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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 digital issues and online access to articles
$59.00 per year
only $4.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Killingsworth, M. A. & Gilbert, D. T. A wandering mind is an unhappy mind. Science 330, 932 (2010).
McGaugh, J. L. Memory — a century of consolidation. Science 287, 248–251 (2000).
Genzel, L. & Wixted, J. T. in Cognitive Neuroscience of Memory Consolidation (eds Axmacher, N. & Rasch, B.) 3–16 (Springer, 2017).
Dudai, Y., Karni, A. & Born, J. The consolidation and transformation of memory. Neuron 88, 20–32 (2015).
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).
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).
Buzsáki, G. Memory consolidation during sleep: a neurophysiological perspective. J. Sleep. Res. 7, 17–23 (1998).
Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997).
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).
Mednick, S. C. et al. The restorative effect of naps on perceptual deterioration. Nat. Neurosci. 5, 677–681 (2002).
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).
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).
Stickgold, R. & Walker, M. P. Sleep-dependent memory triage: evolving generalization through selective processing. Nat. Neurosci. 16, 139–145 (2013).
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).
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).
Brokaw, K. et al. Resting state EEG correlates of memory consolidation. Neurobiol. Learn. Mem. 130, 17–25 (2016).
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).
Mercer, T. Wakeful rest alleviates interference-based forgetting. Memory 23, 127–137 (2015).
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).
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).
Bönstrup, M. et al. A rapid form of offline consolidation in skill learning. Curr. Biol. 29, 1346–1351.e4 (2019).
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).
Frankland, P. W. & Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119–130 (2005).
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).
Tse, D. et al. Schemas and memory consolidation. Science 316, 76–82 (2007).
Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).
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).
Poulet, J. F. A. & Crochet, S. The cortical states of wakefulness. Front. Syst. Neurosci. 12, 64 (2019).
Smallwood, J. & Schooler, J. W. The science of mind wandering: empirically navigating the stream of consciousness. Annu. Rev. Psychol. 66, 487–518 (2015).
Wang, H.-T. et al. Dimensions of experience: exploring the heterogeneity of the wandering mind. Psychol. Sci. 29, 56–71 (2018).
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).
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).
Seli, P., Risko, E. F. & Smilek, D. On the necessity of distinguishing between unintentional and intentional mind wandering. Psychol. Sci. 27, 685–691 (2016).
Seli, P. et al. Mind-wandering as a natural kind: a family-resemblances view. Trends Cogn. Sci. 22, 479–490 (2018).
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).
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).
Vidaurre, D. et al. Spontaneous cortical activity transiently organises into frequency specific phase-coupling networks. Nat. Commun. 9, 2987 (2018).
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).
Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987–11991 (2002).
Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).
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).
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).
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).
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).
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).
Humiston, G. & Wamsley, E. J. A brief period of eyes-closed rest enhances motor skill consolidation. Neurobiol. Learn. Mem. 155, 1–6 (2018).
Craig, M. et al. Comparable rest-related promotion of spatial memory consolidation in younger and older adults. Neurobiol. Aging 48, 143–152 (2016).
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).
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).
Gui, W.-J. et al. Age-related differences in sleep-based memory consolidation: a meta-analysis. Neuropsychologia 97, 46–55 (2017).
Korman, M. et al. Daytime sleep condenses the time course of motor memory consolidation. Nat. Neurosci. 10, 1206–1213 (2007).
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).
Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 (1996).
Seibt, J. & Frank, M. G. Primed to sleep: the dynamics of synaptic plasticity across brain states. Front. Syst. Neurosci. 13, 2 (2019).
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).
Redondo, R. L. & Morris, R. G. M. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 12, 17–30 (2011).
Brodt, S. et al. Rapid and independent memory formation in the parietal cortex. Proc. Natl Acad. Sci. USA 113, 13251–13256 (2016).
Craig, M., Sala, S. D. & Dewar, M. Autobiographical thinking interferes with episodic memory consolidation. PLoS ONE 9, e93915 (2014).
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).
Collins, M. B. & Wamsley, E. J. Effect of postlearning meditation on memory consolidation: level of focused attention matters. Learn. Mem. 27, 250–253 (2020).
Martini, M. & Sachse, P. Factors modulating the effects of waking rest on memory. Cogn. Process. 21, 149–153 (2020).
