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Offline memory consolidation during waking rest

Abstract

People spend approximately half of their waking hours in a so-called offline state — daydreaming, mind wandering or otherwise inattentive to their surroundings. These activities are often viewed as a waste of time, perhaps as moments of lost productivity. However, periods of offline waking rest can facilitate the consolidation of newly formed memories. Even a few minutes of rest with closed eyes can improve memory, perhaps to the same degree as a full night of sleep. These findings have profound implications for understanding the memory consolidation process, its time course and its underlying mechanisms. In this Review, I describe evidence that offline waking rest retroactively facilitates memory. Similar to the beneficial effect of sleep, the effect of rest might be driven by neural-level reactivation of newly formed memory traces. As both rest and sleep seem to support consolidation, I next consider whether these two states support the same or dissociable stages of consolidation. Then I review evidence that seconds-long bouts of offline rest occur throughout the day and that even these ultrashort offline periods might benefit memory. Finally, I conclude by describing future directions for research into the underlying processes of sleep and wake states.

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Fig. 1: The effect of offline waking rest on memory.
Fig. 2: Oscillations proposed to support consolidation.
Fig. 3: Potential mechanisms of memory consolidation in wake and sleep.
Fig. 4: Potential roles of sleep and offline waking rest in memory consolidation.
Fig. 5: Seconds-long offline states while performing a cognitive task.

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References

  1. Killingsworth, M. A. & Gilbert, D. T. A wandering mind is an unhappy mind. Science 330, 932 (2010).

    Article  PubMed  Google Scholar 

  2. McGaugh, J. L. Memory — a century of consolidation. Science 287, 248–251 (2000).

    Article  PubMed  Google Scholar 

  3. Genzel, L. & Wixted, J. T. in Cognitive Neuroscience of Memory Consolidation (eds Axmacher, N. & Rasch, B.) 3–16 (Springer, 2017).

  4. Dudai, Y., Karni, A. & Born, J. The consolidation and transformation of memory. Neuron 88, 20–32 (2015).

    Article  PubMed  Google Scholar 

  5. Chrobak, J. J. & Buzsáki, G. High-frequency oscillations in the output networks of the hippocampal–entorhinal axis of the freely behaving rat. J. Neurosci. 16, 3056–3066 (1996).

    Article  PubMed  PubMed Central  Google Scholar 

  6. McClelland, J. L., McNaughton, B. L. & O’Reilly, R. C. 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).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Mednick, S. C. et al. The restorative effect of naps on perceptual deterioration. Nat. Neurosci. 5, 677–681 (2002).

    Article  PubMed  Google Scholar 

  11. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205–211 (2002).

    Article  PubMed  Google Scholar 

  12. Klinzing, J. G., Niethard, N. & Born, J. Mechanisms of systems memory consolidation during sleep. Nat. Neurosci. https://doi.org/10.1038/s41593-019-0467-3 (2019).

  13. Stickgold, R. & Walker, M. P. Sleep-dependent memory triage: evolving generalization through selective processing. Nat. Neurosci. 16, 139–145 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  14. den Berg van, N. H. et al. Sleep enhances consolidation of memory traces for complex problem-solving skills. Cereb. Cortex https://doi.org/10.1093/cercor/bhab216 (2021).

  15. Dewar, M., Alber, J., Butler, C., Cowan, N. & Della Sala, S. Brief wakeful resting boosts new memories over the long term. Psychol. Sci. 23, 955–960 (2012).

    Article  PubMed  Google Scholar 

  16. Brokaw, K. et al. Resting state EEG correlates of memory consolidation. Neurobiol. Learn. Mem. 130, 17–25 (2016).

    Article  PubMed  Google Scholar 

  17. Humiston, G., Tucker, M. A., Summer, T. & Wamsley, E. J. Resting states and memory consolidation: a preregistered replication and meta-analysis. Sci. Rep. 9, 1–9 (2019).

    Article  Google Scholar 

  18. Mercer, T. Wakeful rest alleviates interference-based forgetting. Memory 23, 127–137 (2015).

    Article  PubMed  Google Scholar 

  19. Sacripante, R., McIntosh, R. D. & Della Sala, S. Benefit of wakeful resting on gist and peripheral memory retrieval in healthy younger and older adults. Neurosci. Lett. 705, 27–32 (2019).

