Consolidation of vocabulary during sleep: The rich get richer?

HighlightsDifferent neural mechanisms may support word learning in children and adults.Children show larger proportions of slow‐wave sleep that supports consolidation.Consolidation in adults can benefit from richer existing knowledge.Meta‐analysis suggests extant vocabulary is associated with new word consolidation.Directions for uncovering prior knowledge influences on consolidation are proposed. ABSTRACT Sleep plays a role in strengthening new words and integrating them with existing vocabulary knowledge, consistent with neural models of learning in which sleep supports hippocampal transfer to neocortical memory. Such models are based on adult research, yet neural maturation may mean that the mechanisms supporting word learning vary across development. Here, we propose a model in which children may capitalise on larger amounts of slow‐wave sleep to support a greater demand on learning and neural reorganisation, whereas adults may benefit from a richer knowledge base to support consolidation. Such an argument is reinforced by the well‐reported “Matthew effect”, whereby rich vocabulary knowledge is associated with better acquisition of new vocabulary. We present a meta‐analysis that supports this association between children's existing vocabulary knowledge and their integration of new words overnight. Whilst multiple mechanisms likely contribute to vocabulary consolidation and neural reorganisation across the lifespan, we propose that contributions of existing knowledge should be rigorously examined in developmental studies. Such research has potential to greatly enhance neural models of learning.

[1]  Dana M. DeMaster,et al.  Developmental Differences in Medial Temporal Lobe Function during Memory Encoding , 2010, The Journal of Neuroscience.

[2]  I. Wilhelm,et al.  Sleep Slow-Wave Activity Reveals Developmental Changes in Experience-Dependent Plasticity , 2014, The Journal of Neuroscience.

[3]  J. Born,et al.  The contribution of sleep to hippocampus-dependent memory consolidation , 2007, Trends in Cognitive Sciences.

[4]  Régine Kolinsky,et al.  The metamorphosis of the statistical segmentation output: Lexicalization during artificial language learning , 2009, Cognition.

[5]  Rebecca L Gómez,et al.  Sleep as a window into early neural development: Shifts in sleep-dependent learning effects across early childhood. , 2015, Child development perspectives.

[6]  G. Winocur,et al.  Systems consolidation and hippocampus: two views , 2007 .

[7]  Timothy O. Laumann,et al.  At the nexus of neuroscience and education , 2012, Developmental Cognitive Neuroscience.

[8]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[9]  Rebecca L. Gómez,et al.  Naps Promote Abstraction in Language-Learning Infants , 2006, Psychological science.

[10]  L. Henderson,et al.  Consolidation of vocabulary is associated with sleep in children. , 2012, Developmental science.

[11]  Matthew H. Davis,et al.  Long-term priming of the meanings of ambiguous words , 2013 .

[12]  Jessica S. Horst,et al.  Goodnight book: sleep consolidation improves word learning via storybooks , 2014, Front. Psychol..

[13]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[14]  C. Guilleminault,et al.  Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. , 2004, Sleep.

[15]  J Bruce Tomblin,et al.  Prevalence and Nature of Late-Emerging Poor Readers. , 2012, Journal of educational psychology.

[16]  Ole Jensen,et al.  Sleep Promotes the Extraction of Grammatical Rules , 2013, PloS one.

[17]  E. Knudsen Sensitive Periods in the Development of the Brain and Behavior , 2004, Journal of Cognitive Neuroscience.

[18]  B. Rasch,et al.  Auditory feedback blocks memory benefits of cueing during sleep , 2015, Nature Communications.

[19]  J. Montplaisir,et al.  Sleep spindle characteristics in healthy subjects of different age groups , 2001, Clinical Neurophysiology.

[20]  J. Born,et al.  Boosting slow oscillations during sleep potentiates memory , 2006, Nature.

[21]  Aize Cao,et al.  Not All Reading Disabilities Are Dyslexia: Distinct Neurobiology of Specific Comprehension Deficits , 2013, Brain Connect..

[22]  B. Rasch,et al.  The beneficial role of memory reactivation for language learning during sleep: A review , 2017, Brain and Language.

[23]  A. Sadeh,et al.  Sleep in children with attention-deficit hyperactivity disorder: a meta-analysis of polysomnographic studies. , 2006, Sleep medicine reviews.

