Review Article | Published:

The memory function of sleep

Nature Reviews Neuroscience volume 11, pages 114126 (2010) | Download Citation

Abstract

Sleep has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and the timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations. Through specific patterns of neuromodulatory activity and electric field potential oscillations, slow-wave sleep (SWS) and rapid eye movement (REM) sleep support system consolidation and synaptic consolidation, respectively. During SWS, slow oscillations, spindles and ripples — at minimum cholinergic activity — coordinate the re-activation and redistribution of hippocampus-dependent memories to neocortical sites, whereas during REM sleep, local increases in plasticity-related immediate-early gene activity — at high cholinergic and theta activity — might favour the subsequent synaptic consolidation of memories in the cortex.

Key points

  • Sleep promotes the consolidation of declarative as well as procedural and emotional memories in a wide variety of tasks. Sleep improves preferentially the consolidation of memories that were encoded explicitly and are behaviourally relevant to the individual.

  • Consolidation during sleep not only strengthens memory traces quantitatively but can also produce qualitative changes in memory representations. An active process of re-organization enables the formation of new associations and the extraction of generalized features. This can ease novel inferences and insights.

  • Spatio-temporal patterns of neuronal activity during encoding in the awake state become re-activated during subsequent sleep, specifically during slow-wave sleep (SWS) which is a state of minimum cholinergic activity. Such re-activations might promote the gradual redistribution of hippocampus-dependent memories from the hippocampus to neocortical sites for long-term storage (system consolidation) and might also trigger enduring synaptic changes to stabilize memories (synaptic consolidation).

  • Neocortical (<1 Hz) slow oscillations, thalamo-cortical spindles and hippocampal sharp-wave ripples are implicated in memory consolidation during SWS. The depolarizing up-states of the slow oscillations synchronously drive the generation of spindles and ripples accompanying hippocampal memory re-activations, thus providing a temporal frame for a fine-tuned hippocampus-to-neocortex transfer of memories.

  • Neocortical slow oscillations concurrently support a global synaptic downscaling that precludes saturation of synaptic networks and improves the capacity to encode new information.

  • Rapid eye movement (REM) sleep is characterized by a local upregulation of plasticity-related immediate early genes in the presence of high cholinergic activity and reduced electroencephalographic coherence between brain regions. These conditions might effectively support local synaptic consolidation.

  • The temporal sequence of SWS and REM sleep in the normal sleep cycle suggests that these sleep stages have complementary roles in memory consolidation: during SWS, system consolidation promotes the re-activation and redistribution of select memory traces for long-term storage, whereas ensuing REM sleep might act to stabilize the transformed memories by enabling undisturbed synaptic consolidation.

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References

  1. 1.

    Sleep viewed as a state of adaptive inactivity. Nature Rev. Neurosci. 10, 747–753 (2009).

  2. 2.

    , & Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419–457 (1995).

  3. 3.

    & Obliviscence during sleep and waking. Am. J. Psychol. 35, 605–612 (1924).

  4. 4.

    Sleep-dependent memory consolidation. Nature 437, 1272–1278 (2005).

  5. 5.

    , & Sleep to remember. Neuroscientist 12, 410–424 (2006).

  6. 6.

    The role of sleep in learning and memory. Science 294, 1048–1052 (2001).

  7. 7.

    & Maintaining memories by reactivation. Curr. Opin. Neurobiol. 17, 698–703 (2007).

  8. 8.

    & The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 11, 442–450 (2007).

  9. 9.

    , & Current concepts in procedural consolidation. Nature Rev. Neurosci. 5, 576–582 (2004).

  10. 10.

    Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med. Rev. 5, 491–506 (2001).

  11. 11.

    & The function of dream sleep. Nature 304, 111–114 (1983).

  12. 12.

    & Effect of sleep on memory. 3. Controlling for time-of-day effects. J. Exp. Psychol. 93, 321–327 (1972).

  13. 13.

    & Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997). The first paper to show that SWS preferentially consolidates declarative memories, whereas REM sleep primarily supports procedural memories.

  14. 14.

    et al. A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol. Learn. Mem. 86, 241–247 (2006).

  15. 15.

    , , & Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315, 1426–1429 (2007). Odours associated with the encoding of visuo-spatial memories were used as cues during post-learning SWS to re-activate the memories. The memory enhancement produced by this re-activation compellingly demonstrates a causal role of re-activations for sleep-dependent consolidation.

  16. 16.