    Article  PubMed  Google Scholar 

  20. Wamsley, E. J. & Summer, T. Spontaneous entry into an “offline” state during wakefulness: a mechanism of memory consolidation? J. Cogn. Neurosci. 32, 1714–1734 (2020).

    Article  PubMed  Google Scholar 

  21. Bönstrup, M. et al. A rapid form of offline consolidation in skill learning. Curr. Biol. 29, 1346–1351.e4 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ben-Yakov, A., Eshel, N. & Dudai, Y. Hippocampal immediate poststimulus activity in the encoding of consecutive naturalistic episodes. J. Exp. Psychol. Gen. 142, 1255 (2013).

    Article  PubMed  Google Scholar 

  23. Frankland, P. W. & Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119–130 (2005).

    Article  PubMed  Google Scholar 

  24. Himmer, L., Schönauer, M., Heib, D. P. J., Schabus, M. & Gais, S. Rehearsal initiates systems memory consolidation, sleep makes it last. Sci. Adv. 5, eaav1695 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Tse, D. et al. Schemas and memory consolidation. Science 316, 76–82 (2007).

    Article  PubMed  Google Scholar 

  26. Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).

    Article  PubMed  Google Scholar 

  27. Hasselmo, M. E. & McGaughy, J. 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).

    Article  PubMed  Google Scholar 

  28. Poulet, J. F. A. & Crochet, S. The cortical states of wakefulness. Front. Syst. Neurosci. 12, 64 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Smallwood, J. & Schooler, J. W. The science of mind wandering: empirically navigating the stream of consciousness. Annu. Rev. Psychol. 66, 487–518 (2015).

    Article  PubMed  Google Scholar 

  30. Wang, H.-T. et al. Dimensions of experience: exploring the heterogeneity of the wandering mind. Psychol. Sci. 29, 56–71 (2018).

    Article  PubMed  Google Scholar 

  31. Delamillieure, P. et al. The resting state questionnaire: an introspective questionnaire for evaluation of inner experience during the conscious resting state. Brain Res. Bull. 81, 565–573 (2010).

    Article  PubMed  Google Scholar 

  32. Gorgolewski, K. J. et al. A correspondence between individual differences in the brain’s intrinsic functional architecture and the content and form of self-generated thoughts. PLoS ONE 9, e97176 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Seli, P., Risko, E. F. & Smilek, D. On the necessity of distinguishing between unintentional and intentional mind wandering. Psychol. Sci. 27, 685–691 (2016).

    Article  PubMed  Google Scholar 

  34. Seli, P. et al. Mind-wandering as a natural kind: a family-resemblances view. Trends Cogn. Sci. 22, 479–490 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Andrews-Hanna, J. R., Irving, Z. C., Fox, K. C. R., Spreng, R. N. & Christo, K. in The Oxford Handbook of Spontaneous Thought: Mind-Wandering, Creativity, and Dreaming (eds Kalina Christoff, K. & Fox, K. C. R.) (Oxford Univ. Press, 2018).

  36. Christoff, K., Irving, Z. C., Fox, K. C. R., Spreng, R. N. & Andrews-Hanna, J. R. Mind-wandering as spontaneous thought: a dynamic framework. Nat. Rev. Neurosci. https://doi.org/10.1038/nrn.2016.113 (2016).

  37. Vidaurre, D. et al. Spontaneous cortical activity transiently organises into frequency specific phase-coupling networks. Nat. Commun. 9, 2987 (2018).

  38. Payne, J. D., Stickgold, R., Swanberg, K. & Kensinger, E. A. Sleep preferentially enhances memory for emotional components of scenes. Psychol. Sci. 19, 781–788 (2008).

    Article  PubMed  Google Scholar 

  39. Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987–11991 (2002).

    Article  PubMed Central  Google Scholar 

  40. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    Article  PubMed  Google Scholar 

  41. Tucker, M. A., Humiston, G., Summer, T. & Wamsley, E. Comparing the effects of sleep and rest on memory consolidation. Nat. Sci. Sleep 12, 79–91 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Martini, M., Martini, C., Bernegger, C. & Sachse, P. Post-encoding wakeful resting supports the retention of new verbal memories in children aged 13–14 years. Br. J. Dev. Psychol. 37, 199–210 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Hermans, E. J. et al. Persistence of amygdala–hippocampal connectivity and multi-voxel correlation structures during awake rest after fear learning predicts long-term expression of fear. Cereb. Cortex 27, 3028–3041 (2017).