[24]  Monika Schönauer,et al.  Sleep-mediated memory consolidation depends on the level of integration at encoding , 2017, Neurobiology of Learning and Memory.

[25]  Matthew H. Davis,et al.  A complementary systems account of word learning: neural and behavioural evidence , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  M. Carskadon,et al.  Spectral analysis of the sleep electroencephalogram during adolescence. , 2004, Sleep.

[27]  Mathieu Bourguignon,et al.  Sleep in children triggers rapid reorganization of memory-related brain processes , 2016, NeuroImage.

[28]  I. Wilhelm,et al.  Reduced sleep-associated consolidation of declarative memory in attention-deficit/hyperactivity disorder. , 2011, Sleep medicine.

[29]  James M. McQueen,et al.  Competition from unseen or unheard novel words: Lexical consolidation across modalities , 2014 .

[30]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[31]  K. Paller,et al.  Sleep-based memory processing facilitates grammatical generalization: Evidence from targeted memory reactivation , 2017, Brain and Language.

[32]  K. Plunkett,et al.  A Daytime Nap Facilitates Generalization of Word Meanings in Young Toddlers. , 2016, Sleep.

[33]  M. Gareth Gaskell,et al.  A Day in the Life of a Spoken Word , 2004 .

[34]  A. Sims Tamas Pataki's (2014) “Wish-fulfillment in philosophy and psychoanalysis” , 2014, Front. Psychol..

[35]  Jane Oakhill,et al.  Matthew Effects in Young Readers , 2011, Journal of learning disabilities.

[36]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[37]  J. Rapoport,et al.  Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years , 1995, The Journal of comparative neurology.

[38]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[39]  Jill R. Hoover,et al.  The influence of part-word phonotactic probability/neighborhood density on word learning by preschool children varying in expressive vocabulary. , 2011, Journal of child language.

[40]  Efthymia C. Kapnoula,et al.  Learning and integration of new word-forms: Consolidation, pruning, and the emergence of automaticity , 2016 .

[41]  Margaret J. Snowling,et al.  Dissecting the relationship between language skills and learning to read: Semantic and phonological contributions to new vocabulary learning in children with poor reading comprehension , 2007 .

[42]  B. McNaughton,et al.  Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[43]  B. Staresina,et al.  Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep , 2015, Nature Neuroscience.

[44]  Joshua B. Tenenbaum,et al.  The Large-Scale Structure of Semantic Networks: Statistical Analyses and a Model of Semantic Growth , 2001, Cogn. Sci..

[45]  Thomas T. Hills,et al.  Longitudinal Analysis of Early Semantic Networks , 2009, Psychological science.

[46]  Arielle Borovsky,et al.  Lexical leverage: category knowledge boosts real-time novel word recognition in 2-year-olds. , 2016, Developmental science.

[47]  Christian Büchel,et al.  The sleeping child outplays the adult's capacity to convert implicit into explicit knowledge , 2013, Nature Neuroscience.

[48]  R. Huber,et al.  EEG sleep slow-wave activity as a mirror of cortical maturation. , 2011, Cerebral cortex.

[49]  James L. McClelland Incorporating rapid neocortical learning of new schema-consistent information into complementary learning systems theory. , 2013, Journal of experimental psychology. General.

[50]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[51]  R. Stickgold,et al.  Sleep Dependent Memory Consolidation in Children with Autism Spectrum Disorder. , 2014, Sleep.

[52]  M. Gareth Gaskell,et al.  Does Sleep Improve Your Grammar? Preferential Consolidation of Arbitrary Components of New Linguistic Knowledge , 2016, PloS one.

[53]  Angela D. Friederici,et al.  Generalization of word meanings during infant sleep , 2015, Nature Communications.

[54]  C. Norbury,et al.  Learning and consolidation of new spoken words in autism spectrum disorder. , 2014, Developmental science.

[55]  K. Plunkett,et al.  Napping facilitates word learning in early lexical development , 2015, Journal of sleep research.

[56]  J. Born,et al.  Sleep after learning aids memory recall. , 2006, Learning & memory.

[57]  B. Rasch,et al.  Boosting Vocabulary Learning by Verbal Cueing During Sleep. , 2015, Cerebral cortex.

[58]  Matthew H. Davis,et al.  The role of memory consolidation in generalisation of new linguistic information , 2012, Cognition.

