Advertisement

Differential Effects of Non-REM and REM Sleep on Memory Consolidation?

  • Sandra Ackermann
  • Björn RaschEmail author
Sleep (M Thorpy, M Billiard, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Sleep

Abstract

Sleep benefits memory consolidation. Previous theoretical accounts have proposed a differential role of slow-wave sleep (SWS), rapid-eye-movement (REM) sleep, and stage N2 sleep for different types of memories. For example the dual process hypothesis proposes that SWS is beneficial for declarative memories, whereas REM sleep is important for consolidation of non-declarative, procedural and emotional memories. In fact, numerous recent studies do provide further support for the crucial role of SWS (or non-REM sleep) in declarative memory consolidation. However, recent evidence for the benefit of REM sleep for non-declarative memories is rather scarce. In contrast, several recent studies have related consolidation of procedural memories (and some also emotional memories) to SWS (or non-REM sleep)-dependent consolidation processes. We will review this recent evidence, and propose future research questions to advance our understanding of the role of different sleep stages for memory consolidation.

Keywords

Slow wave sleep Rapid eye movement sleep Declarative memory Non-declarative memory Emotional memory Procedural memory Memory consolidation Reactivation 

Notes

Acknowledgments

This work was supported by grants from the Swiss National Foundation (SNF) (PP00P1_133685) and the University of Zürich (Clinical Research Priority Programm "Sleep and Health").

Compliance with Ethics Guidelines

Conflict of Interest

Sandra Ackermann received a grant from the University of Zurich Clinical research priority project “Sleep and Health”.