    PubMed  Google Scholar 

  44. Mednick, S. C., Makovski, T., Cai, D. J. & Jiang, Y. V. Sleep and rest facilitate implicit memory in a visual search task. Vis. Res. 49, 2557–2565 (2009).

    Article  PubMed  Google Scholar 

  45. Martini, M., Martini, C., Maran, T. & Sachse, P. Effects of post-encoding wakeful rest and study time on long-term memory performance. J. Cogn. Psychol. 30, 5–6, 558–569 (2018).

    Article  Google Scholar 

  46. Humiston, G. & Wamsley, E. J. A brief period of eyes-closed rest enhances motor skill consolidation. Neurobiol. Learn. Mem. 155, 1–6 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Craig, M. et al. Comparable rest-related promotion of spatial memory consolidation in younger and older adults. Neurobiol. Aging 48, 143–152 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Wang, S. Y. et al. ‘Sleep-dependent’ memory consolidation? Brief periods of post-training rest and sleep provide an equivalent benefit for both declarative and procedural memory. Learn. Mem. 28, 195–203 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Schmid, D., Erlacher, D., Klostermann, A., Kredel, R. & Hossner, E.-J. Sleep-dependent motor memory consolidation in healthy adults: a meta-analysis. Neurosci. Biobehav. Rev. 118, 270–281 (2020).

    Article  PubMed  Google Scholar 

  50. Gui, W.-J. et al. Age-related differences in sleep-based memory consolidation: a meta-analysis. Neuropsychologia 97, 46–55 (2017).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  52. Landauer, T. K. Consolidation in human memory: retrograde amnestic effects of confusable items in paired-associate learning. J. Verbal Learn. Verbal Behav. 13, 45–53 (1974).

    Article  Google Scholar 

  53. Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 (1996).

    Article  PubMed  Google Scholar 

  54. Seibt, J. & Frank, M. G. Primed to sleep: the dynamics of synaptic plasticity across brain states. Front. Syst. Neurosci. 13, 2 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Bailey, C. H. & Kandel, E. R. Synaptic remodeling, synaptic growth and the storage of long-term memory in aplysia. Prog. Brain Res. 169, 179–198 (2008).

    Article  PubMed  Google Scholar 

  56. Redondo, R. L. & Morris, R. G. M. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 12, 17–30 (2011).

    Article  PubMed  Google Scholar 

  57. Brodt, S. et al. Rapid and independent memory formation in the parietal cortex. Proc. Natl Acad. Sci. USA 113, 13251–13256 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Craig, M., Sala, S. D. & Dewar, M. Autobiographical thinking interferes with episodic memory consolidation. PLoS ONE 9, e93915 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Varma, S., Daselaar, S. M., Kessels, R. P. C. & Takashima, A. Promotion and suppression of autobiographical thinking differentially affect episodic memory consolidation. PLoS ONE 13, e0201780 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Collins, M. B. & Wamsley, E. J. Effect of postlearning meditation on memory consolidation: level of focused attention matters. Learn. Mem. 27, 250–253 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Martini, M. & Sachse, P. Factors modulating the effects of waking rest on memory. Cogn. Process. 21, 149–153 (2020).

    Article  PubMed  Google Scholar 

  62. Varma, S. et al. Non-interfering effects of active post-encoding tasks on episodic memory consolidation in humans. Front. Behav. Neurosci. 11, 54 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Mednick, S. C., Cai, D. J., Shuman, T., Anagnostaras, S. & Wixted, J. T. An opportunistic theory of cellular and systems consolidation. Trends Neurosci. https://doi.org/10.1016/j.tins.2011.06.003 (2011).

  64. Lewis, P. A. & Durrant, S. J. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn. Sci. 15, 343–351 (2011).

    Article  PubMed  Google Scholar 

  65. Paller, K. A., Creery, J. D. & Schechtman, E. Memory and sleep: how sleep cognition can change the waking mind for the better. Annu. Rev. Psychol. 72, 123–150 (2021).

    Article  PubMed  Google Scholar 

  66. Nere, A., Hashmi, A., Cirelli, C. & Tononi, G. Sleep-dependent synaptic down-selection (I): modeling the benefits of sleep on memory consolidation and integration. Front. Neurol. 4, 143 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Humphreys, G. W. et al. Place cells, navigational accuracy, and the human hippocampus. Phil. Trans. R. Soc. Lond. B 353, 1333–1340 (1998).