    , , & An ultra short episode of sleep is sufficient to promote declarative memory performance. J. Sleep Res. 17, 3–10 (2008).

  17. 17.

    , , & Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987–11991 (2002).

  18. 18.

    et al. Sleep and the time course of motor skill learning. Learn. Mem. 10, 275–284 (2003).

  19. 19.

    et al. Daytime sleep condenses the time course of motor memory consolidation. Nature Neurosci. 10, 1206–1213 (2007).

  20. 20.

    , , & Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830–6834 (2002).

  21. 21.

    , , , & Visual discrimination task improvement: A multi-step process occurring during sleep. J. Cogn. Neurosci. 12, 246–254 (2000).

  22. 22.

    , & Visual discrimination learning requires sleep after training. Nature Neurosci. 3, 1237–1238 (2000).

  23. 23.

    , & Sleep-dependent learning: a nap is as good as a night. Nature Neurosci. 6, 697–698 (2003).

  24. 24.

    , , & Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616–620 (2003).

  25. 25.

    , & Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn. Mem. 8, 112–119 (2001).

  26. 26.

    , , & Sleep preferentially enhances memory for emotional components of scenes. Psychol. Sci. 19, 781–788 (2008).

  27. 27.

    , , & REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb. Cortex 19, 1158–1166 (2009).

  28. 28.

    , , & Brief sleep after learning keeps emotional memories alive for years. Biol. Psychiat. 60, 788–790 (2006).

  29. 29.

    , & The whats and whens of sleep-dependent memory consolidation. Sleep Med. Rev. 13, 309–321 (2009).

  30. 30.

    & Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE. 2, e341 (2007).

  31. 31.

    , , & Early sleep triggers memory for early visual discrimination skills. Nature Neurosci. 3, 1335–1339 (2000).

  32. 32.

    , & Sleep after learning aids memory recall. Learn. Mem. 13, 259–262 (2006).

  33. 33.

    , , & Sleep directly following learning benefits consolidation of spatial associative memory. Learn. Mem. 15, 233–237 (2008).

  34. 34.

    , & Awareness modifies the skill-learning benefits of sleep. Curr. Biol. 14, 208–212 (2004). By comparing effects of post-learning sleep on an implicitly and explicitly learned motor skill, this study showed that sleep preferentially benefits the consolidation of explicitly encoded memories.

  35. 35.

    , , & Sleep's function in the spontaneous recovery and consolidation of memories. J. Exp. Psychol. Gen. 136, 169–183 (2007).

  36. 36.

    , & Sleep-dependent learning and motor-skill complexity. Learn. Mem. 11, 705–713 (2004).

  37. 37.

    & Anticipated reward enhances offline learning during sleep. J. Exp. Psychol. Learn. Mem. Cogn. 35, 1586–1593 (2009).

  38. 38.

    The prefrontal cortex and cognitive control. Nature Rev. Neurosci. 1, 59–65 (2000).

  39. 39.

    , , & An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37, 1013–1025 (2003).

  40. 40.

    et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188–1191 (1998).

  41. 41.

    , , , & Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference. Curr. Biol. 16, 1290–1294 (2006).

  42. 42.

    , , , & Early boost and slow consolidation in motor skill learning. Learn. Mem. 13, 580–583 (2006).

  43. 43.

    , , , & Sleep does not enhance motor sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 34, 834–842 (2008).

  44. 44.

    The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 55, 235–269 (2004).

  45. 45.

    , & The role of sleep in declarative memory consolidation: passive, permissive, active or none? Curr. Opin. Neurobiol. 16, 716–722 (2006).

  46. 46.

    , , , & Sleep inspires insight. Nature 427, 352–355 (2004). An experimental demonstration that sleep promotes insight into a logical problem, which can be considered a behavioural proof that memory representations undergo qualitative changes during sleep.

  47. 47.

    , , , & Human relational memory requires time and sleep. Proc. Natl Acad. Sci. USA 104, 7723–7728 (2007).

  48. 48.

    , , & Implicit learning -- explicit knowing: a role for sleep in memory system interaction. J. Cogn. Neurosci. 18, 311–319 (2006).

  49. 49.

    From creation to consolidation: a novel framework for memory processing. PLoS Biol. 7, e19 (2009).

  50. 50.

    & Off-line processing: reciprocal interactions between declarative and procedural memories. J. Neurosci. 27, 10468–10475 (2007).

  51. 51.

    & REM sleep deprivation: the wrong paradigm leading to wrong conclusions. Behav. Brain Sci. 23, 912–913 (2000).

