprivation in Recurrent Nightmares
Nielsen, T., Paquette, T., Solomonova, E., Lara-Carrasco, J., Colombo, R., & Lanfranchi, P. A. (2010) · SLEEP · doi:10.1093/sleep/33.1.113 · Cited by 89 · see citing works
Signs of REM sleep dependent enhancement of implicit face memory: a repetition priming study
Wagner, U., Hallschmid, M., Verleger, R., & Born, J. (2003) · Biological Psychology · doi:10.1016/s0301-0511(02)00125-4 · Cited by 63 · see citing works
“To control for possible influences of the pituitaryadrenal stress system on sleep-related memory formation (Plihal et al., 1999), cortisol levels were assessed in saliva samples obtained immediately before and after each 3-h interval as described previously (Wagner et al., 2002).”
MethodSelf-citationOvernight neuronal plasticity and adaptation to emotional distress
Cabrera, Y., Koymans, K. J., Poe, G. R., Kessels, H. W. H. G., Someren, E. J. W. V., & Wassing, R. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00799-w · Cited by 66 · see citing works
“During REM sleep , instead of being”
Werner, G. G., Schabus, M., Blechert, J., Kolodyazhniy, V., & Wilhelm, F. (2015) · Psychophysiology · doi:10.1111/psyp.12404 · Cited by 63 · see citing works
Gilson, M., Deliens, G., Leproult, R., Bodart, A., Nonclercq, A., Ercek, R., & Peigneux, P. (2015) · Brain Sciences · doi:10.3390/brainsci6010001 · Cited by 58 · see citing works
“Contrarily however, enhanced emotional reactivity and increased negative valence ratings for emotional pictures were reported after late-night sleep periods rich in REM sleep [18].”
BackgroundREM sleep and memory reorganization: Potential relevance for psychiatry and psychotherapy
Landmann, N., Kühn, M., Maier, J.-G., Spiegelhalder, K., Baglioni, C., Frase, L., Riemann, D. W., Sterr, A., & Nissen, C. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.01.004 · Cited by 56 · see citing works
Pickett, S. M., Barbaro, N., & Mello, D. (2015) · Psychological Trauma Theory Research Practice and Policy · doi:10.1037/tra0000064 · Cited by 54 · see citing works
Rihm, J. S., & Rasch, B. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.008 · Cited by 50 · see citing works
The Role of Sleep in Human Declarative Memory Consolidation
Alger, S. E., Chambers, A. M., Cunningham, T. J., & Payne, J. D. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_341 · Cited by 49 · see citing works
“An additional experiment found that after a total night of sleep, there was also a shift toward increased aversiveness, comparable to that seen after the late-night REM-rich sleep (Wagner et al. 2002).”
ResultSleep and intrusive memories immediately after a traumatic event in emergency department patients
Porcheret, K., Iyadurai, L., Bonsall, M. B., Goodwin, G. M., Beer, S., Darwent, M., & Holmes, E. A. (2020) · SLEEP · doi:10.1093/sleep/zsaa033 · Cited by 45 · see citing works
Role of sleep for encoding of emotional memory
Kaida, K., Niki, K., & Jan Born, A. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.002 · Cited by 45 · see citing works
Memory Processing in Relation to Sleep
Peigneux, P., & Smith, C. T. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00029-3 · Cited by 43 · see citing works
Targeted memory reactivation in REM but not SWS selectively reduces arousal responses
Hutchison, I. C., Pezzoli, S., Tsimpanouli, M.-E., Abdellahi, M. E. A., Pobric, G., Hulleman, J., & Lewis, P. A. (2021) · Communications Biology · doi:10.1038/s42003-021-01854-3 · Cited by 43 · see citing works
Sleep divergently affects cognitive and automatic emotional response in children
Bolinger, E., Jan Born, A., & Zinke, K. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.05.015 · Cited by 42 · see citing works
Kim, S. Y., Kark, S. M., Daley, R. T., Alger, S. E., Reboucas, D. A., Kensinger, E. A., & Payne, J. D. (2019) · Hippocampus · doi:10.1002/hipo.23138 · Cited by 42 · see citing works
Sleep deprivation affects reactivity to positive but not negative stimuli
Pilcher, J. J., Callan, C., & Posey, J. L. (2015) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2015.05.003 · Cited by 41 · see citing works
“The current results differ from previous findings that suggest responses to aversive pictures are most vulnerable to the effects of sleep deprivation (Wagner et al., 2002; Franzen et al., 2008; Franzen et al., 2009).”