    Article  Google Scholar 

  68. Pavlides, C. & Winson, J. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).

    Article  PubMed  Google Scholar 

  70. Gupta, A. S., van der Meer, M. A. A., Touretzky, D. S. & Redish, A. D. Hippocampal replay is not a simple function of experience. Neuron 65, 695–705 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Michon, F., Sun, J.-J., Kim, C. Y., Ciliberti, D. & Kloosterman, F. Post-learning hippocampal replay selectively reinforces spatial memory for highly rewarded locations. Curr. Biol. 29, 1436–1444.e5 (2019).

    Article  PubMed  Google Scholar 

  72. Ji, D. & Wilson, M. A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100–107 (2007).

    Article  PubMed  Google Scholar 

  73. Carr, M. F., Jadhav, S. P. & Frank, L. M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147–153 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Foster, D. J. & Wilson, M. A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

    Article  PubMed  Google Scholar 

  75. Valdés, J. L., McNaughton, B. L. & Fellous, J.-M. Offline reactivation of experience-dependent neuronal firing patterns in the rat ventral tegmental area. J. Neurophysiol. 114, 1183–1195 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Tambini, A. & Davachi, L. Awake reactivation of prior experiences consolidates memories and biases cognition. Trends Cogn. Sci. https://doi.org/10.1016/j.tics.2019.07.008 (2019).

  77. Tambini, A. & Davachi, L. Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory. Proc. Natl Acad. Sci. USA 110, 19591–19596 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Liu, Y., Dolan, R. J., Kurth-Nelson, Z. & Behrens, T. E. J. Human replay spontaneously reorganizes experience. Cell 178, 640–652.e14 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Kudrimoti, H. S., Barnes, C. A. & McNaughton, B. L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19, 4090–4101 (1999).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Jadhav, S. P., Kemere, C., German, P. W. & Frank, L. M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454–1458 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Ego-Stengel, V. & Wilson, M. A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1–10 (2010).

    PubMed  PubMed Central  Google Scholar 

  82. Axmacher, N., Elger, C. E. & Fell, J. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain J. Neurol. 131, 1806–1817 (2008).

    Article  Google Scholar 

  83. Oyanedel, C. N., Durán, E., Niethard, N., Inostroza, M. & Born, J. Temporal associations between sleep slow oscillations, spindles and ripples. Eur. J. Neurosci. 52, 4762–4778 (2020).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  85. Destexhe, A., Hughes, S. W., Rudolph, M. & Crunelli, V. Are corticothalamic UP states fragments of wakefulness? Trends Neurosci. 30, 334–342 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  86. Clemens, Z., Fabó, D. & Halász, P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529–535 (2005).

    Article  PubMed  Google Scholar 

  87. Mednick, S. C. et al. The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J. Neurosci. 33, 4494–4504 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Clemens, Z., Fabó, D. & Halász, P. Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 403, 52–56 (2006).

    Article  PubMed  Google Scholar 

  89. Staba, R. J. et al. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol. 56, 108–115 (2004).

    Article  PubMed  Google Scholar 

  90. Billeke, P. et al. Brain state-dependent recruitment of high-frequency oscillations in the human hippocampus. Cortex 94, 87–99 (2017).

    Article  PubMed  Google Scholar 

  91. Jadhav, S. P., Rothschild, G., Roumis, D. K. & Frank, L. M. Coordinated excitation and inhibition of prefrontal ensembles during awake hippocampal sharp-wave ripple events. Neuron 90, 113–127 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Buzsáki, G., Lai-Wo, S. L. & Vanderwolf, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. Rev. 6, 139–171 (1983).

    Article  Google Scholar 

  93. Clemens, Z. et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain J. Neurol. 130, 2868–2878 (2007).

    Article  Google Scholar 

  94. Chen, Y. Y. et al. Stability of ripple events during task engagement in human hippocampus. Cell Rep. 35, 109304 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  96. Hasselmo, M. E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710–715 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Decker, A. L. & Duncan, K. Acetylcholine and the complex interdependence of memory and attention. Curr. Opin. Behav. Sci. 32, 21–28 (2020).

    Article  Google Scholar 

  98. Marrosu, F. et al. Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res. 671, 329–332 (1995).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  100. Inayat, S. et al. Low acetylcholine during early sleep is important for motor memory consolidation. Sleep 43, zsz297 (2020).

