Sleep and human cognitive development

Gina M Mason, Sanna Lokhandwala, Tracy Riggins, Rebecca M C Spencer, Gina M Mason, Sanna Lokhandwala, Tracy Riggins, Rebecca M C Spencer

Abstract

Emerging studies across learning domains have shed light on mechanisms underlying sleep's benefits during numerous developmental periods. In this conceptual review, we survey recent studies of sleep and cognition across infancy, childhood, and adolescence. By summarizing recent findings and integrating across studies with disparate approaches, we provide a novel understanding of sleep's role in human cognitive function. Collectively, these studies point to an interrelation between brain development, sleep, and cognition. Moreover, we point to gaps in our understanding, which inform the agenda for future research in developmental and sleep science.

Keywords: Childhood; Cognition; Development; Infancy; Memory; Naps.

Conflict of interest statement

Conflicts of interest The authors do not have any conflicts of interest to disclose.

Copyright © 2021 Elsevier Ltd. All rights reserved.

References

    1. Iglowstein I, Jenni OG, Molinari L, Largo RH. Sleep duration From infancy to adolescence: Reference values and generational trends. Pediatrics 2004;111:302–7. 10.1542/peds.111.2.302.
    1. Weissbluth M Naps in children: 6 months-7 years. Sleep 1995;18:82–7.
    1. Galland BC, Taylor BJ, Elder DE, Herbison P. Normal sleep patterns in infants and children: a systematic review of observational studies. Sleep Med Rev 2012;16:213–22. 10.1016/j.smrv.2011.06.001.
    1. Urbán R, Magyaródi T, Rigó A. Morningness-eveningness, chronotypes and health-impairing behaviors in adolescents. Chronobiol Int 2011;28:238–47. 10.3109/07420528.2010.549599.
    1. Riggins T Longitudinal investigation of source memory reveals different developmental trajectories for item memory and binding. Dev Psychol 2014;50:449–59.
    1. Lam JC, Mahone EM, Mason T, Scharf SM. The effects of napping on cognitive function in preschoolers. J Dev Behav Pediatr 2011;32:90–7. 10.1097/DBP.0b013e318207ecc7.
    1. Kurdziel L, Duclos K, Spencer RMC. Sleep spindles in midday naps enhance learning in preschool children. Proc Natl Acad Sci U S A 2013;110:17267–72. 10.1073/pnas.1306418110.
    1. Riggins T, Spencer RMC. Habitual sleep is associated with both source memory and hippocampal subfield volume during early childhood. Sci Rep n.d.
    1. Kurth S, Ringli M, LeBourgeois MK, Geiger A, Buchmann A, Jenni OG, et al. Mapping the electrophysiological marker of sleep depth reveals skill maturation in children and adolescents. Neuroimage 2012;63:959–65. 10.1016/j.neuroimage.2012.03.053.
    1. Kurth S, Riedner BA, Dean DC, O’Muircheartaigh J, Huber R, Jenni OG, et al. Traveling slow oscillations during sleep: A marker of brain connectivity in childhood. Sleep 2017;40:1–10. 10.1093/sleep/zsx121.
    1. Kurth S, Achermann P, Rusterholz T, Lebourgeois MK. Development of brain EEG connectivity across early childhood: Does sleep play a role? Brain Sci 2013;3:1445–60. 10.3390/brainsci3041445.
    1. Horváth K, Hannon B, Ujma PP, Gombos F, Plunkett K. Memory in 3-month-old infants benefits from a short nap. Dev Sci 2018;21:e12587. 10.1111/desc.12587.
    1. Seehagen S, Konrad C, Herbert JS, Schneider S, Heller HC. Timely sleep facilitates declarative memory consolidation in infants. Proc Natl Acad Sci 2015;3:1625–9. 10.1073/pnas.1414000112.
    1. Friedrich M, Wilhelm I, Born J, Friederici AD. Generalization of word meanings during infant sleep. Nat Commun 2015;6:6004. 10.1038/ncomms7004.
