REM-enriched naps are associated with memory consolidation for sad stories and enhance mood-related reactivity

Brain Sciences

Volumn 6, Issue 1, 2016, Pages

  Gilson, Médhi ^a,b   Deliens, Gaétane ^a,b,c   Leproult, Rachel ^a,b   Bodart, Alice ^a,b   Nonclercq, Antoine ^d   Ercek, Rudy ^d   Peigneux, Philippe ^a,b  

^a UR2NF Neuropsychology and Functional Neuroimaging Research Unit   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c Cognition and Computation Group ^*  (Belgium)

^d LISA   (Belgium)

Author keywords

Affect; Electrodermal activity; Emotion; Memory; Rapid eye movement; Sleep; Sleep spindles

Indexed keywords

CLINICAL ARTICLE; CONTROLLED STUDY; EXPOSURE; HUMAN; INFORMATION RETRIEVAL; MEMORY CONSOLIDATION; MOOD; RECALL; REM SLEEP; SKIN CONDUCTANCE;

EID: 85013224979     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci6010001     Document Type: Article

References (65)

1. McGaugh, J.L. Time-dependent processes in memory storage. Science 1966, 153, 1351-1358. [CrossRef] [PubMed]
2. Cahill, L. Neurobiological mechanisms of emotionally influenced, long-term memory. Prog. Brain Res. 2000, 126, 29-37. [PubMed]
3. McGaugh, J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 2004, 27, 1-28. [CrossRef] [PubMed]
4. Ochsner, K.N. Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. J. Exp. Psychol. Gen. 2000, 129, 242-261. [CrossRef] [PubMed]
5. Peigneux, P.; Smith, C. Memory processing in relation to sleep. In Principles and Practice of Sleep Medicine, 5th ed.; Kryger, M., Ed.; Elsevier: Philadelphia, PA, USA, 2010; pp. 335-347.
6. Rasch, B.; Born, J. About sleep's role in memory. Physiol. Rev. 2013, 93, 681-766. [CrossRef] [PubMed]
7. Walker, M.P. Sleep, memory and emotion. Prog. Brain Res. 2010, 185, 49-68. [PubMed]
8. Deliens, G.; Gilson, M.; Peigneux, P. Sleep and the processing of emotions. Exp. Brain Res. 2014, 232, 1403-1414. [CrossRef] [PubMed]
9. Genzel, L.; Spoormaker, V.I.; Konrad, B.N.; Desler, M. The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol. Learn. Mem. 2015, 122, 110-121. [CrossRef] [PubMed]
10. Baglioni, C.; Spiegelhalder, K.; Lombardo, C.; Riemann, D. Sleep and emotions: A focus on insomnia. Sleep Med. Rev. 2010, 14, 227-238. [CrossRef] [PubMed]
11. Bower, B.; Bylsma, L.M.; Morris, B.H.; Rottenberg, J. Poor reported sleep quality predicts low positive affect in daily life among healthy and mood-disordered persons. J. Sleep Res. 2010, 19, 323-332. [CrossRef] [PubMed]
12. Mauss, I.B.; Troy, A.S.; LeBourgeois, M.K. Poorer sleep quality is associated with lower emotion-regulation ability in a laboratory paradigm. Cogn. Emot. 2013, 27, 567-576. [CrossRef] [PubMed]
13. Franzen, P.L.; Buysse, D.J.; Dahl, R.E.; Thompson,W.; Siegle, G.J. Sleep deprivation alters pupillary reactivity to emotional stimuli in healthy young adults. Biol. Psychol. 2009, 80, 300-305. [CrossRef] [PubMed]
14. Yoo, S.S.; Gujar, N.; Hu, P.; Jolesz, F.A.;Walker, M.P. The human emotional brain without sleep-A prefrontal amygdala disconnect. Curr. Biol. 2007, 17, R877-R878. [CrossRef] [PubMed]
15. Lang, P.J.; Bradley, M.M.; Cuthbert, B.N. International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual ; Technical Report A-6; University of Florida: Gainesville, FL, USA, 2005.