Björn Rasch received grants from the Swiss National Science Foundation (PP00P1_133685) and from the University of Zurich Clinical research priority project “Sleep and Health”.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.••
    Rasch B, Born J. About sleep’s role in memory. Physiol Rev. 2013;93:681–766. A comprehensive review on the curent status of sleep and memory research.Google Scholar
  2. 2.
    Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11:114–26.PubMedCrossRefGoogle Scholar
  3. 3.
    Marshall L, Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci. 2007;11:442–50.PubMedCrossRefGoogle Scholar
  4. 4.
    Born J, Wilhelm I. System consolidation of memory during sleep. Psychol Res. 2012;76:192–203.PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Mölle M, Marshall L, Gais S, Born J. Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc Natl Acad Sci U S A. 2004;101:13963–8.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Menicucci D, Piarulli A, Debarnot U, d’Ascanio P, Landi A, Gemignani A. Functional structure of spontaneous sleep slow oscillation activity in humans. PLoS One. 2009;4:e7601.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Mölle M, Born J. Slow oscillations orchestrating fast oscillations and memory consolidation. Prog Brain Res. 2011;193:93–110.PubMedCrossRefGoogle Scholar
  8. 8.
    Cantero JL, Atienza M, Stickgold R, Kahana MJ, Madsen JR, Kocsis B. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J Neurosci. 2003;23:10897–903.PubMedGoogle Scholar
  9. 9.
    Buzsáki G. Theta oscillations in the hippocampus. Neuron. 2002;33:325–40.PubMedCrossRefGoogle Scholar
  10. 10.
    Smith CT. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev. 2001;5:491–506.PubMedCrossRefGoogle Scholar
  11. 11.
    Plihal W, Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci. 1997;9:534–47.PubMedCrossRefGoogle Scholar
  12. 12.
    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;8:112–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Squire LR. Memory systems of the brain: A brief history and current perspective. Neurobiol Learn Mem. 2004;82:171–7.PubMedCrossRefGoogle Scholar
  14. 14.
    Rauchs G, Desgranges B, Foret J, Eustache F. The relationships between memory systems and sleep stages. J Sleep Res. 2005;14:123–40.PubMedCrossRefGoogle Scholar
  15. 15.
    Walker MP, Stickgold R. Sleep-dependent learning and memory consolidation. Neuron. 2004;44:121–33.PubMedCrossRefGoogle Scholar
  16. 16.
    Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10:49–62.PubMedCrossRefGoogle Scholar
  17. 17.
    Oudiette D, Paller K A. Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn Sci. 2013;1–8.Google Scholar
  18. 18.
    Rasch B, Buchel C, Gais S, Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007;315:1426–9.PubMedCrossRefGoogle Scholar
  19. 19.••
    Rudoy JD, Voss JL, Westerberg CE, Paller KA. Strengthening individual memories by reactivating them during sleep. Science. 2009;326:1079. The authors show that reactivation can selectively enhance memory consolidation. Spatial locations of items in an object-location task that are cued (sound) during a post-learning nap are less often forgotten than locations of uncued items.Google Scholar
  20. 20.••
    Schönauer M, Geisler T, Gais S. Strengthening procedural memories by reactivation in sleep. J Cogn Neurosci. 2013;1–11. The study shows that auditory reactivation during early sleep strenghtens procedural memory consolidation (finger-tapping task) during sleep, but not during wakefulness. The benefit is selective for cued sequences. Google Scholar
  21. 21.••
    Antony JW, Gobel EW, O’Hare JK, Reber PJ, Paller KA. Cued memory reactivation during sleep influences skill learning. Nat Neurosci. 2012;15:1114–6. Auditory reactivation of procedural memory during SWS of an afternoon nap improved accuracy in after sleep memory performance showing a role of SWS for consolidation of procedural memory.Google Scholar
  22. 22.••
    Hauner KK, Howard JD, Zelano C, Gottfried JA. Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat Neurosci. 2013;16:1553–5. The authors show that in humans, memories that are reactivated during SWS elicit a smaller fear response when cues are again presented during wake (smaller skin conductance response). This study is in contrast with a recent study in mice showing that consolidation of fear memories during sleep is strengthened [97].PubMedCrossRefGoogle Scholar