    1. Horváth K, Myers K, Foster R, Plunkett K. Napping facilitates word learning in early lexical development. J Sleep Res 2015;24:503–9. 10.1111/jsr.12306.
    1. Seehagen S, Zmyj N, Herbert JS. Remembering in the context of internal states: the role of sleep for infant memory. Child Dev Perspect 2019;13:110–5. 10.1111/cdep.12321.
    1. Friedrich M, Mölle M, Friederici AD, Born J. Sleep-dependent memory consolidation in infants protects new episodic memories from existing semantic memories. Nat Commun 2020;11:1–9.
    1. Lokhandwala S, Spencer RMC. Slow wave sleep in naps supports episodic memories in early childhood. Dev Sci 2020;00:e13035. 10.1111/desc.13035.
    1. Williams SE, Horst JS. Goodnight book: sleep consolidation improves word learning via storybooks. Front Psychol 2014;5:184. 10.3389/fpsyg.2014.00184.
    1. Backhaus J, Hoeckesfeld R, Born J, Hohagen F, Junghanns K. Immediate as well as delayed post learning sleep but not wakefulness enhances declarative memory consolidation in children. Neurobiol Learn Mem 2008;89:76–80. 10.1016/j.nlm.2007.08.010.
    1. Henderson LM, Weighall AR, Brown H, Gaskell MG. Consolidation of vocabulary is associated with sleep in children. Dev Sci 2012;15:674–87. 10.1111/j.1467-7687.2012.01172.x.
    1. Wilhelm I, Diekelmann S, Born J. Sleep in children improves memory performance on declarative but not procedural tasks. Learn Mem 2008;15:373–7. 10.1101/lm.803708.
    1. James E, Gaskell MG, Henderson LM. Sleep-dependent consolidation in children with comprehension and vocabulary weaknesses: it’ll be alright on the night? J Child Psychol Psychiatry Allied Discip 2020;61:1104–15. 10.1111/jcpp.13253.
    1. Gais S, Lucas B, Born J. Sleep after learning aids memory recall. Learn Mem 2006;13:259–62. 10.1101/lm.132106.
    1. Lau EYY, McAteer S, Leung CNW, Tucker MA, Li C. Beneficial effects of a daytime nap on verbal memory in adolescents. J Adolesc 2018;67:77–84. 10.1016/j.adolescence.2018.06.004.
    1. Leong RLF, van Rijn E, Koh SYJ, Chee MWL, Lo JC. Sleep improves memory for the content but not execution of intentions in adolescents. Sleep Med 2019:(E-pub ahead of print). 10.1016/j.sleep.2018.12.023.
    1. Holz J, Piosczyk H, Landmann N, Feige B, Spiegelhalder K, Riemann D, et al. The timing of learning before night-time sleep differentially affects declarative and procedural long-term memory consolidation in adolescents. PLoS One 2012;7:e40963. 10.1371/journal.pone.0040963.
    1. Kopasz M, Loessl B, Valerius G, Koenig E, Matthaeas N, Hornyak M, et al. No persisting effect of partial sleep curtailment on cognitive performance and declarative memory recall in adolescents. J Sleep Res 2010;19:71–9. 10.1111/j.1365-2869.2009.00742.x.
    1. Voderholzer U, Piosczyk H, Holz J, Landmann N, Feige B, Loessl B, et al. Sleep restriction over several days does not affect long-term recall of declarative and procedural memories in adolescents. Sleep Med 2011;12:170–8. 10.1016/j.sleep.2010.07.017.
    1. Cousins JN, Sasmita K, Chee MWL. Memory encoding is impaired after multiple nights of partial sleep restriction. J Sleep Res 2018;27:138–45. 10.1111/jsr.12578.
    1. Short MA, Chee MWL. Adolescent sleep restriction effects on cognition and mood. Prog. Brain Res, 2019. 10.1016/bs.pbr.2019.02.008.