  52. 52.

    & The consolidation hypothesis for REM sleep function: stress and other confounding factors — a review. Biol. Psychol. 18, 165–184 (1984).

  53. 53.

    , , & Processing of learned information in paradoxical sleep: relevance for memory. Behav. Brain Res. 69, 125–135 (1995).

  54. 54.

    The REM sleep window and memory processing in Sleep and brain plasticity (eds. Maquet, P., Smith, C. & Stickgold, R.) 117–133 (Oxford University Press, New York, 2003).

  55. 55.

    Sleep states and memory processes. Behav. Brain Res. 69, 137–145 (1995).

  56. 56.

    , , & Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nature Neurosci. 12, 396–397 (2009).

  57. 57.

    & Time for the sleep community to take a critical look at the purported role of sleep in memory processing. Sleep 28, 1228–1229 (2005).

  58. 58.

    , , & Neuronal plasticity: A link between stress and mood disorders. Psychoneuroendocrinology(2009).

  59. 59.

    & Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36, 571–582 (1999).

  60. 60.

    , , & Local sleep and learning. Nature 430, 78–81 (2004). Using high-density EEG in humans the experiments reveal a local increase in slow wave activity (SWA) over motor cortical areas during sleep after learning a motor skill, which was correlated with the sleep-induced gain in skill. The experiments show that the homeostatic regulation of SWA is locally influenced by prior learning and suggest that this activity contributes to consolidation.

  61. 61.

    , & A role for non-rapid-eye-movement sleep homeostasis in perceptual learning. J. Neurosci. 28, 2766–2772 (2008).

  62. 62.

    , & Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav. Brain Res. 180, 48–61 (2007).

  63. 63.

    et al. Consolidation of strictly episodic memories mainly requires rapid eye movement sleep. Sleep 27, 395–401 (2004).

  64. 64.

    et al. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69, 157–166 (1995).

  65. 65.

    & What in sleep is for memory. Sleep Med. 5, 225–230 (2004).

  66. 66.

    & A role for stage 2 sleep in memory processing in Sleep and brain plasticity (eds. Maquet, P., Smith, C. & Stickgold, R.) 87–98 (Oxford University Press, New York, 2003).

  67. 67.

    Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci. 20, 8607–8613 (2000).

  68. 68.

    The organization of behavior: A neuropsychological theory. (John Wiley & Sons, New York, 1949).

  69. 69.

    & Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J. Neurosci. 9, 2907–2918 (1989).

  70. 70.

    & Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994). A pioneering study revealing that in rats spatial–temporal patterns of neuronal firing in the hippocampus during learning are re-activated in the same order during subsequent SWS.

  71. 71.

    , , , & Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).

  72. 72.

    & Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neurosci. 10, 100–107 (2007). The first study to report that neuronal ensembles in the hippocampus and neocortex become re-activated in parallel during SWS in temporal frames corresponding to the slow oscillation.

  73. 73.

    , & Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318, 1147–1150 (2007).

  74. 74.

    et al. Preferential reactivation of motivationally relevant information in the ventral striatum. J. Neurosci. 28, 6372–6382 (2008).

  75. 75.

    , & Methodological considerations on the use of template matching to study long-lasting memory trace replay. J. Neurosci. 26, 10727–10742 (2006).

  76. 76.

    & Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).

  77. 77.

    , , & Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855, 176–180 (2000).

  78. 78.

    et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2, e24 (2004).

  79. 79.

    & Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

  80. 80.

    et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535–545 (2004).

  81. 81.

    et al. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neurosci. 3, 831–836 (2000).

  82. 82.

    et al. Sleep transforms the cerebral trace of declarative memories. Proc. Natl Acad. Sci. USA 104, 18778–18783 (2007). Using functional brain imaging the authors show that sleep leads to a redistribution of memory traces from the hippocampus to neocortical sites for long-term storage.

  83. 83.

    et al. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc. Natl Acad. Sci. USA 103, 756–761 (2006).

  84. 84.

    The neurobiology of consolidations, or, how stable is the engram? Annu. Rev. Psychol. 55, 51–86 (2004).

  85. 85.

    & The organization of recent and remote memories. Nature Rev. Neurosci. 6, 119–130 (2005).

  86. 86.

    & Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res. 493, 74–86 (1989).

  87. 87.

    & Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 25, 9398–9405 (2005).

  88. 88.

    , , & Hebbian modification of a hippocampal population pattern in the rat. J. Physiol. 521, 159–167 (1999).

  89. 89.