    Article  PubMed  Google Scholar 

  101. Reimer, J. et al. Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nat. Commun. 7, 13289 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  102. McGinley, M. J. et al. Waking state: rapid variations modulate neural and behavioral responses. Neuron 87, 1143–1161 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  103. Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D. L. The brain’s default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1–38 (2008).

    Article  PubMed  Google Scholar 

  104. Buckner, R. L. The serendipitous discovery of the brain’s default network. NeuroImage https://doi.org/10.1016/j.neuroimage.2011.10.035 (2011).

  105. Higgins, C. et al. Replay bursts in humans coincide with activation of the default mode and parietal alpha networks. Neuron https://doi.org/10.1016/j.neuron.2020.12.007 (2020).

  106. Kaplan, R. et al. Hippocampal sharp-wave ripples influence selective activation of the default mode network. Curr. Biol. 26, 686–691 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Norman, Y., Raccah, O., Liu, S., Parvizi, J. & Malach, R. Hippocampal ripples and their coordinated dialogue with the default mode network during recent and remote recollection. Neuron https://doi.org/10.1016/j.neuron.2021.06.020 (2021).

  108. Pace-Schott, E. F. & Picchioni, D. in Principles And Practice Of Sleep Medicine (eds Kryger, M. H., Roth, T. & Dement, W. C.) 529–538 (Elsevier, 2022).

  109. Larson-Prior, L. J. et al. Cortical network functional connectivity in the descent to sleep. Proc. Natl Acad. Sci. USA 106, 4489–4494 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Dang-Vu, T. T. et al. Functional neuroimaging insights into the physiology of human sleep. Sleep 33, 1589–1603 (2010).

    Article  PubMed Central  Google Scholar 

  111. Nofzinger, E. et al. Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain J. Neurol. 125, 1105–1115 (2002).

    Article  Google Scholar 

  112. Cox, R., Hofman, W. F. & Talamini, L. M. Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn. Mem. 19, 264–267 (2012).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  114. Tamminen, J., Payne, J. D., Stickgold, R., Wamsley, E. J. & Gaskell, M. G. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J. Neurosci. 30, 14356–14360 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Boutin, A. et al. Transient synchronization of hippocampo-striato-thalamo-cortical networks during sleep spindle oscillations induces motor memory consolidation. NeuroImage 169, 419–430 (2018).

    Article  PubMed  Google Scholar 

  116. Alger, S. E., 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. 98, 188–196 (2012).

    Article  PubMed  Google Scholar 

  117. Crupi, D. et al. Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep 32, 1273–1284 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Marshall, L., Helgadóttir, H., Mölle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006).

    Article  PubMed  Google Scholar 

  119. Backhaus, J. et al. Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep. Learn. Mem. 14, 336–341 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  120. 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. 98, 103–111 (2012).

    Article  PubMed  Google Scholar 

  121. Scullin, M. K. Sleep, memory, and aging: the link between slow-wave sleep and episodic memory changes from younger to older adults. Psychol. Aging 28, 105–114 (2013).

    Article  Google Scholar 

  122. Backhaus, J. et al. Impaired declarative memory consolidation during sleep in patients with primary insomnia: influence of sleep architecture and nocturnal cortisol release. Biol. Psychiat. 60, 1324–1330 (2006).

    Article  PubMed  Google Scholar 

  123. Wamsley, E. J., Tucker, M. A., Payne, J. D. & Stickgold, R. A brief nap is beneficial for human route-learning: the role of navigation experience and EEG spectral power. Learn. Mem. 17, 332–336 (2010).

    Article  PubMed Central  Google Scholar 

  124. Cordi, M. J. & Rasch, B. No evidence for intra-individual correlations between sleep-mediated declarative memory consolidation and slow-wave sleep. Sleep https://doi.org/10.1093/sleep/zsab034 (2021).

  125. Ackermann, S., Hartmann, F., Papassotiropoulos, A., de Quervain, D. J. F. & Rasch, B. No associations between interindividual differences in sleep parameters and episodic memory consolidation. Sleep https://doi.org/10.5665/sleep.4748 (2015).

  126. Fehér, K. D. et al. Shaping the slow waves of sleep: a systematic and integrative review of sleep slow wave modulation in humans using non-invasive brain stimulation. Sleep. Med. Rev. 58, 101438 (2021).