    1. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci 2010;11:114–26. 10.1038/nrn2762.
    1. Gómez RL, Edgin JO. The extended trajectory of hippocampal development: Implications for early memory development and disorder. Dev Cogn Neurosci 2016;18:57–69. 10.1016/j.dcn.2015.08.009.
    1. Tononi G, Cirelli C. Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration. Neuron 2014;81:12–34. 10.1016/J.NEURON.2013.12.025.
    1. Cowan E, Liu A, Henin S, Kothare S, Devinsky O, Davachi XL. Sleep spindles promote the restructuring of memory representations in ventromedial prefrontal cortex through enhanced hippocampal–cortical functional connectivity. J Neurosci 2020;40:1909–19. 10.1523/JNEUROSCI.1946-19.2020.
    1. Ngo HV, Fell J, Staresina B. Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples. Elife 2020;9:1–18. 10.7554/eLife.57011.
    1. Mednick SC, McDevitt EA, Walsh JK, Wamsley E, Paulus M, Kanady JC, et al. The critical role of sleep spindles in hippocampal-dependent memory: A pharmacology study. J Neurosci 2013;33:4494–504. 10.1523/JNEUROSCI.3127-12.2013.
    1. Niethard N, Ngo HVV., Ehrlich I, Born J. Cortical circuit activity underlying sleep slow oscillations and spindles. Proc Natl Acad Sci 2018;115:E9220–9. 10.1073/pnas.1805517115.
    1. Spanò G, Gómez RL, Demara BI, Alt M, Cowen SL, Edgin JO. REM sleep in naps differentially relates to memory consolidation in typical preschoolers and children with Down syndrome. Proc Natl Acad Sci 2018;115:11844–9.
    1. Ackermann S, Rasch B. Differential effects of non-REM and REM sleep on memory consolidation? Curr Neurol Neurosci Rep 2014;14:1–10. 10.1007/s11910-013-0430-8.
    1. Wilhelm I, Rose M, Imhof KI, Rasch B, Büchel C, Born J. The sleeping child outplays the adult’s capacity to convert implicit into explicit knowledge. Nat Neurosci 2013;16:391–3.
    1. Peiffer A, Brichet M, De Tiège X, Peigneux P, Urbain C. The power of children’s sleep - Improved declarative memory consolidation in children compared with adults. Sci Rep 2020;10. 10.1038/s41598-020-66880-3.
    1. Hahn M, Joechner AK, Roell J, Schabus M, Heib DP, Gruber G, et al. Developmental changes of sleep spindles and their impact on sleep-dependent memory consolidation and general cognitive abilities: A longitudinal approach. Dev Sci 2019;22:e12706. 10.1111/desc.12706.
    1. Ong JL, Lo JC, Gooley JJ, Chee MWL. EEG changes across multiple nights of sleep restriction and recovery in adolescents: the need for sleep study. Sleep 2016;39:1233–40. 10.5665/sleep.5840.
    1. Piosczyk H, Holz J, Feige B, Spiegelhalder K, Weber F, Landmann N, et al. The effect of sleep-specific brain activity versus reduced stimulus interference on declarative memory consolidation. J Sleep Res 2013;22:406–13.
    1. Fagen JW, Rovee-Collier C. Memory retrieval: A time-locked process in infancy. Science (80- ) 1983;222:1349–51.
    1. Berger SE, Scher A. Naps improve new walkers’ locomotor problem solving. J Exp Child Psychol 2017;162:292–300. 10.1016/j.jecp.2017.04.021.
    1. Desrochers PC, Kurdziel LBF, Spencer RMC. Delayed benefit of naps on motor learning in preschool children. Exp Brain Res 2016;234:763–72.
    1. Wilhelm I, Metzkow-Mészàros M, Knapp S, Born J. Sleep-dependent consolidation of procedural motor memories in children and adults: the pre-sleep level of performance matters. Dev Sci 2012;15:506–15. 10.1111/j.1467-7687.2012.01146.x.