[59]  Lisa M. Henderson,et al.  Learning new vocabulary during childhood: effects of semantic training on lexical consolidation and integration. , 2013, Journal of experimental child psychology.

[60]  P. Lewis,et al.  Overlapping memory replay during sleep builds cognitive schemata , 2011, Trends in Cognitive Sciences.

[61]  D. Amaral,et al.  Assessing hippocampal development and language in early childhood: Evidence from a new application of the Automatic Segmentation Adapter Tool , 2015, Human brain mapping.

[62]  M. Gaskell,et al.  Markers of automaticity in sleep-associated consolidation of novel words , 2015, Neuropsychologia.

[63]  H. Catts,et al.  Developmental Relationships Between Language and Reading: Reconciling a Beautiful Hypothesis With Some Ugly Facts , 2005 .

[64]  I. Wilhelm,et al.  Memory cueing during sleep modifies the interpretation of ambiguous scenes in adolescents and adults , 2015, Developmental Cognitive Neuroscience.

[65]  Jeffrey S Bowers,et al.  Teaching adults new words: the role of practice and consolidation. , 2007, Journal of experimental psychology. Learning, memory, and cognition.

[66]  S. Ghetti,et al.  Developmental differences in hippocampal and cortical contributions to episodic retrieval , 2013, Cortex.

[67]  W. Stone,et al.  Characterizing sleep in children with autism spectrum disorders: a multidimensional approach. , 2006, Sleep.

[68]  I. Wilhelm,et al.  Sleep-dependent memory consolidation – What can be learnt from children? , 2012, Neuroscience & Biobehavioral Reviews.

[69]  Paul J. Reber,et al.  Sleep facilitates learning a new linguistic rule , 2014, Neuropsychologia.

[70]  Thomas Martinetz,et al.  Driving Sleep Slow Oscillations by Auditory Closed-Loop Stimulation—A Self-Limiting Process , 2015, The Journal of Neuroscience.

[71]  Ylva Østby,et al.  Dissociating memory processes in the developing brain: the role of hippocampal volume and cortical thickness in recall after minutes versus days. , 2012, Cerebral cortex.

[72]  Annette Karmiloff-Smith,et al.  Sleep enhances memory consolidation in children , 2014, Journal of sleep research.

[73]  A. Samuel,et al.  Lexical configuration and lexical engagement: When adults learn new words , 2007, Cognitive Psychology.

[74]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[75]  Jessica S. Horst,et al.  Learning What to Remember: Vocabulary Knowledge and Children's Memory for Object Names and Features. , 2016 .

[76]  J. Born,et al.  Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory , 2013, Neuron.

[77]  Matthew H. Davis,et al.  Learning and Consolidation of Novel Spoken Words , 2009, Journal of Cognitive Neuroscience.

[78]  Susan E. Stothard,et al.  A comparison of phonological skills in children with reading comprehension difficulties and children with decoding difficulties. , 1995, Journal of child psychology and psychiatry, and allied disciplines.

[79]  Kiralee M. Hayashi,et al.  Dynamic mapping of normal human hippocampal development , 2006, Hippocampus.

[80]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[81]  Margaret J. Snowling,et al.  Semantic processing and the development of word-recognition skills: Evidence from children with reading comprehension difficulties. , 1998 .

[82]  Erica H. Wojcik,et al.  Remembering New Words: Integrating Early Memory Development into Word Learning , 2013, Front. Psychol..

[83]  Susanne Diekelmann,et al.  Sleep in children improves memory performance on declarative but not procedural tasks. , 2008, Learning & memory.

[84]  A. Karmiloff-Smith,et al.  Impaired sleep-related learning in children with Williams Syndrome , 2013 .

[85]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[86]  Tobias Sommer,et al.  The Emergence of Knowledge and How it Supports the Memory for Novel Related Information , 2016, Cerebral cortex.

[87]  Matthew A Lambon Ralph,et al.  Sleep Spindle Density Predicts the Effect of Prior Knowledge on Memory Consolidation , 2016, The Journal of Neuroscience.

[88]  J. Born,et al.  Learning-Dependent Increases in Sleep Spindle Density , 2002, The Journal of Neuroscience.

[89]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[90]  Sharon L. Thompson-Schill,et al.  Fast mapping rapidly integrates information into existing memory networks. , 2014, Journal of experimental psychology. General.