ResultMemory Consolidation during Sleep: Role of Cortisol Feedback
BORN, J., & WAGNER, U. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.020 · Cited by 51 · see citing works
Self-citationGroch, S., Preiss, A., McMakin, D. L., Rasch, B., Walitza, S., Huber, R., & Wilhelm, I. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1912-16.2017 · Cited by 39 · see citing works
“SAM is a nonverbal instrument for the assessment of emotional responses to a stimulus found to be suitable for this purpose in previous studies using International Affective Picture System pictures (Hamm et al., 1993; Wagner et al., 2002; Groch et al., 2013).”
MethodMild Traumatic Brain Injury Chronically Impairs Sleep- and Wake-Dependent Emotional Processing
Mantua, J., Henry, O. S., Garskovas, N. F., & Spencer, R. M. C. (2017) · SLEEP · doi:10.1093/sleep/zsx062 · Cited by 37 · see citing works
The impact of five nights of sleep restriction on emotional reactivity
Tempesta, D., Salfi, F., Gennaro, L. D., & Ferrara, M. (2020) · Journal of Sleep Research · doi:10.1111/jsr.13022 · Cited by 37 · see citing works
“Indeed, Wagner, Fischer, and Born (2002) suggested that sleep increases emotional reactivity, showing that subjective ratings of the negative valence following late sleep were more negative for pictures viewed before sleep compared to new, unfamiliar pictures.”
BackgroundNielsen, T., O’Reilly, C., Carr, M., Dumel, G., Godin, I., Solomonova, E., Lara-Carrasco, J., Blanchette‐Carrière, C., & Paquette, T. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.09.007 · Cited by 35 · see citing works
Paré, D., & Headley, D. B. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100529 · Cited by 35 · see citing works
“…Paré and D.B. Headley Neurobiology of Stress 24 (2023) 100529 scripts (Wagner et al., 2001) and images (Hu et al., 2006; Nishida et al., 2009; Wagner et al., 2002), and to the recall (Kumar and Jha, 2012) and extinction of conditioned fear responses (Fu et al., 2007; Pace-Schott et al.,…”
BackgroundAi, S., Chen, J., Liu, J., He, J., Xue, Y.-X., Bao, Y., Han, F., Tang, X., Lü, L., & Shi, J. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.005 · Cited by 33 · see citing works
Werner, G. G., Schabus, M., Blechert, J., & Wilhelm, F. H. (2020) · Behavioral Sleep Medicine · doi:10.1080/15402002.2020.1713134 · Cited by 34 · see citing works
“(used in many studies), REM sleep has been linked with increased emotional responses when measured directly after sleep (e.g., Gilson et al., 2015; Lara-Carrasco et al., 2009; Wagner et al., 2002), whereas at least three hours after awakening from sleep, REM sleep (versus no REM sleep) has”
BackgroundMethodTargeted Memory Reactivation During REM Sleep in Patients With Social Anxiety Disorder
Borghese, F., Henckaerts, P., Guy, F., Mayo, C., Delplanque, S., Schwartz, S., & Perogamvros, L. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.904704 · Cited by 33 · see citing works
“Thus, REM sleep would not strengthen the emotional tone of memories (Baran et al., 2012; Jones & Spencer, 2019; Wagner et al., 2002; Werner et al., 2015), but might instead consolidate negative memories while attenuating their emotional tone (Cunningham et al.”
BackgroundPorcheret, K., der Kloet, D. V. H., Goodwin, G. M., Foster, F., Wulff, K., & Holmes, E. A. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0403-z · Cited by 31 · see citing works
Sleep Preserves Physiological Arousal in Emotional Memory
Ashton, J. E., Harrington, M. O., Guttesen, A. Á. V., Smith, A. K., & Cairney, S. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-42478-2 · Cited by 34 · see citing works
Sleep's benefits to emotional processing emerge in the long term
Bolinger, E., Cunningham, T. J., Payne, J. D., Bowman, M. A., Bulca, E., Jan Born, A., & Zinke, K. (2019) · Cortex · doi:10.1016/j.cortex.2019.07.008 · Cited by 31 · see citing works
Hornung, O. P., Regen, F., Warnstedt, C., Anghelescu, I., Danker‐Hopfe, H., Heuser, I., & Lammers, C. (2007) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2007.07.001 · Cited by 31 · see citing works
How Emotional Arousal Enhances Episodic Memory
Baraly, K. T. A., Hot, P., Davidson, P. S. R., & Talmi, D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21051-1 · Cited by 30 · see citing works
“While sleep deprivation has myriad implications, REM-sleep may be particularly important to these changes in neural responses.”