    1. Prehn-Kristensen A, Göder R, Chirobeja S, Breßmann I, Ferstl R, Baving L. Sleep in children enhances preferentially emotional declarative but not procedural memories. J Exp Child Psychol 2009;104:132–9. 10.1016/j.jecp.2009.01.005.
    1. Fischer S, Wilhelm I, Born J. Developmental differences in sleep’s role for implicit off-line learning: comparing children with adults. J Cogn Neurosci 2007;19:214–27. 10.1162/jocn.2007.19.2.214.
    1. Derégnaucourt S, Mitra PP, Fehér O, Pytte C, Tchernichovski O. How sleep affects the developmental learning of bird song. Nature 2005;433:710–6. 10.1038/nature03275.
    1. Kurdziel LBF. The memory function of sleep across the lifespan. In: Jha SK, Jha VM, editors. Sleep, Mem. Synaptic Plast, Singapore: 2019, p. 1–39. 10.1007/978-981-13-2814-5.
    1. Prehn-Kristensen A, Molzow I, Munz M, Wilhelm I, Müller K, Freytag D, et al. Sleep restores daytime deficits in procedural memory in children with attention-deficit/hyperactivity disorder. Res Dev Disabil 2011;32:2480–8. 10.1016/j.ridd.2011.06.021.
    1. Cremone A, Lugo-Candelas CI, Harvey EA, McDermott JM, Spencer RMC. REM theta activity enhances inhibitory control in typically developing children but not children with ADHD symptoms. Exp Brain Res 2017;235:1491–500. 10.1007/s00221-017-4906-7.
    1. Chabernaud C, Mennes M, Kelly C, Nooner K, Di Martino A, Castellanos FX, et al. Dimensional brain-behavior relationships in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 2012;71:434–42. 10.1016/j.biopsych.2011.08.013.
    1. Saletin JM, Coon WG, Carskadon MA. Stage 2 sleep EEG sigma activity and motor learning in childhood ADHD: a pilot study. J Clin Child Adolesc Psychol 2017;46:188–97. 10.1080/15374416.2016.1157756.
    1. Fogel SM, Ray LB, Binnie L, Owen AM. How to become an expert: A new perspective on the role of sleep in the mastery of procedural skills. Neurobiol Learn Mem 2015;125:236–48. 10.1016/j.nlm.2015.10.004.
    1. Blumberg MS, Marques HG, Iida F. Twitching in sensorimotor development from sleeping rats to robots. Curr Biol 2013;23:R532–7. 10.1016/j.cub.2013.04.075.
    1. Del Rio-Bermudez C, Blumberg MS. Active sleep promotes functional connectivity in developing sensorimotor networks. BioEssays 2018;40. 10.1002/bies.201700234.
    1. Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 2007;17:1582–94. 10.1093/cercor/bhl069.
    1. Zinke K, Wilhelm I, Bayramoglu M, Klein S, Born J. Children’s initial sleep-associated changes in motor skill are unrelated to long-term skill levels. Dev Sci 2017;20. 10.1111/desc.12463.
    1. Aslin RN, Newport EL. Statistical learning: from acquiring specific items to forming general rules. Curr Dir Psychol Sci 2012;21:170–6. 10.1177/0963721412436806.
    1. Gómez RL, Bootzin RR, Nadel L. Naps promote abstraction in language-learning infants. Psychol Sci 2006;17:670–4. 10.1111/j.1467-9280.2006.01764.x.
    1. Hupbach A, Gomez RL, Bootzin RR, Nadel L. Nap-dependent learning in infants. Dev Sci 2009;12:1007–12. 10.1111/j.1467-7687.2009.00837.x.
    1. Konrad C, Herbert JS, Schneider S, Seehagen S. Gist extraction and sleep in 12-month-old infants. Neurobiol Learn Mem 2016;134:216–20. 10.1016/j.nlm.2016.08.021.