  23. 23.
    Gais S, Born J. Declarative memory consolidation: mechanisms acting during human sleep. Learn Mem. 2004;11:679–85.PubMedCrossRefGoogle Scholar
  24. 24.
    Yaroush R, Sullivan MJ, Ekstrand BR. Effect of sleep on memory. II. Differential effect of the first and second half of the night. J Exp Psychol. 1971;88:361–6.PubMedCrossRefGoogle Scholar
  25. 25.
    Fowler MJ, Sullivan MJ, Ekstrand BR. Sleep and memory. Science. 1973;179.Google Scholar
  26. 26.
    Barrett TR, Ekstrand BR. Effect of sleep on memory: III. Controlling for time-of-day effects. J Exp Psychol. 1972;96:321–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Plihal W, Born J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology. 1999;36:571–82.PubMedCrossRefGoogle Scholar
  28. 28.
    Verleger R, Schuknecht S-V, Jaśkowski P, Wagner U. Changes in processing of masked stimuli across early- and late-night sleep: a study on behavior and brain potentials. Brain Cogn. 2008;68:180–92.PubMedCrossRefGoogle Scholar
  29. 29.
    Wagner U, Hallschmid M, Verleger R, Born J. Signs of REM sleep dependent enhancement of implicit face memory: a repetition priming study. Biol Psychol. 2002;62.Google Scholar
  30. 30.
    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;64:627–34.PubMedCrossRefGoogle Scholar
  31. 31.
    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.PubMedCrossRefGoogle Scholar
  32. 32.
    Smith CT, MacNeill C. Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students. J Sleep Res. 1994;3:206–13.PubMedCrossRefGoogle Scholar
  33. 33.
    Smith CT. Sleep states, memory processes and synaptic plasticity. Behav Brain Res. 1996;78:49–56.PubMedCrossRefGoogle Scholar
  34. 34.
    Smith CT. Sleep states and memory processes. Behav Brain Res. 1995;69:137–45.PubMedCrossRefGoogle Scholar
  35. 35.
    Alger SE, Lau H, Fishbein W. Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention. Neurobiol Learn Mem. 2012;98:188–96.PubMedCrossRefGoogle Scholar
  36. 36.••
    Diekelmann S, Biggel S, Rasch B, Born J. Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations. Neurobiol Learn Mem. 2012;98:103–11. This study shows that reactivation can boost the beneficial effect of sleep on memory consolidation. While a 40-min nap without reactivation does not benefit memory as compared to wakefulness, a nap of 40 minutes with reactivation led to the same consolidation benefit as a 90-min nap without reactivation. External reactivation leads to faster consolidation and may compensate for less SWS.Google Scholar
  37. 37.
    Alger SE, Lau H, Fishbein W. Delayed onset of a daytime nap facilitates retention of declarative memory. PLoS One. 2010;5:e12131.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Mander BA, Rao V, Lu B, Saletin JM, Lindquist JR, Ancoli-Israel S, et al. Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat Neurosci. 2013;1–10.Google Scholar
  39. 39.
    Scullin MK. Sleep, memory, and aging: the link between slow-wave sleep and episodic memory changes from younger to older adults. Psychol Aging. 2013;28:105–14.PubMedCrossRefGoogle Scholar
  40. 40.
    Piosczyk H, Holz J, Feige B, Spiegelhalder K, Weber F, Landmann N, et al. The effect of sleep-specific brain activity versus reduced stimulus interference on declarative memory consolidation. J Sleep Res. 2013;22:406–13.PubMedCrossRefGoogle Scholar
  41. 41.
    Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci. 2010;30:14356–60.PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Tamminen J, Lambon Ralph MA, Lewis PA. The role of sleep spindles and slow-wave activity in integrating new information in semantic memory. J Neurosci. 2013;33:15376–81.PubMedCrossRefGoogle Scholar
  43. 43.
    Kurdziel L, Duclos K, Spencer RMC. Sleep spindles in midday naps enhance learning in preschool children. Proc Natl Acad Sci U S A. 2013;110:17627–72.CrossRefGoogle Scholar
  44. 44.
    Marshall L, Helgadottir H, Mölle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444:610–3.PubMedCrossRefGoogle Scholar