BackgroundResultInfluentialPolta, S., Fenzl, T., Jakubcakova, V., Kimura, M., Yassouridis, A., & Wotjak, C. T. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00060 · Cited by 28 · see citing works
“Also, REMS has been proposed to play a role in re-processing emotional information and stabilizing emotional reactivity (Horne, 2000; Wagner, 2002; Walker, 2009; Walker and van der Helm, 2009; Gujar et al., 2011; van der Helm et al., 2011; Baran et al., 2012; Groch et al., 2012).”
BackgroundLong lasting alteration in REM sleep of female rats submitted to long maternal separation
Tiba, P. A., Tufik, S., & Suchecki, D. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.10.001 · Cited by 27 · see citing works
“In clinical studies, there have been attempts to associate personality features and coping style with changes in REM sleep patternafterdisturbingevents[42, 43 ]Unfortunately,nodefinitive conclusions have been reached.”
BackgroundSleep and Affective Brain Regulation
van der Helm, E., & Walker, M. P. (2012) · Social and Personality Psychology Compass · doi:10.1111/j.1751-9004.2012.00464.x · Cited by 26 · see citing works
Emotional Modulation of Pain and Spinal Nociception in Persons with Severe Insomnia Symptoms
DelVentura, J. L., Terry, E. L., Bartley, E. J., & Rhudy, J. L. (2013) · Annals of Behavioral Medicine · doi:10.1007/s12160-013-9551-1 · Cited by 25 · see citing works
Glosemeyer, R. W., Diekelmann, S., Cassel, W., Kesper, K., Koehler, U., Westermann, S., Steffen, A., Borgwardt, S., Wilhelm, I., Müller‐Pinzler, L., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-74169-8 · Cited by 25 · see citing works
Ballot, O., Daviaux, Y., Sanz-Arigita, E. J., Ivers, H., Micoulaud-Franchi, J. A., Bioulac, S., Philip, P., Morin, C. M., & Altena, E. (2021) · Sleep Medicine · doi:10.1016/j.sleep.2021.10.014 · Cited by 22 · see citing works
Interactions between Sleep and Emotions in Humans and Animal Models
Lefter, R. M., Cojocariu, R. O., Ciobica, A. S., Balmuș, I.-M., Mavroudis, I. A., & Kis, A. (2022) · Medicina · doi:10.3390/medicina58020274 · Cited by 24 · see citing works
“In addition, considering that differences between early and late-night REM sleep were previously described [18], Khan et al.”
BackgroundTo sleep or not to sleep – Effects on memory in normal aging and disease
Kroeger, D., & Vetrivelan, R. (2023) · Aging Brain · doi:10.1016/j.nbas.2023.100068 · Cited by 25 · see citing works
“If, as several reports indicate, REM sleep serves to enhance emotional memories during sleep [289,290], then it might be reasonable in certain circumstances to advocate for REM sleep deprivation as a therapeutic tool after traumatic events to prevent these memories from being strengthened [291].”
BackgroundDenis, D., Kim, S. Y., Kark, S. M., Daley, R. T., Kensinger, E. A., & Payne, J. D. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15132 · Cited by 23 · see citing works
Sleep benefits emotional and neutral associative memories equally
Lehmann, M., Seifritz, E., & Rasch, B. (2016) · Somnologie - Schlafforschung und Schlafmedizin · doi:10.1007/s11818-015-0034-4 · Cited by 22 · see citing works
“Evidence for this model is somewhat inconsistent, as studies have reported the role of sleep indepotentiation[4, 24], but also theprotection [2, 9] or even potentiation [18, 31] of emotional reactivity to arousing stimuli.”
ResultHuman Studies of Sleep and Off-line Memory Reprocessing
Stickgold, R. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198574002.003.0003 · Cited by 22 · see citing works
Lerner, I., Lupkin, S. M., Corter, J. E., Peters, S. E., Cannella, L. A., & Gluck, M. A. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.032 · Cited by 20 · see citing works
“In contrast, Wagner et al. (2002) found REM sleep to intensify the perceived negativity of negative stimuli.”
BackgroundSleep and the generalization of fear learning
Davidson, P., Carlsson, I., Jönsson, P., & Johansson, M. (2015) · Journal of Sleep Research · doi:10.1111/jsr.12339 · Cited by 20 · see citing works
“Furthermore, sleep has been found to both increase (Pace-Schott et al., 2011) and decrease (Baran et al., 2012; Wagner et al., 2002) intersession habituation to negative images.”