    Article  PubMed  Google Scholar 

  127. Andrillon, T. et al. Does the mind wander when the brain takes a break? Local sleep in wakefulness, attentional lapses and mind-wandering. Front. Neurosci. 13, 949 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  128. Vyazovskiy, V. V. et al. Local sleep in awake rats. Nature 472, 443–447 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Greene, R. L. Effects of maintenance rehearsal on human memory. Psychol. Bull. 102, 403–413 (1987).

    Article  Google Scholar 

  130. Craig, M., Ottaway, G. & Dewar, M. Rest on it: awake quiescence facilities insight. Cortex https://doi.org/10.1016/j.cortex.2018.09.009 (2018).

  131. Dewar, M., Alber, J., Cowan, N. & Della Sala, S. Boosting long-term memory via wakeful rest: intentional rehearsal is not necessary, consolidation is sufficient. PLoS ONE 9, e109542 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Wixted, J. T. A theory about why we forget what we once knew. Curr. Dir. Psychol. Sci. 14, 6–9 (2005).

    Article  Google Scholar 

  133. Fernández-Ruiz, A. et al. Long-duration hippocampal sharp wave ripples improve memory. Science 364, 1082–1086 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Craig, M., Dewar, M., Harris, M. A., Della Sala, S. & Wolbers, T. Wakeful rest promotes the integration of spatial memories into accurate cognitive maps. Hippocampus 26, 185–193 (2016).

    Article  PubMed  Google Scholar 

  135. Killgore, W. D. S. Effects of sleep deprivation on cognition. Prog. Brain Res. 185, 105–129 (2010).

    Article  PubMed  Google Scholar 

  136. Krause, A. J. et al. The sleep-deprived human brain. Nat. Rev. Neurosci. 18, 404–418 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Craig, M., Dewar, M., Della Sala, S. & Wolbers, T. Rest boosts the long-term retention of spatial associative and temporal order information. Hippocampus https://doi.org/10.1002/hipo.22424 (2015).

  138. Gottselig, J. M. et al. Sleep and rest facilitate auditory learning. Neuroscience 127, 557–561 (2004).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  140. Walker, M. P. A refined model of sleep and the time course of memory formation. Behav. Brain Sci. 28, 51–64 (2005).

    Article  PubMed  Google Scholar 

  141. Nissen, C. et al. Sleep is more than rest for plasticity in the human cortex. Sleep https://doi.org/10.1093/sleep/zsaa216 (2021).

  142. Studte, S., Bridger, E. & Mecklinger, A. Nap sleep preserves associative but not item memory performance. Neurobiol. Learn. Mem. 120, 84–93 (2015).

    Article  PubMed  Google Scholar 

  143. Sopp, M. R., Michael, T. & Mecklinger, A. Effects of early morning nap sleep on associative memory for neutral and emotional stimuli. Brain Res. 1698, 29–42 (2018).

    Article  PubMed  Google Scholar 

  144. van der Helm, E., Gujar, N., Nishida, M. & Walker, M. P. Sleep-dependent facilitation of episodic memory details. PLoS ONE 6, e27421 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Pan, S. C. & Rickard, T. C. Sleep and motor learning: is there room for consolidation? Psychol. Bull. 141, 812–834 (2015).

    Article  PubMed  Google Scholar 

  146. Rickard, T. C., Cai, D. J., Rieth, C. A., Jones, J. & Ard, M. C. Sleep does not enhance motor sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 34, 834–842 (2008).

    Article  PubMed  Google Scholar 

  147. Hotermans, C., Peigneux, P., Maertens de Noordhout, A., Moonen, G. & Maquet, P. Early boost and slow consolidation in motor skill learning. Learn. Mem. 13, 580–583 (2006).

    Article  PubMed  Google Scholar 

  148. Alger, S. E., Lau, H. & Fishbein, W. Delayed onset of a daytime nap facilitates retention of declarative memory. PLoS ONE 5, e12131 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  149. Gregory, M. D. et al. Resting state connectivity immediately following learning correlates with subsequent sleep-dependent enhancement of motor task performance. NeuroImage 102P2, 666–673 (2014).

    Article  Google Scholar 

  150. Murphy, M., Stickgold, R., Parr, M. E., Callahan, C. & Wamsley, E. J. Recurrence of task-related electroencephalographic activity during post-training quiet rest and sleep. Sci. Rep. 8, 5398 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Yang, G., Pan, F. & Gan, W.-B. Stably maintained dendritic spines are associated with lifelong memories. Nature 462, 920–924 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  152. McDevitt, E., Duggan, K. A. & Mednick, S. C. REM sleep rescues learning from interference. Neurobiol. Learn. Mem. 122, 51–62 (2015).