16. Rosales-Lagarde, A.; Armony, J.L.; del Río-Portilla, Y.; Trejo-Martínez, D.; Conde, R.; Corsi-Cabrera, M. Enhanced emotional reactivity after selective REM sleep deprivation in humans: An fMRI study. Front. Behav. Neurosci. 2012, 6, 25. [CrossRef] [PubMed]
17. Cunningham, T.J.; Crowell, C.R.; Alger, S.E.; Kensinger, E.A.; Villano, M.; Mattingly, S.M.; Payne, J.D. Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep. Neurobiol. Learn. Mem. 2014, 114, 155-164. [CrossRef] [PubMed]
18. Wagner, U.; Fischer, S.; Born, J. Changes in emotional responses to aversive pictures across periods rich in slow-wave sleep versus rapid eye movement sleep. Psychosom. Med. 2002, 64, 627-634. [PubMed]
19. Werner, G.G.; Schabus, M.; Blechert, J.; Kolodyazhniy, V.; Wilhelm, F.H. Pre-to postsleep change in psychophysiological reactivity to emotional films: Late-night REM sleep is associated with attenuated emotional processing. Psychophysiology 2015, 52, 813-825. [CrossRef] [PubMed]
20. Talamini, L.M.; Bringmann, L.F.; de Boer, M.; Hofman, W.F. Sleeping worries away or worrying away sleep? Physiological evidence on sleep-emotion interactions. PLoS ONE 2013, 8, e62480. [CrossRef] [PubMed]
21. Pace-Schott, E.F.; Shepherd, E.; Spencer, R.; Marcello, M.; Tucker, M.; Propper, R.E.; Stickgold, R. Napping promotes inter-session habituation to emotional stimuli. Neurobiol. Learn. Mem. 2011, 95, 24-36. [CrossRef] [PubMed]
22. Lara Carrasco, J.; Nielsen, T.A.; Solomonova, E.; Levrier, K.; Popova, A. Overnight emotional adaptation to negative stimuli is altered by REM sleep deprivation and is correlated with intervening dream emotions. J. Sleep Res. 2009, 18, 178-187. [CrossRef] [PubMed]
23. Hu, P.; Stylos-Allan, M.; Walker, M.P. Sleep facilitates consolidation of emotional declarative memory. Psychol. Sci. 2006, 17, 891-898. [CrossRef] [PubMed]
24. Payne, J.D.; Stickgold, R.; Swanberg, K.; Kensinger, E.A. Sleep preferentially enhances memory for emotional components of scenes. Psychol. Sci. 2008, 19, 781-788. [CrossRef] [PubMed]
25. Wagner, U.; Hallschmid, M.; Rasch, B.; Born, J. Brief sleep after learning keeps emotional memories alive for years. Biol. Psychiatry 2006, 60, 788-790. [CrossRef] [PubMed]
26. Atienza, M.; Cantero, J.L. Modulatory effects of emotion and sleep on recollection and familiarity. J. Sleep Res. 2008, 17, 285-294. [CrossRef] [PubMed]
27. Van Heugten-van der Kloet, D.; Giesbrecht, T.; Merckelbach, H. Sleep loss increases dissociation and affects memory for emotional stimuli. J. Behav. Ther. Exp. Psychiatry 2014, 47, 9-17. [CrossRef] [PubMed]
28. Sterpenich, V.; Albouy, G.; Boly, M.; Vandewalle, G.; Darsaud, A.; Balteau, E.; Dang-Vu, T.T.; Desseilles, M.; D'Argembeau, A.; Gais, S.; et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol. 2007, 5, e282. [CrossRef] [PubMed]
29. Wagner, U.; Gais, S.; Born, J. Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn. Mem. 2001, 8, 112-119. [CrossRef] [PubMed]
30. Nishida, M.; Pearsall, J.; Buckner, R.L.;Walker, M.P. REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb. Cortex 2009, 19, 1158-1166. [CrossRef] [PubMed]