BackgroundSleep preserves subjective and sympathetic emotional response of memories
Jones, B. J., & Spencer, R. M. C. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107096 · Cited by 20 · see citing works
“Preservation or strengthening of valence and arousal ratings has been linked to REM sleep (Baran et al., 2012, Lara-Carrasco et al., 2009, Wagner et al., 2002).”
BackgroundResultDavidson, P., & Pace-Schott, E. F. (2021) · Current Sleep Medicine Reports · doi:10.1007/s40675-020-00200-z · Cited by 20 · see citing works
Sleep selectively stabilizes contextual aspects of negative memories
Cox, R., van Bronkhorst, M. L. V., Bayda, M., Gomillion, H., Cho, E., Parr, E., Manickas-Hill, O. P., Schapiro, A. C., & Stickgold, R. (2018) · Scientific Reports · doi:10.1038/s41598-018-35999-9 · Cited by 20 · see citing works
Griffith, E. L., Jin, L., Contractor, A. A., Slavish, D. C., & Vujanovic, A. A. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.06.052 · Cited by 18 · see citing works
Neural Dynamics of Emotional Salience Processing in Response to Voices during the Stages of Sleep
Chen, C., Sung, J., & Cheng, Y. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00117 · Cited by 18 · see citing works
“Nocturnal sleep rich in REM sleep had a priming-like enhancement of emotional reactivity (Wagner et al., 2002).”
BackgroundRoles of Early and Late Nocturnal Sleep for the Consolidation of Human Memories
Jan Born, A., & Gais, S. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198574002.003.0004 · Cited by 18 · see citing works
Sleep’s role in updating aversive autobiographical memories
Azza, Y., Wilhelm, F. H., Seifritz, E., Junghanns, K., Kleim, B., & Wilhelm, I. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01878-1 · Cited by 17 · see citing works
“More specifically, some studies reported that sleep decreases [20, 21], or even increases [22] the emotional tone as measured by both subjective ratings and physiological response (i.”
BackgroundZink, N., & Pietrowsky, R. (2015) · International journal of dream research · doi:10.11588/ijodr.2015.1.17811 · Cited by 17 · see citing works
Murdoch, M., Partin, M. R., Vang, D., & Kehle‐Forbes, S. (2018) · Journal of Empirical Research on Human Research Ethics · doi:10.1177/1556264618810302 · Cited by 16 · see citing works
Pesonen, A., Koskinen, M.-K., Vuorenhela, N., Halonen, R., Mäkituuri, S., Selin, M., Luokkala, S., Suutari, A., & Hovatta, I. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105714 · Cited by 16 · see citing works
“Also, in healthy participants, the evidence for the dissipation of affective load in sleep is not without controversies, as decreases in emotional reactivity have not been observed in all studies (Wagner et al., 2002, Baran et al., 2012).”
ResultMemory Processing in Relation to Sleep
Peigneux, P., Fogel, S. M., & Smith, C. T. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-24288-2.00022-2 · Cited by 16 · see citing works
Emotional Memory Consolidation During Sleep
Cunningham, T. J., & Payne, J. D. (2017) · Studies in neuroscience, psychology and behavioral economics · doi:10.1007/978-3-319-45066-7_9 · Cited by 15 · see citing works
- Authors
- Wagner, U.
- Affiliations
- University of Lübeck (DE)
- Corresponding author
- Wagner, U.
- ORCID
- Wagner, U.
- Venue
- Psychosomatic Medicine
- Published
- 2002-07-01
- Volume
- 64
- Issue
- 4
- Pages
- 627-634
- ISSN
- 0033-3174 (ISSN-L)
- 1534-7796
- OpenAlex
- W2013586907
- Cited by
- 152
- References
- 54
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 12 · 2021: 9 · 2020: 7 · 2019: 13 · 2018: 6 · 2017: 7 · 2016: 6 · 2015: 18 · 2014: 9 · 2013: 10 · 2012: 9
- FWCI
- 1.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychosomatic Medicine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- REM sleep, slow-wave sleep, emotional reactivity, valence, arousal, sleep and emotion, catharsis, dream function
- MeSH terms
- Adolescent, Adult, Affect, Electroencephalography, Electromyography, Electrooculography, Humans, Hydrocortisone, Hypothalamo-Hypophyseal System, Judgment, Male, Nonverbal Communication, Pituitary-Adrenal System, Surveys and Questionnaires, Random Allocation, Saliva, Semantics, Sleep, Sleep, REM, Visual Perception, Polysomnography
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