    Article  PubMed  Google Scholar 

  153. Ekstrand, B. R. Effect of sleep on memory. J. Exp. Psychol. 75, 64–72 (1967).

    Article  PubMed  Google Scholar 

  154. Drosopoulos, S., Schulze, C., Fischer, S. & Born, J. Sleep’s function in the spontaneous recovery and consolidation of memories. J. Exp. Psychol. Gen. 136, 169–183 (2007).

    Article  PubMed  Google Scholar 

  155. Smallwood, J. & Schooler, J. W. The restless mind. Psychol. Bull. 132, 946–958 (2006).

    Article  PubMed  Google Scholar 

  156. Grandchamp, R., Braboszcz, C. & Delorme, A. Oculometric variations during mind wandering. Front. Psychol. 5, 31 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Hasenkamp, W., Wilson-Mendenhall, C. D., Duncan, E. & Barsalou, L. W. Mind wandering and attention during focused meditation: a fine-grained temporal analysis of fluctuating cognitive states. NeuroImage 59, 750–760 (2012).

    Article  PubMed  Google Scholar 

  158. Voss, M. J., Zukosky, M. & Wang, R. F. A new approach to differentiate states of mind wandering: effects of working memory capacity. Cognition 179, 202–212 (2018).

    Article  PubMed  Google Scholar 

  159. Antrobus, J. S., Singer, J. L. & Greenberg, S. Studies in the stream of consciousness: experimental enhancement and suppression of spontaneous cognitive processes. Percept. Mot. Skills 23, 399–417 (1966).

    Article  Google Scholar 

  160. Giambra, L. M. A laboratory method for investigating influences on switching attention to task-unrelated imagery and thought. Conscious. Cogn. 4, 1–21 (1995).

    Article  PubMed  Google Scholar 

  161. Stawarczyk, D., Majerus, S., Maj, M., Van der Linden, M. & D’Argembeau, A. Mind-wandering: phenomenology and function as assessed with a novel experience sampling method. Acta Psychol. 136, 370–381 (2011).

    Article  Google Scholar 

  162. Barron, E., Riby, L. M., Greer, J. & Smallwood, J. Absorbed in thought the effect of mind wandering on the processing of relevant and irrelevant events. Psychol. Sci. 22, 596–601 (2011).

    Article  PubMed  Google Scholar 

  163. Smallwood, J., Beach, E., Schooler, J. W. & Handy, T. C. Going AWOL in the brain: mind wandering reduces cortical analysis of external events. J. Cogn. Neurosci. 20, 458–469 (2008).

    Article  PubMed  Google Scholar 

  164. Groot, J. M. et al. Probing the neural signature of mind wandering with simultaneous fMRI-EEG and pupillometry. NeuroImage 224, 117412 (2021).

    Article  PubMed  Google Scholar 

  165. Smallwood, J. et al. Pupillometric evidence for the decoupling of attention from perceptual input during offline thought. PLoS ONE 6, e18298 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  166. Schooler, J. W. et al. Meta-awareness, perceptual decoupling and the wandering mind. Trends Cogn. Sci. https://doi.org/10.1016/j.tics.2011.05.006 (2011).

  167. Reimer, J. et al. Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84, 355–362 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  168. Poulet, J. F. A. Keeping an eye on cortical states. Neuron 84, 246–248 (2014).

    Article  PubMed  Google Scholar 

  169. McCormick, D. A., Nestvogel, D. B. & He, B. J. Neuromodulation of brain state and behavior. Annu. Rev. Neurosci. 43, 391–415 (2020).

    Article  PubMed  Google Scholar 

  170. Beaman, C. B., Eagleman, S. L. & Dragoi, V. Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state. Nat. Commun. 8, 1308 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  171. Lee, C. C. Y., Kheradpezhouh, E., Diamond, M. E. & Arabzadeh, E. State-dependent changes in perception and coding in the mouse somatosensory cortex. Cell Rep. 32, 108197 (2020).

    Article  PubMed  Google Scholar 

  172. McGinley, M. J., David, S. V. & McCormick, D. A. Cortical membrane potential signature of optimal states for sensory signal detection. Neuron 87, 179–192 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  173. Arnau, S. et al. Inter-trial alpha power indicates mind wandering. Psychophysiology 57, e13581 (2020).