    1. Ellenbogen JM, Payne JD, Stickgold R. The role of sleep in declarative memory consolidation: passive, permissive, active or none? Curr Opin Neurobiol 2006;16:716–22. 10.1016/j.conb.2006.10.006.
    1. González-Rueda A, Pedrosa V, Feord RC, Clopath C, Paulsen O. Activity-Dependent Downscaling of Subthreshold Synaptic Inputs during Slow-Wave-Sleep-like Activity In Vivo. Neuron 2018;97:1244–1252.e5. 10.1016/j.neuron.2018.01.047.
    1. Werchan DM, Gómez RL. Wakefulness (Not Sleep) Promotes Generalization of Word Learning in 2.5-Year-Old Children. Child Dev 2014;85:429–36. 10.1111/cdev.12149.
    1. Sandoval M, Leclerc JA, Gómez RL. Words to Sleep On: Naps facilitate verb generalization in habitually and nonhabitually napping preschoolers. Child Dev 2017;88:1615–28.
    1. Werchan DM, Kim J-S, Gómez RL. A daytime nap combined with nighttime sleep promotes learning in toddlers. J Exp Child Psychol 2021;202:105006. 10.1016/j.jecp.2020.105006.
    1. Cai DJ, Mednick SA, Harrison EM, Kanady JC, Mednick SC. REM, not incubation, improves creativity by priming associative networks. Proc Natl Acad Sci U S A 2009;106:10130–4. 10.1073/pnas.0900271106.
    1. Pereira SIR, Lewis PA. The differing roles of NREM and REM sleep in the slow enhancement of skills and schemas. Curr Opin Physiol 2020;15:82–8. 10.1016/j.cophys.2019.12.005.
    1. Bridi MCD, Aton SJ, Seibt J, Renouard L, Coleman T, Frank MG. Rapid eye movement sleep promotes cortical plasticity in the developing brain. Sci Adv 2015;1. 10.1126/sciadv.1500105.
    1. Blasi A, Mercure E, Lloyd-Fox S, Thomson A, Brammer M, Sauter D, et al. Early specialization for voice and emotion processing in the infant brain. Curr Biol 2011;21:1220–4. 10.1016/j.cub.2011.06.009.
    1. Graham AM, Fisher PA, Pfeifer JH. What sleeping babies hear: a functional MRI study of interparental conflict and infants’ emotion processing. Psychol Sci 2013;24:782–9. 10.1177/0956797612458803.
    1. Mindell JA, Leichman ES, DuMond C, Sadeh A. Sleep and social-emotional development in infants and toddlers. J Clin Child Adolesc Psychol 2017;46:236–46. 10.1080/15374416.2016.1188701.
    1. Kurdziel LBF, Kent J, Spencer RMC. Sleep-dependent enhancement of emotional memory in early childhood. Sci Rep 2018;8:1–10. 10.1038/s41598-018-30980-y.
    1. Cremone A, Kurdziel LBF, Fraticelli-Torres A, McDermott JM, Spencer RMC. Napping reduces emotional attention bias during early childhood. Dev Sci 2016;20:e12411. 10.1111/desc.12411.
    1. Berger RH, Miller AL, Seifer R, Cares SR, LeBourgeois MK. Acute sleep restriction effects on emotion responses in 30- to 36-month-old children. J Sleep Res 2012;21:235–46. 10.1111/j.1365-2869.2011.00962.x.
    1. Bolinger E, Born J, Zinke K. Sleep divergently affects cognitive and automatic emotional response in children. Neuropsychologia 2018;117:84–91. 10.1016/j.neuropsychologia.2018.05.015.
    1. Baran B, Pace-Schott EF, Ericson C, Spencer RMC. Processing of emotional reactivity and emotional memory over sleep. J Neurosci 2012;32:1035–42. 10.1523/JNEUROSCI.2532-11.2012.
    1. Jones BJ, Schultz KS, Adams S, Baran B, Spencer RMC. Emotional bias of sleep-dependent processing shifts from negative to positive with aging. Neurobiol Aging 2016;45:178–89. 10.1016/j.neurobiolaging.2016.05.019.