    , & Cellular mechanisms of burst firing-mediated long-term depression in rat neocortical pyramidal cells. J. Physiol. 578, 471–479 (2007).

  90. 90.

    & Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur. J. Neurosci. 20, 3453–3462 (2004).

  91. 91.

    et al. A local signature of LTP- and LTD-like plasticity in human NREM sleep. Eur. J. Neurosci. 27, 2241–2249 (2008).

  92. 92.

    , , , & Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neurosci. 11, 200–208 (2008). The authors demonstrate that physiological markers of synaptic strength increase during waking and decrease during sleep. The results provide strong evidence for global synaptic downscaling during sleep.

  93. 93.

    & Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J. Neurosci. 20, 9187–9194 (2000).

  94. 94.

    , , , & Long-term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states. J. Neurosci. 29, 620–629 (2009).

  95. 95.

    , & Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41, 35–43 (2004).

  96. 96.

    , , & Brain gene expression during REM sleep depends on prior waking experience. Learn. Mem. 6, 500–508 (1999).

  97. 97.

    et al. Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J. Neurosci. 22, 10914–10923 (2002). An important study showing that hippocampal activity during waking produces an increase in plasticity-related IEG expression in specific cortical areas during subsequent REM sleep, supporting a role of REM sleep in synaptic consolidation.

  98. 98.

    et al. Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front. Neurosci. 1, 43–55 (2007).

  99. 99.

    , & Blockade of postsynaptic activity in sleep inhibits developmental plasticity in visual cortex. Neuroreport 17, 1459–1463 (2006).

  100. 100.

    , & Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275–287 (2001).

  101. 101.

    et al. Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61, 454–466 (2009).

  102. 102.

    , , & Visual-procedural memory consolidation during sleep blocked by glutamatergic receptor antagonists. J. Neurosci. 28, 5513–5518 (2008).

  103. 103.

    & Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004).

  104. 104.

    Rhythms of the brain (Oxford University Press, New York, 2006).

  105. 105.

    , , & Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl Acad. Sci. USA 100, 2065–2069 (2003). First study in rats and mice that demonstrated a temporally fine-tuned relationship between slow oscillations, spindles and sharp-wave ripples possibly underlying the transfer of information between the hippocampus and neocortical regions.

  106. 106.

    & Interaction between neocortical and hippocampal networks via slow oscillations. Thalamus. Relat Syst. 3, 245–259 (2005).

  107. 107.

    , , & Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc. Natl Acad. Sci. USA 101, 13963–13968 (2004).

  108. 108.

    , , , & The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci. 29, 1071–1081 (2009).

  109. 109.

    et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nature Neurosci. 9, 1169–1176 (2006).

  110. 110.

    et al. TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS ONE. 2, e276 (2007).

  111. 111.

    et al. Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J. Neurosci. 28, 7911–7918 (2008).

  112. 112.

    , , & Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006). By applying electrical stimulation (at the slow oscillation frequency) to healthy humans the authors induced slow oscillation activity during non-REM sleep and improved the retention of memories in humans. These findings provide first evidence for a causal contribution of slow oscillations to sleep-dependent memory consolidation.

  113. 113.

    , & Induction of long-term potentiation leads to increased reliability of evoked neocortical spindles in vivo. Neuroscience 131, 793–800 (2005).

  114. 114.

    et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479–1485 (2004).

  115. 115.

    & Learning-dependent changes in sleep spindles and Stage 2 sleep. J. Sleep Res. 15, 250–255 (2006).

  116. 116.

    , , & Elevated sleep spindle density after learning or after retrieval in rats. J. Neurosci. 26, 12914–12920 (2006).

  117. 117.

    et al. Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J. Neurosci. 26, 8976–8982 (2006).

  118. 118.

    et al. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 31, 1149–1156 (2008).

  119. 119.

    , & Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529–535 (2005).

  120. 120.

    , & Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 403, 52–56 (2006).

  121. 121.

    Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31, 551–570 (1989).

  122. 122.

    , , , & Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nature Neurosci. 12, 919–926 (2009).

  123. 123.

    , , , & Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nature Neurosci. 8, 1560–1567 (2005).

  124. 124.

    , & Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res. 435, 331–333 (1987).

  125. 125.

    , , & Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585–594 (2000).

  126. 126.

    , , , & Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn. Mem. 15, 222–228 (2008).

  127. 127.

    , & Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131, 1806–1817 (2008).

  128. 128.