    Article  PubMed  Google Scholar 

  174. Compton, R. J., Gearinger, D. & Wild, H. The wandering mind oscillates: EEG alpha power is enhanced during moments of mind-wandering. Cogn. Affect. Behav. Neurosci. 19, 1184–1191 (2019).

    Article  PubMed  Google Scholar 

  175. Braboszcz, C. & Delorme, A. Lost in thoughts: neural markers of low alertness during mind wandering. NeuroImage 54, 3040–3047 (2011).

    Article  PubMed  Google Scholar 

  176. Unsworth, N. & Robison, M. K. Pupillary correlates of lapses of sustained attention. Cogn. Affect. Behav. Neurosci. 16, 601–615 (2016).

    Article  PubMed  Google Scholar 

  177. Konishi, M., Brown, K., Battaglini, L. & Smallwood, J. When attention wanders: pupillometric signatures of fluctuations in external attention. Cognition 168, 16–26 (2017).

    Article  PubMed  Google Scholar 

  178. Murphy, P. R., O’Connell, R. G., O’Sullivan, M., Robertson, I. H. & Balsters, J. H. Pupil diameter covaries with BOLD activity in human locus coeruleus. Hum. Brain Mapp. 35, 4140–4154 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  179. van Son, D. et al. Electroencephalography theta/beta ratio covaries with mind wandering and functional connectivity in the executive control network. Ann. N. Y. Acad. Sci. 1452, 52–64 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  180. Brink, R. L., van den, Murphy, P. R. & Nieuwenhuis, S. Pupil diameter tracks lapses of attention. PLoS ONE 11, e0165274 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  181. Vidaurre, D., Smith, S. M. & Woolrich, M. W. Brain network dynamics are hierarchically organized in time. Proc. Natl Acad. Sci. USA 114, 12827–12832 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  182. Ben-Yakov, A. & Dudai, Y. Constructing realistic engrams: poststimulus activity of hippocampus and dorsal striatum predicts subsequent episodic memory. J. Neurosci. 31, 9032–9042 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  183. Sols, I., DuBrow, S., Davachi, L. & Fuentemilla, L. Event boundaries trigger rapid memory reinstatement of the prior events to promote their representation in long-term memory. Curr. Biol. 27, 3499–3504.e4 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  184. Staresina, B. P., Alink, A., Kriegeskorte, N. & Henson, R. N. Awake reactivation predicts memory in humans. Proc. Natl Acad. Sci. USA 110, 21159–21164 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  185. Grossman, N. et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell 169, 1029–1041.e16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  186. Tambini, A., Berners-Lee, A. & Davachi, L. Brief targeted memory reactivation during the awake state enhances memory stability and benefits the weakest memories. Sci. Rep. 7, 15325 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  187. Schreiner, T. & Rasch, B. Boosting vocabulary learning by verbal cueing during sleep. Cereb. Cortex 25, 4169–4179 (2014).

    Article  PubMed  Google Scholar 

  188. Martini, M., Heinz, A., Hinterholzer, J., Martini, C. & Sachse, P. Effects of wakeful resting versus social media usage after learning on the retention of new memories. Appl. Cogn. Psychol. 34, 551–558 (2020).

    Article  Google Scholar 

  189. McGhee, J. D., Cowan, N., Beschin, N., Mosconi, C. & Della Sala, S. Wakeful rest benefits before and after encoding in anterograde amnesia. Neuropsychology 34, 524 (2020).

    Article  PubMed  Google Scholar 

  190. Riley, G. A. & Pearce, A. Wakeful rest during storage and consolidation enhances priming effects for those with acquired memory impairment. Memory 29, 547–558 (2021).

    Article  PubMed  Google Scholar 

  191. McDevitt, E. A., Rokem, A., Silver, M. A. & Mednick, S. C. Sex differences in sleep-dependent perceptual learning. Vis. Res. 99, 172–179 (2014).

    Article  PubMed  Google Scholar 

  192. Wamsley, E. J. Memory consolidation during waking rest. Trends Cogn. Sci. 23, 171–173 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

E.J.W.’s laboratory has been funded by the National Science Foundation (BCS-1849026), the National Institute of Mental Health (R15MH107891), and the BIAL Foundation (Bursaries Award 211/16).

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Wamsley, E.J. Offline memory consolidation during waking rest. Nat Rev Psychol 1, 441–453 (2022). https://doi.org/10.1038/s44159-022-00072-w

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