  45. 45.
    Eggert T, Dorn H, Sauter C, Nitsche MA, Bajbouj M, Danker-Hopfe H. No effects of slow oscillatory transcranial direct current stimulation (tDCS) on sleep-dependent memory consolidation in healthy elderly subjects. Brain Stimul. 2013;6:938–45.PubMedCrossRefGoogle Scholar
  46. 46.
    Marshall L, Kirov R, Brade J, Mölle M, Born J. Transcranial electrical currents to probe EEG brain rhythms and memory consolidation during sleep in humans. PLoS One. 2011;6:e16905.PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Antonenko D, Diekelmann S, Olsen C, Born J, Mölle M. Napping to renew learning capacity: enhanced encoding after stimulation of sleep slow oscillations. Eur J Neurosci. 2013;37:1142–51.PubMedCrossRefGoogle Scholar
  48. 48.
    Van Der Werf YD, Altena E, Schoonheim MM, Sanz-Arigita EJ, Vis JC, De Rijke W, et al. Sleep benefits subsequent hippocampal functioning. Nat Neurosci. 2009;12:122–3.CrossRefGoogle Scholar
  49. 49.
    Van Der Werf YD, Altena E, Vis JC, Koene T, Van Someren EJW. Reduction of nocturnal slow-wave activity affects daytime vigilance lapses and memory encoding but not reaction time or implicit learning. Prog Brain Res. 2011;193:245–55.CrossRefGoogle Scholar
  50. 50.
    Ngo H-VV, Martinetz T, Born J, Mölle M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron. 2013;78:545–53.PubMedCrossRefGoogle Scholar
  51. 51.
    O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010;33:220–9.PubMedCrossRefGoogle Scholar
  52. 52.••
    Fuentemilla L, Miró J, Ripollés P, Vilà-Balló A, Juncadella M, Castañer S, et al. Hippocampus-dependent strengthening of targeted memories via reactivation during sleep in humans. Curr Biol. 2013;23:1769–75. This study shows that hippocampal activity is crucial for beneficial effects of reactivation on memory consolidation.The authors compared effects of external reactivation cues (sounds) during SWS on memory consolidation in healthy individuals and epileptic patients with unilateral and bilateral hippocampal sclerosis. External reactivation during sleep only benefited memory in healthy individuals and epileptic patients with unilateral hippocampal sclerosis.Google Scholar
  53. 53.
    Oudiette D, Antony JW, Creery JD, Paller KA. The role of memory reactivation during wakefulness and sleep in determining which memories endure. J Neurosci. 2013;33:6672–8.PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.••
    Diekelmann S, Büchel C, Born J, Rasch B. Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci. 2011;14:381–6. The authors investigated differential effects of reactivation during waking and sleep. Interestingly, reactivation of memory during wake leads to destabilization of memory while reactivation of memory during sleep leads to stabilization of memory. Morevoer, REM sleep does not seem to be necessary for stabilization of memory, as also reactivation during a period of SWS sleep not containing REM sleep leads to stabilization of memory.Google Scholar
  55. 55.
    Lüthi A. Sleep spindles: where they come from, what they do. Neuroscientist. 2013 Aug 27 [Epub ahead of print].Google Scholar
  56. 56.
    Cox R, Hofman WF, Talamini LM. Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem. 2012;19:264–7.PubMedCrossRefGoogle Scholar
  57. 57.
    Ruch S, Markes O, Duss SB, Oppliger D, Reber TP, Koenig T, et al. Sleep stage II contributes to the consolidation of declarative memories. Neuropsychologia. 2012;50:2389–96.PubMedCrossRefGoogle Scholar
  58. 58.
    Mednick SC, McDevitt EA, Walsh JK, Wamsley E, Paulus M, Kanady JC, et al. The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J Neurosci. 2013;33:4494–504.PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Feld GB, Wilhelm I, Ma Y, Groch S, Binkofski F, Mölle M, et al. Slow wave sleep induced by GABA agonist tiagabine fails to benefit memory consolidation. Sleep. 2013;36:1317–26.PubMedGoogle Scholar
  60. 60.
    Albouy G, King BR, Maquet P, Doyon J. Hippocampus and striatum: Dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus. 2013;23:985–1004.PubMedCrossRefGoogle Scholar
  61. 61.
    Peigneux P, Laureys S, Delbeuck X, Maquet P. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport. 2001;12:A111–24.PubMedCrossRefGoogle Scholar