[91]  M. Styner,et al.  Longitudinal development of cortical and subcortical gray matter from birth to 2 years. , 2012, Cerebral cortex.

[92]  Denise M Werchan,et al.  Wakefulness (not sleep) promotes generalization of word learning in 2.5-year-old children. , 2014, Child development.

[93]  Irwin Feinberg,et al.  Sleep EEG changes during adolescence: An index of a fundamental brain reorganization , 2010, Brain and Cognition.

[94]  Dorothy V. M. Bishop,et al.  Investigating orthographic and semantic aspects of word learning in poor comprehenders , 2008 .

[95]  Benjamin Thyreau,et al.  Sleep duration during weekdays affects hippocampal gray matter volume in healthy children , 2012, NeuroImage.

[96]  Anders M. Fjell,et al.  Heterogeneity in Subcortical Brain Development: A Structural Magnetic Resonance Imaging Study of Brain Maturation from 8 to 30 Years , 2009, The Journal of Neuroscience.

[97]  B. Nolan Boosting slow oscillations during sleep potentiates memory , 2008 .

[98]  M. L. Lambon Ralph,et al.  The Role of Sleep Spindles and Slow-Wave Activity in Integrating New Information in Semantic Memory , 2013, The Journal of Neuroscience.

[99]  S. Mattys,et al.  Lexical activity in speech processing: Evidence from pause detection , 2002 .

[100]  Nicholas B. Turk-Browne,et al.  Hippocampal Structure Predicts Statistical Learning and Associative Inference Abilities during Development , 2017, Journal of Cognitive Neuroscience.

[101]  A. Hupbach,et al.  Nap-dependent learning in infants. , 2009, Developmental science.

[102]  K. Stanovich Matthew Effects in Reading: Some Consequences of Individual Differences in the Acquisition of Literacy , 2009 .

[103]  Ronn Carpenter,et al.  Characterizing ℎ(Ω) , 1975 .

[104]  Silvia A. Bunge,et al.  Neural changes underlying the development of episodic memory during middle childhood , 2012, Developmental Cognitive Neuroscience.

[105]  William D. Marslen-Wilson,et al.  Integrating Form and Meaning: A Distributed Model of Speech Perception. , 1997 .

[106]  Lisa M. Henderson,et al.  When the daffodat flew to the intergalactic zoo: off-line consolidation is critical for word learning from stories. , 2015, Developmental psychology.

[107]  J. Born,et al.  The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats , 2009, The European journal of neuroscience.

[108]  B. Rasch,et al.  Cueing vocabulary in awake subjects during the day has no effect on memory , 2015, Somnologie - Schlafforschung und Schlafmedizin.

[109]  James L. McClelland,et al.  Generalization Through the Recurrent Interaction of Episodic Memories , 2012, Psychological review.

[110]  Maya Ringli,et al.  Mapping of Cortical Activity in the First Two Decades of Life: A High-Density Sleep Electroencephalogram Study , 2010, The Journal of Neuroscience.

[111]  Lisa M. Henderson,et al.  Eye-tracking the time‐course of novel word learning and lexical competition in adults and children , 2017, Brain and Language.

[112]  G. Buzsáki,et al.  Interaction between neocortical and hippocampal networks via slow oscillations. , 2005, Thalamus & related systems.

[113]  Robert Stickgold,et al.  Sleep Spindle Activity is Associated with the Integration of New Memories and Existing Knowledge , 2010, The Journal of Neuroscience.

[114]  C. Houston-Price,et al.  Once upon a time, there was a pulchritudinous princess . . .: The role of word definitions and multiple story contexts in children's learning of difficult vocabulary , 2012, Applied Psycholinguistics.

[115]  K. Stanovich Does reading make you smarter? Literacy and the development of verbal intelligence. , 1993, Advances in child development and behavior.

[116]  M. Gaskell,et al.  Sleep-Associated Changes in the Mental Representation of Spoken Words , 2007, Psychological science.

[117]  J. Born,et al.  Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[118]  Guillén Fernández,et al.  Consolidation Differentially Modulates Schema Effects on Memory for Items and Associations , 2013, PloS one.

[119]  G. Gaskell,et al.  Online lexical competition during spoken word recognition and word learning in children and adults. , 2013, Child development.