    , , , & Selective suppression of hippocampal ripples impairs spatial memory. Nature Neurosci. 12, 1222–1223 (2009). The authors showed that the suppression of hippocampal ripples by electrical pulses during post-learning rest in rats impaired the consolidation of a hippocampus-dependent spatial task. These experiments provide direct evidence for an involvement of hippocampal sharp-wave ripples in the off-line consolidation of memory.

  129. 129.

    et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52, 871–882 (2006).

  130. 130.

    , , & Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 22, 10941–10947 (2002).

  131. 131.

    , , , & Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol. 96, 62–70 (2006).

  132. 132.

    Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087–1106 (2006).

  133. 133.

    , , , & Slow oscillations as a probe of the dynamics of the locus coeruleus-frontal cortex interaction in anesthetized rats. J. Physiol. Paris 91, 273–284 (1997).

  134. 134.

    & Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation? Cereb. Cortex 18, 2596–2603 (2008).

  135. 135.

    & Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123–1128 (1998).

  136. 136.

    , , & State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61, 587–596 (2009).

  137. 137.

    Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res. 7 (Suppl 1), 17–23 (1998).

  138. 138.

    & Hippocampus whispering in deep sleep to prefrontal cortex — for good memories? Neuron 61, 496–498 (2009).

  139. 139.

    & Spatio-temporal activation of cyclic AMP response element-binding protein, activity-regulated cytoskeletal-associated protein and brain-derived nerve growth factor: a mechanism for pontine-wave generator activation-dependent two-way active-avoidance memory processing in the rat. J. Neurochem. 95, 418–428 (2005).

  140. 140.

    , & Activation of phasic pontine-wave generator in the rat: a mechanism for expression of plasticity-related genes and proteins in the dorsal hippocampus and amygdala. Eur. J. Neurosci. 27, 1876–1892 (2008).

  141. 141.

    Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).

  142. 142.

    , & Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J. Neurosci. 17, 6470–6477 (1997).

  143. 143.

    & Fear conditioning increases NREM sleep. Behav. Neurosci. 121, 310–323 (2007).

  144. 144.

    , , & Enhancement of neocortical-medial temporal EEG correlations during non-REM sleep. Neural Plast. 2008, e563028 (2008).

  145. 145.

    et al. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23, 10897–10903 (2003).

  146. 146.

    , & Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J. Neurosci. 28, 6731–6741 (2008).

  147. 147.

    & Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49–62 (2006).

  148. 148.

    & Long-term depression: a cascade of induction and expression mechanisms. Prog. Neurobiol. 65, 339–365 (2001).

  149. 149.

    , , , & Motor memory consolidation in sleep shapes more effective neuronal representations. J. Neurosci. 25, 11248–11255 (2005).

  150. 150.

    et al. Sleep after spatial learning promotes covert reorganization of brain activity. Proc. Natl Acad. Sci. USA 103, 7124–7129 (2006).

  151. 151.

    et al. Sleep benefits subsequent hippocampal functioning. Nature Neurosci. 12, 122–123 (2009).

  152. 152.

    Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262, 23–81 (1971).

  153. 153.

    & Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc. Natl Acad. Sci. USA 101, 2140–2144 (2004).

  154. 154.

    Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351–359 (1999).

  155. 155.

    & High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog. Brain Res. 145, 207–231 (2004).

  156. 156.

    , , , & Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 7, e1000173 (2009).

  157. 157.

    & Why do we sleep? Brain Res. 886, 208–223 (2000).

  158. 158.

    et al. Sleep promotes the neural reorganization of remote emotional memory. J. Neurosci. 29, 5143–5152 (2009).

  159. 159.

    et al. Source modeling sleep slow waves. Proc. Natl Acad. Sci. USA 106, 1608–1613 (2009).

  160. 160.

    , , , & The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862–6870 (2004).

  161. 161.

    et al. Muscarinic acetylcholine receptors activate expression of the EGR gene family of transcription factors. J. Biol. Chem. 273, 14538–14544 (1998).

  162. 162.

    , , , & Muscarinic acetylcholine receptor stimulation induces expression of the activity-regulated cytoskeleton-associated gene (ARC). Brain Res. Mol. Brain Res. 121, 131–136 (2004).

  163. 163.

    et al. Muscarinic acetylcholine neurotransmission enhances the late-phase of long-term potentiation in the hippocampal-prefrontal cortex pathway of rats in vivo: a possible involvement of monoaminergic systems. Neuroscience 153, 1309–1319 (2008).

  164. 164.

    & Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81, 213–222 (1997).

  165. 165.

    , , & Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci. 30, 334–342 (2007).

  166. 166.

    , , , & Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl Acad. Sci. USA 104, 347–352 (2007).

  167. 167.

    , , & Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22, 8691–8704 (2002).

  168. 168.

    & Mechanisms and biological role of thalamocortical oscillations in Trends in Chronobiology Research (ed. Columbus, F.) 1–47 (Nova Science Publishers, Inc, 2005).

  169. 169.

    & Sleep spindles: an overview. Sleep Med. Rev. 7, 423–440 (2003).

  170. 170.

    & Awake replay of remote experiences in the hippocampus. Nature Neurosci. 12, 913–918 (2009).

  171. 171.

    & The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nature Rev. Neurosci. 3, 591–605 (2002).

  172. 172.

    , & Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J. Cogn. Neurosci. 18, 793–802 (2006).

  173. 173.

    , , & Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269–301 (1998).

  174. 174.

    & Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation. Stress 11, 28–41 (2008).

  175. 175.

    , & Post-training intra-striatal scopolamine or flupenthixol impairs radial maze learning in rats. Behav. Brain Res. 170, 148–155 (2006).

  176. 176.

    , & Impaired off-line consolidation of motor memories after combined blockade of cholinergic receptors during REM sleep-rich sleep. Neuropsychopharmacology 34, 1843–1853 (2009).

  177. 177.

    , , , & The relationship between REM sleep and memory consolidation in old age and effects of cholinergic medication. Biol. Psychiatry 61, 750–757 (2007).

  178. 178.

    The role of sleep in cognition and emotion. Ann. N. Y. Acad. Sci. 1156, 168–197 (2009).

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Acknowledgements

We apologize to those whose work was not cited because of space constraints. We thank Drs. B. Rasch, L. Marshall, I. Wilhelm, M. Hallschmid, E. Robertson and S. Ribeiro for helpful discussions and comments on earlier drafts. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (SFB 654 'Plasticity and Sleep').

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  1. University of Lübeck, Department of Neuroendocrinology, Haus 50, 2. OG, Ratzeburger Allee 160, 23538 Lübeck, Germany.

    • Susanne Diekelmann
    •  & Jan Born

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jan Born.

Glossary

Declarative memory

Memories that are accessible to conscious recollection including memories for facts and episodes, for example, learning vocabulary or remembering events. Declarative memories rely on the hippocampus and associated medial temporal lobe structures, together with neocortical regions for long-term storage.

Procedural memory

Memories for skills that result from repeated practice and are not necessarily available for conscious recollection, for example, riding a bike or playing the piano. Procedural memories rely on the striatum and cerebellum, although recent studies indicate that the hippocampus can also be implicated in procedural learning.

Serial reaction time task

A task in which subjects are required to rapidly respond to different spatial cues by pressing corresponding buttons. This task can be performed implicitly (that is, without knowledge that there is a regularity underlying the sequence of cue positions) or explicitly (by informing the subject about this underlying regularity).

Implicit learning

Learning without being aware that something is being learned.

Explicit learning

Learning while being aware that something is being learned.

Memory systems

Different types of memory, such as declarative and non-declarative memory, are thought to be mediated by distinct neural systems, the organization of which is still a topic of debate.

Transitory sleep

Short transitory periods of sleep in rats that, based on EEG criteria, can neither be classified as REM sleep or SWS.

Immediate early genes

Genes that encode transcription factors that are induced within minutes of raised neuronal activity without requiring a protein signal. Immediate-early gene activation is, therefore, used as an indirect marker of neuronal activation. The immediate early genes Arc and Egr1 (zif268) are associated with synaptic plasticity.

Hebbian plasticity

Refers to the functional changes at synapses that increase the efficacy of synaptic transmission and occurs when the presynaptic neuron repeatedly and persistently stimulates the postsynaptic neuron.

Spike-time dependent plasticity

Refers to the functional changes at synapses that alter the efficacy of synaptic transmission depending on the relative timing of pre- and postsynaptic firing ('spiking'). The synaptic connection is strengthened if the presynaptic neuron fires shortly before the postsynaptic neuron, but is weakened if the sequence of firing is reversed.

Up- and down-states

The slow oscillations that predominate EEG activity during SWS are characterized by alternating states of neuronal silence with an absence of spiking activity and membrane hyperpolarization in all cortical neurons ('down-state') and strongly increased wake-like firing of large neuronal populations and membrane depolarization ('up-state').

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DOI

https://doi.org/10.1038/nrn2762