  62. 62.
    Fischer S, Hallschmid M, Elsner AL, Born J. Sleep forms memory for finger skills. Proc Natl Acad Sci U S A. 2002;99:11987–91.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Fischer S, Nitschke MF, Melchert UH, Erdmann C, Born J. Motor memory consolidation in sleep shapes more effective neuronal representations. J Neurosci. 2005;25:11248–55.PubMedCrossRefGoogle Scholar
  64. 64.
    Rasch B, Gais S, Born J. Impaired off-line consolidation of motor memories after combined blockade of cholinergic receptors during REM sleep-rich sleep. Neuropsychopharmacology. 2009;34:1843–53.PubMedCrossRefGoogle Scholar
  65. 65.
    Rasch B, Pommer J, Diekelmann S, Born J. Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci. 2009;12:396–7.PubMedCrossRefGoogle Scholar
  66. 66.
    Siegel JM. The REM, sleep-memory consolidation hypothesis. Science. 2001;294:1058–63.PubMedCrossRefGoogle Scholar
  67. 67.
    Vertes RP, Eastman KE. The case against memory consolidation in REM sleep. Behav Brain Sci. 2000;23:867–76.PubMedCrossRefGoogle Scholar
  68. 68.
    Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron. 2002;35:205–11.PubMedCrossRefGoogle Scholar
  69. 69.
    Nishida M, Walker MP. Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One. 2007;2:e341.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Fogel SM, Smith CT, Cote KA. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res. 2007;180:48–61.PubMedCrossRefGoogle Scholar
  71. 71.
    Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430:78–81.PubMedCrossRefGoogle Scholar
  72. 72.
    Huber R, Ghilardi MF, Massimini M, Ferrarelli F, Riedner BA, Peterson MJ, et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci. 2006;9:1169–76.PubMedCrossRefGoogle Scholar
  73. 73.
    Aeschbach D, Cutler AJ, Ronda JM. A role for non-rapid-eye-movement sleep homeostasis in perceptual learning. J Neurosci. 2008;28:2766–72.PubMedCrossRefGoogle Scholar
  74. 74.••
    Landsness EC, Crupi D, Hulse BK, Peterson MJ, Huber R, Ansari H, et al. Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep. 2009;32:1273–84. Acoustic suppression of slow wave activity diminished overnight improvement in a visuomotor learning task as compared to a control group. These results demonstrate the importance of slow wave activity for the formation of procedural memory.Google Scholar
  75. 75.
    Born J, Gais S. REM sleep deprivation: The wrong paradigm leading to wrong conclusions. Behav Brain Sci. 2000;23:912–3.CrossRefGoogle Scholar
  76. 76.
    Albouy G, Sterpenich V, Vandewalle G, Darsaud A, Gais S, Rauchs G, et al. Interaction between hippocampal and striatal systems predicts subsequent consolidation of motor sequence memory. PLoS One. 2013;8:e59490.PubMedCentralPubMedCrossRefGoogle Scholar
  77. 77.
    McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci. 2004;27:1–28.PubMedCrossRefGoogle Scholar
  78. 78.
    Hu P, Stylos-Allan M, Walker MP. Sleep facilitates consolidation of emotional declarative memory. Psychol Sci. 2006;17:891–8.PubMedCrossRefGoogle Scholar
  79. 79.
    Payne JD, Kensinger EA. Sleep’s role in the consolidation of emotional episodic memories. Curr Dir Psychol Sci. 2010;19:290–5.CrossRefGoogle Scholar
  80. 80.
    Wagner U, Hallschmid M, Rasch B, Born J. Brief sleep after learning keeps emotional memories alive for years. Biol Psychiatry. 2006;60:788–90.PubMedCrossRefGoogle Scholar
  81. 81.
    Hennevin E, Huetz C, Edeline J-M. Neural representations during sleep: from sensory processing to memory traces. Neurobiol Learn Mem. 2007;87:416–40.PubMedCrossRefGoogle Scholar
  82. 82.
    Freud S. The interpretation of dreams. 1900.Google Scholar
  83. 83.
    Hobson JA, Pace-Schott EF. The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat Rev Neurosci. 2002;3:679–93.PubMedCrossRefGoogle Scholar
  84. 84.
    Tsuno N, Besset A, Ritchie K. Sleep and depression. J Clin Psychiatry. 2005;66:1254–69.PubMedCrossRefGoogle Scholar
  85. 85.
    Walker MP. The role of sleep in cognition and emotion. Ann N Y Acad Sci. 2009;1156:168–97.PubMedCrossRefGoogle Scholar
  86. 86.••