31. Wagner, U.; Degirmenci, M.; Drosopoulos, S.; Perras, B.; Born, J. Effects of cortisol suppression on sleep-associated consolidation of neutral and emotional memory. Biol. Psychiatry 2005, 58, 885-893. [CrossRef] [PubMed]
32. Baran, B.; Pace-Schott, E.F.; Ericson, C.; Spencer, R.M.C. Processing of emotional reactivity and emotional memory over sleep. J. Neurosci. 2012, 32, 1035-1042. [CrossRef] [PubMed]
33. Groch, S.;Wilhelm, I.; Diekelmann, S.; Born, J. The role of REM sleep in the processing of emotional memories: Evidence from behavior and event-related potentials. Neurobiol. Learn. Mem. 2013, 99, 1-9. [CrossRef] [PubMed]
34. Benca, R.M.; Obermeyer,W.H.; Thisted, R.A.; Gillin, J.C. Sleep and psychiatric disorders. A meta-analyses. Arch. Gen. Psychiatry 1992, 49, 651-670. [CrossRef] [PubMed]
35. Cartwright, R.; Luten, A.; Young, M.; Mercer, P.; Bears, M. Role of REM sleep and dream affect in overnight mood regulation: A study of normal volunteers. Psychiatry Res. 1998, 81, 1-8. [CrossRef]
36. Tinguely, G.; Huber, R.; Borbely, A.A.; Achermann, P. Non-rapid eye movement sleep with low muscle tone as a marker of rapid eye movement sleep regulation. BMC Neurosci. 2006, 7, 2. [CrossRef] [PubMed]
37. Deliens, G.; Leproult, R.; Neu, D.; Peigneux, P. Rapid eye movement and non-rapid eye movement sleep contributions in memory consolidation and resistance to retroactive interference for verbal material. Sleep 2013, 36, 1875-1883. [CrossRef] [PubMed]
38. Buysse, D.J.; Reynolds, C.F.; Monk, T.H.; Berman, S.R.; Kupfer, D.J. The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Res. 1989, 28, 193-213. [CrossRef]
39. Johns, M.W. A new method for measuring daytime sleepiness: The Epworth Sleepiness Scale. Sleep 1991, 14, 50-55.
40. Beck, A.T.; Steer, R.A.; Garbin, M.G. Psychometric properties of Beck Depression Inventory: Twenty-five years of evaluation. Clin. Psychol. 1988, 8, 77-100. [CrossRef]
41. Zigmond, A.S.; Snaith, R.P. The hospital anxiety and depression scale. Acta Psychiatr. Scand. 1983, 67, 361-370. [CrossRef] [PubMed]
42. Deltour, J.J. Echelle de Vocabulaire Mill Hill de J. C. Raven: Adaptation Française et normes Comparées du Mill Hill et du Standard Progressive Matrices (PM38). Manuel et Annexes ; Application des Techniques Modernes: Braine le Château, Belgique, 1933.
43. Bagby, R.M.; Parker, J.D.A.; Taylor, G.J. The twenty-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. J. Psychosom. Res. 1994, 38, 23-32. [CrossRef]
44. Horne, J.A.; Ostberg, O.A. Self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 1976, 4, 97-110. [PubMed]
45. Akerstedt, T.; Gillberg, M. Subjective and objective sleepiness in the active individual. Int. J. Neurosci. 1990, 52, 29-37. [CrossRef] [PubMed]
46. Dinges, D.I.; Powell, J.W. Microcomputer analysis of performance on a portable, simple visual RT task sustained operations. Behav. Res. Methods Instrum. Comput. 1985, 17, 652-655. [CrossRef]
47. Bradley, M.M.; Lang, P.J. Measuring emotion: The self-assessment Manikin and the semantic differential. J. Behav. Ther. Exp. Psychiatry 1994, 25, 49-59. [CrossRef]
48. Ekman, P.; Friesen, W.V.; Ellsworth, P. What emotion categories or dimensions can observers judge from facial behavior? In Emotion in the Human Face ; Ekman, P., Ed.; Cambridge University Press: New York, NY, USA, 1972; pp. 39-55.