    1. Vriend JL, Davidson FD, Corkum PV, Rusak B, Chambers CT, McLaughlin EN. Manipulating sleep duration alters emotional functioning and cognitive performance in children. J Pediatr Psychol 2013;38:1058–69. 10.1093/jpepsy/jst033.
    1. Baum KT, Desai A, Field J, Miller LE, Rausch J, Beebe DW. Sleep restriction worsens mood and emotion regulation in adolescents. J Child Psychol Psychiatry Allied Discip 2014;55:180–90. 10.1111/jcpp.12125.
    1. Short MA, Louca M. Sleep deprivation leads to mood deficits in healthy adolescents. Sleep Med 2015;16:987–93. 10.1016/j.sleep.2015.03.007.
    1. Payne JD, Kensinger EA, Wamsley EJ, Spreng RN, Alger SE, Gibler K, et al. Napping and the selective consolidation of negative aspects of scenes. Emotion 2015;15:176–86. 10.1037/a0038683.
    1. Bennion KA, Payne JD, Kensinger EA. Selective Effects of Sleep on Emotional Memory: What Mechanisms Are Responsible? Transl Issues Psychol Sci 2015;1:79–88. 10.1037/tps0000019.
    1. Prehn-Kristensen A, Munz M, Molzow I, Wilhelm I, Wiesner CD, Baving L. Sleep promotes consolidation of emotional memory in healthy children but not in children with attention-deficit hyperactivity disorder. PLoS One 2013;8:e65098. 10.1371/journal.pone.0065098.
    1. Prehn-Kristensen A, Göder R, Fischer J, Wilhelm I, Seeck-Hirschner M, Aldenhoff J, et al. Reduced sleep-associated consolidation of declarative memory in attention-deficit/hyperactivity disorder. Sleep Med 2011;12:672–9. 10.1016/j.sleep.2010.10.010.
    1. Cao J, Herman AB, West GB, Poe G, Savage VM. Unraveling why we sleep: Quantitative analysis reveals abrupt transition from neural reorganization to repair in early development. vol. 6. 2020.
    1. Li W, Ma L, Yang G, Gan WB. REM sleep selectively prunes and maintains new synapses in development and learning. Nat Neurosci 2017;20:427–37. 10.1038/nn.4479.
    1. Huttenlocher PR. Dendritic and synaptic development in human cerebral cortex: Time course and critical periods. Dev Neuropsychol 1999;16:347–9. 10.1207/S15326942DN1603_12.
    1. Mindell JA, Sadeh A, Kwon R, Goh DYT. Cross-cultural differences in the sleep of preschool children. Sleep Med 2013;14:1283–9. 10.1016/j.sleep.2013.09.002.
    1. Sio UN, Monaghan P, Ormerod T. Sleep on it, but only if it is difficult: Effects of sleep on problem solving. Mem Cogn 2013;41:159–66. 10.3758/s13421-012-0256-7.
    1. Friedrich M, Wilhelm I, Mölle M, Born J, Friederici AD. The sleeping infant brain anticipates development. Curr Biol 2017;27:2374–2380.e3. 10.1016/j.cub.2017.06.070.
    1. Simon KNS, Werchan D, Goldstein MR, Sweeney L, Bootzin RR, Nadel L, et al. Sleep confers a benefit for retention of statistical language learning in 6.5 month old infants. Brain Lang 2017;167:3–12. 10.1016/j.bandl.2016.05.002.
    1. Horváth K, Liu S, Plunkett K. A daytime nap facilitates generalization of word meanings in young toddlers. Sleep 2016;39:203–7. 10.5665/sleep.5348.
    1. Friedrich M, Mölle M, Friederici AD, Born J. The reciprocal relation between sleep and memory in infancy: Memory-dependent adjustment of sleep spindles and spindle-dependent improvement of memories. Dev Sci 2019;22:e12743. 10.1111/desc.12743.

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