Varma, S. et al. Non-interfering effects of active post-encoding tasks on episodic memory consolidation in humans. Front. Behav. Neurosci. 11, 54 (2017).
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).
Lewis, P. A. & Durrant, S. J. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn. Sci. 15, 343–351 (2011).
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).
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).
Humphreys, G. W. et al. Place cells, navigational accuracy, and the human hippocampus. Phil. Trans. R. Soc. Lond. B 353, 1333–1340 (1998).
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).
Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).
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).
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).
Ji, D. & Wilson, M. A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100–107 (2007).
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).
Foster, D. J. & Wilson, M. A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).
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).
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).
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).
Liu, Y., Dolan, R. J., Kurth-Nelson, Z. & Behrens, T. E. J. Human replay spontaneously reorganizes experience. Cell 178, 640–652.e14 (2019).
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).
Jadhav, S. P., Kemere, C., German, P. W. & Frank, L. M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454–1458 (2012).
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).
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).
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).
Rosanova, M. & Ulrich, D. Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 25, 9398–9405 (2005).
Destexhe, A., Hughes, S. W., Rudolph, M. & Crunelli, V. Are corticothalamic UP states fragments of wakefulness? Trends Neurosci. 30, 334–342 (2007).
Clemens, Z., Fabó, D. & Halász, P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529–535 (2005).
Mednick, S. C. et al. The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J. Neurosci. 33, 4494–4504 (2013).
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).
Staba, R. J. et al. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol. 56, 108–115 (2004).
Billeke, P. et al. Brain state-dependent recruitment of high-frequency oscillations in the human hippocampus. Cortex 94, 87–99 (2017).
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).
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).
Clemens, Z. et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain J. Neurol. 130, 2868–2878 (2007).
Chen, Y. Y. et al. Stability of ripple events during task engagement in human hippocampus. Cell Rep. 35, 109304 (2021).
Hasselmo Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351–359 (1999).
Hasselmo, M. E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710–715 (2006).
Decker, A. L. & Duncan, K. Acetylcholine and the complex interdependence of memory and attention. Curr. Opin. Behav. Sci. 32, 21–28 (2020).
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).
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).
Inayat, S. et al. Low acetylcholine during early sleep is important for motor memory consolidation. Sleep 43, zsz297 (2020).
Reimer, J. et al. Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nat. Commun. 7, 13289 (2016).
McGinley, M. J. et al. Waking state: rapid variations modulate neural and behavioral responses. Neuron 87, 1143–1161 (2015).
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).
Buckner, R. L. The serendipitous discovery of the brain’s default network. NeuroImage https://doi.org/10.1016/j.neuroimage.2011.10.035 (2011).
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).
Kaplan, R. et al. Hippocampal sharp-wave ripples influence selective activation of the default mode network. Curr. Biol. 26, 686–691 (2016).
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).
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).
Larson-Prior, L. J. et al. Cortical network functional connectivity in the descent to sleep. Proc. Natl Acad. Sci. USA 106, 4489–4494 (2009).
Dang-Vu, T. T. et al. Functional neuroimaging insights into the physiology of human sleep. Sleep 33, 1589–1603 (2010).
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).
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).
Schabus, M. et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479–1485 (2004).
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).
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).
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).
Crupi, D. et al. Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep 32, 1273–1284 (2009).
Marshall, L., Helgadóttir, H., Mölle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Vyazovskiy, V. V. et al. Local sleep in awake rats. Nature 472, 443–447 (2011).
Greene, R. L. Effects of maintenance rehearsal on human memory. Psychol. Bull. 102, 403–413 (1987).
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).
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).
Wixted, J. T. A theory about why we forget what we once knew. Curr. Dir. Psychol. Sci. 14, 6–9 (2005).
Fernández-Ruiz, A. et al. Long-duration hippocampal sharp wave ripples improve memory. Science 364, 1082–1086 (2019).
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).
Killgore, W. D. S. Effects of sleep deprivation on cognition. Prog. Brain Res. 185, 105–129 (2010).
Krause, A. J. et al. The sleep-deprived human brain. Nat. Rev. Neurosci. 18, 404–418 (2017).
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).
Gottselig, J. M. et al. Sleep and rest facilitate auditory learning. Neuroscience 127, 557–561 (2004).