49. Bertels, J.; Deliens, G.; Peigneux, P.; Destrebecqz, A. The Brussels Mood Inductive Audio Stories (MIAS) database. Behav. Res. Methods 2014, 46, 1098-1107. [CrossRef] [PubMed]
50. Boucsein, W.; Fowles, D.C.; Grimnes, S.; Ben-Shakhar, G.; Roth, W.T.; Dawson, M.E.; Filion, D.L. Publication recommendations for electrodermal measurements. Psychophysiology 2012, 49, 1017-1034. [PubMed]
51. Iber, C.; Ancoli-Israel, S.; Chesson, A.; Quand, S.F. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Technical Specification, 1st ed.; American Academy of Sleep Medicine: Westchester, IL, USA, 2007.
52. Basner, M.; Dinges, D.F. Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. Sleep 2011, 34, 581-591. [PubMed]
53. Hornung, O.P.; Regen, F.; Danker-Hopfe, H.; Schredl, M.; Heuser, I. The relationship between REM sleep and memory consolidation in old age and effects of cholinergic medication. Biol. Psychiatry 2007, 61, 750-757. [CrossRef] [PubMed]
54. Datta, S. PGO Wave Generation: Mechanisms and functional significance. In Rapid Eye Movement Sleep ; Mallick, B.N., Inoue, S., Eds.; Narosa Publishing House: New Delhi, India, 1999; pp. 91-106.
55. Datta, S. Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci. 2000, 20, 8607-8613. [PubMed]
56. Mavanji, V.; Datta, S. Activation of the phasic pontine-wave generator enhances improvement of learning performance: A mechanism for sleep-dependent plasticity. Eur. J. Neurosci. 2003, 17, 359-370. [CrossRef] [PubMed]
57. Datta, S.; Mavanji, V.; Ulloor, J.; Patterson, E.H. Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci. 2004, 24, 1416-1427. [CrossRef] [PubMed]
58. Peigneux, P.; Laureys, S.; Fuchs, S.; Delbeuck, X.; Degueldre, C.; Aerts, J.; Delfiore, G.; Luxen, A.; Maquet, P. Generation of rapid eye movements during paradoxical sleep in humans. Neuroimage 2001, 14, 701-708. [CrossRef] [PubMed]
59. Lim, A.S.; Lozano, A.M.; Moro, E.; Hamani, C.; Hutchison,W.D.; Dostrovsky, J.O.; Lang, A.E.;Wennberg, R.A.; Murray, B.J. Characterization of REM-sleep associated ponto-geniculo-occipital waves in the human pons. Sleep 2007, 30, 823-827. [PubMed]
60. Ioannides, A.A.; Corsi-Cabrera, M.; Fenwick, P.B.; del Rio Portilla, Y.; Laskaris, N.A.; Khurshudyan, A.; Theofilou, D.; Shibata, T.; Uchida, S.; Nakabayashi, T.; et al. MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades. Cereb. Cortex 2004, 14, 56-72. [CrossRef] [PubMed]
61. Ramirez-Salado, I.; Cruz-Aguilar, M.A. The origin and functions of dreams based on PGO activity. Salud Ment. 2014, 37, 49-58.
62. Van der Helm, E.; Walker, M.P. Overnight therapy? The role of sleep in emotional brain processing. Psychol. Bull. 2009, 135, 731-748.
63. Talbot, L.S.; Hairston, I.S.; Eidelman, P.; Gruber, J.; Harvey, A.G. The effect of mood on sleep onset latency and REM sleep in interepisode bipolar disorder. J. Abnorm. Psychol. 2009, 118, 448-458. [CrossRef] [PubMed]
64. Gujar, N.; McDonald, S.A.; Nishida, M.; Walker, M.P. A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb. Cortex 2011, 21, 1115-1123. [CrossRef] [PubMed]
65. Deliens, G.; Peigneux, P. One night of sleep is insufficient to achieve sleep-to-forget emotional decontextualisation processes. Cogn. Emot. 2014, 28, 698-706. [CrossRef] [PubMed]