    Walker MP, van der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychol Bull. 2009;135:731–48. An important review proposing that a role of sleep for emotional memory proessing is twofold: while the emotional context ist strengthened by sleep, the associated emotion of the memory is reduced.Google Scholar
  87. 87.
    Nishida M, Pearsall J, Buckner RL, Walker MP. REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex. 2009;19:1158–66.PubMedCrossRefGoogle Scholar
  88. 88.
    Menz MM, Rihm JS, Salari N, Born J, Kalisch R, Pape HCC, et al. The role of sleep and sleep deprivation in consolidating fear memories. Neuroimage. 2013;75:87–96.PubMedCrossRefGoogle Scholar
  89. 89.
    Van der Helm E, Yao J, Dutt S, Rao V, Saletin JM, Walker MP. REM sleep depotentiates amygdala activity to previous emotional experiences. Curr Biol. 2011;21:2029–32.PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Gujar N, McDonald SA, Nishida M, Walker MP. A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb Cortex. 2011;21:115–23.PubMedCrossRefGoogle Scholar
  91. 91.
    Baran B, Pace-Schott EF, Ericson C, Spencer RM. Processing of emotional reactivity and emotional memory over sleep. J Neurosci. 2012;32:1035–42.PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    Deliens G, Neu D, Peigneux P. Rapid eye movement sleep does not seem to unbind memories from their emotional context. J Sleep Res. 2013;36:1875–83.Google Scholar
  93. 93.
    Groch S, Wilhelm I, Diekelmann S, Sayk F, Gais S, Born J. Contribution of norepinephrine to emotional memory consolidation during sleep. Psychoneuroendocrinology. 2011;36:1342–50.PubMedCrossRefGoogle Scholar
  94. 94.
    Kaestner EJ, Wixted JT, Mednick SC. Pharmacologically increasing sleep spindles enhances recognition for negative and high-arousal memories. J Cogn Neurosci 2013;1597–610.Google Scholar
  95. 95.
    Hars B, Hennevin E. Impairment of learning by cueing during postlearning slow-wave sleep in rats. Neurosci Lett. 1987;79:290–4.PubMedCrossRefGoogle Scholar
  96. 96.
    Hennevin E, Hars B. Is increase in post-learning paradoxical sleep modified by cueing? Behav Brain Res. 1987;24:243–9.PubMedCrossRefGoogle Scholar
  97. 97.••
    Rolls A, Makam M, Kroeger D, Colas D, de Lecea L, Heller HC. Sleep to forget: interference of fear memories during sleep. Mol Psychiatry. 2013;18:1166–70. Reactivating fear memories during non-REM sleep in mice using an odor conditioning paradigm, leads to stronger consolidation of fear memories during sleep. This effect depends on protein synthesis in the basolateral amygdala. These results are in contrast with a study of fear consolidation during sleep in humans [21].Google Scholar
  98. 98.
    Stickgold R. Parsing the role of sleep in memory processing. Curr Opin Neurobiol. 2013;23:847–53.PubMedCrossRefGoogle Scholar
  99. 99.
    Ficca G, Salzarulo P. What in sleep is for memory. Sleep Med. 2004;5:225–30.PubMedCrossRefGoogle Scholar
  100. 100.
    Stickgold R, Walker MP. Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci. 2013;16:139–45.PubMedCrossRefGoogle Scholar
  101. 101.
    Rauchs G, Feyers D, Landeau B, Bastin C, Luxen A, Maquet P, et al. Sleep contributes to the strengthening of some memories over others, depending on hippocampal activity at learning. J Neurosci. 2011;31:2563–8.PubMedCentralPubMedCrossRefGoogle Scholar
  102. 102.
    Saletin JM, Goldstein AN, Walker MP. The role of sleep in directed forgetting and remembering of human memories. Cereb Cortex. 2011;21:2534–41.PubMedCrossRefGoogle Scholar
  103. 103.
    Wilhelm I, Diekelmann S, Molzow I, Ayoub A, Mo M, Born J. Sleep selectively enhances memory expected to be of future relevance. J Neurosci. 2011;31:1563–9.PubMedCrossRefGoogle Scholar
  104. 104.
    Diekelmann S, Wilhelm I, Wagner U, Born J. Sleep to implement an intention. Sleep. 2013;36:149–53.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Psychology, Division of BiopsychologyUniversity of ZurichZurichSwitzerland
  2. 2.Clinic of Affective Disorders and General PsychiatryPsychiatric University Hospital ZurichZurichSwitzerland
  3. 3.Division of Cognitive Biopsychology and Methods, Department of PsychologyUniversity of FribourgFribourgSwitzerland
  4. 4.Zurich Center of Integrative Sleep Research (ZiS)University of ZurichZurichSwitzerland

Personalised recommendations