Robertson, E. M. From creation to consolidation: a novel framework for memory processing. PLoS Biol. 7, e19 (2009).
Walker, M. P. A refined model of sleep and the time course of memory formation. Behav. Brain Sci. 28, 51–64 (2005).
Nissen, C. et al. Sleep is more than rest for plasticity in the human cortex. Sleep https://doi.org/10.1093/sleep/zsaa216 (2021).
Studte, S., Bridger, E. & Mecklinger, A. Nap sleep preserves associative but not item memory performance. Neurobiol. Learn. Mem. 120, 84–93 (2015).
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).
van der Helm, E., Gujar, N., Nishida, M. & Walker, M. P. Sleep-dependent facilitation of episodic memory details. PLoS ONE 6, e27421 (2011).
Pan, S. C. & Rickard, T. C. Sleep and motor learning: is there room for consolidation? Psychol. Bull. 141, 812–834 (2015).
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).
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).
Alger, S. E., Lau, H. & Fishbein, W. Delayed onset of a daytime nap facilitates retention of declarative memory. PLoS ONE 5, e12131 (2010).
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).
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).
Yang, G., Pan, F. & Gan, W.-B. Stably maintained dendritic spines are associated with lifelong memories. Nature 462, 920–924 (2009).
McDevitt, E., Duggan, K. A. & Mednick, S. C. REM sleep rescues learning from interference. Neurobiol. Learn. Mem. 122, 51–62 (2015).
Ekstrand, B. R. Effect of sleep on memory. J. Exp. Psychol. 75, 64–72 (1967).
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).
Smallwood, J. & Schooler, J. W. The restless mind. Psychol. Bull. 132, 946–958 (2006).
Grandchamp, R., Braboszcz, C. & Delorme, A. Oculometric variations during mind wandering. Front. Psychol. 5, 31 (2014).
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).
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).
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).
Giambra, L. M. A laboratory method for investigating influences on switching attention to task-unrelated imagery and thought. Conscious. Cogn. 4, 1–21 (1995).
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).
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).
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).
Groot, J. M. et al. Probing the neural signature of mind wandering with simultaneous fMRI-EEG and pupillometry. NeuroImage 224, 117412 (2021).
Smallwood, J. et al. Pupillometric evidence for the decoupling of attention from perceptual input during offline thought. PLoS ONE 6, e18298 (2011).
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).
Reimer, J. et al. Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84, 355–362 (2014).
Poulet, J. F. A. Keeping an eye on cortical states. Neuron 84, 246–248 (2014).
McCormick, D. A., Nestvogel, D. B. & He, B. J. Neuromodulation of brain state and behavior. Annu. Rev. Neurosci. 43, 391–415 (2020).
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).
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).
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).
Arnau, S. et al. Inter-trial alpha power indicates mind wandering. Psychophysiology 57, e13581 (2020).
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).
Braboszcz, C. & Delorme, A. Lost in thoughts: neural markers of low alertness during mind wandering. NeuroImage 54, 3040–3047 (2011).
Unsworth, N. & Robison, M. K. Pupillary correlates of lapses of sustained attention. Cogn. Affect. Behav. Neurosci. 16, 601–615 (2016).
Konishi, M., Brown, K., Battaglini, L. & Smallwood, J. When attention wanders: pupillometric signatures of fluctuations in external attention. Cognition 168, 16–26 (2017).
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).
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).
Brink, R. L., van den, Murphy, P. R. & Nieuwenhuis, S. Pupil diameter tracks lapses of attention. PLoS ONE 11, e0165274 (2016).
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).
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).
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).
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).
Grossman, N. et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell 169, 1029–1041.e16 (2017).
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).
Schreiner, T. & Rasch, B. Boosting vocabulary learning by verbal cueing during sleep. Cereb. Cortex 25, 4169–4179 (2014).
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).
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).
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).
McDevitt, E. A., Rokem, A., Silver, M. A. & Mednick, S. C. Sex differences in sleep-dependent perceptual learning. Vis. Res. 99, 172–179 (2014).
Wamsley, E. J. Memory consolidation during waking rest. Trends Cogn. Sci. 23, 171–173 (2019).
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Reviews Psychology thanks Maren Cordi, Ruth Leong, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s44159-022-00072-w