Sleep in children triggers rapid reorganization of memory-related brain processes

Behavioral evidence shows that sleep is crucial for the consolidation of declarative memories in children as in adults. However, the underlying cerebral mechanisms remain virtually unexplored. Using magnetoencephalography, we investigated in children (8.0-12.5years) the impact of sleep (90-minute nap) on the neurophysiological processes underlying the creation and consolidation of novel associations between unknown objects and their functions. Learning-dependent changes in brain activity were observed within hippocampal and parahippocampal regions, followed by sleep-dependent changes in the prefrontal cortex, whereas no equivalent change was observed after a similar period of wakeful rest. Hence, our results show that in school-age children a 90-minute daytime nap after learning is sufficient to trigger the reorganization of memory-related brain activity toward prefrontal areas, where it incorporates into pre-existing semantic knowledge. This functional reorganization process in children is similar to that observed in adults but occurs at a much faster rate, which may contribute to the development of the impressive learning skills that characterize childhood.

[1]  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.

[2]  V. Jaswal,et al.  Preschoolers favor the creator's label when reasoning about an artifact's function , 2006, Cognition.

[3]  Karl J. Friston,et al.  Applications of random field theory to electrophysiology , 2005, Neuroscience Letters.

[4]  Evelyne Balteau,et al.  Sleep Modulates the Neural Substrates of Both Spatial and Contextual Memory Consolidation , 2008, PloS one.

[5]  Maria Pia Viggiano,et al.  The effect of a daytime nap on priming and recognition tasks in preschool children. , 2014, Sleep.

[6]  Karl J. Friston,et al.  Canonical Source Reconstruction for MEG , 2007, Comput. Intell. Neurosci..

[7]  S. Taulu,et al.  Presentation of electromagnetic multichannel data: The signal space separation method , 2005 .

[8]  P. Peigneux,et al.  Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood , 2015, Epilepsy & Behavior.

[9]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

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

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

[12]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[13]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

[14]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  Karl J. Friston,et al.  Bayesian decoding of brain images , 2008, NeuroImage.

[16]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[17]  A. Chesson,et al.  The American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications , 2007 .

[18]  Giulio Tononi,et al.  Characteristics of sleep slow waves in children and adolescents. , 2010, Sleep.

[19]  H Eichenbaum,et al.  Memory for items and memory for relations in the procedural/declarative memory framework. , 1997, Memory.

[20]  Jan Born,et al.  Immediate as well as delayed post learning sleep but not wakefulness enhances declarative memory consolidation in children , 2008, Neurobiology of Learning and Memory.

[21]  Hubert Preissl,et al.  Source Reconstruction Accuracy of MEG and EEG Bayesian Inversion Approaches , 2012, PloS one.

[22]  Sidarta Ribeiro,et al.  Naps in school can enhance the duration of declarative memories learned by adolescents , 2014, Front. Syst. Neurosci..

[23]  Jan Born,et al.  Sleep-dependent consolidation of procedural motor memories in children and adults: the pre-sleep level of performance matters. , 2012, Developmental science.

[24]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

[25]  John D E Gabrieli,et al.  The Development of Brain Systems Associated with Successful Memory Retrieval of Scenes , 2012, The Journal of Neuroscience.

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

[27]  Mathieu Bourguignon,et al.  MEG Correlates of Learning Novel Objects Properties in Children , 2013, PloS one.

[28]  H. Eichenbaum,et al.  The Neurophysiology of Memory , 2000, Annals of the New York Academy of Sciences.

[29]  Junrrs F. Kri.  Recognizing Words, Pictures, and Concepts: A Comparison of Lexical, Object, and Reality Decisions , 1984 .

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

[31]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[32]  Reto Huber,et al.  Sleep, synaptic connectivity, and hippocampal memory during early development , 2014, Trends in Cognitive Sciences.

[33]  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.

[34]  J. Born,et al.  Labile or stable: opposing consequences for memory when reactivated during waking and sleep , 2011, Nature Neuroscience.

[35]  C. Degueldre,et al.  Sleep after spatial learning promotes covert reorganization of brain activity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  B W Ellis,et al.  The St. Mary's Hospital sleep questionnaire: a study of reliability. , 1981, Sleep.

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

[38]  Axel Cleeremans,et al.  Sleep-dependent Neurophysiological Processes in Implicit Sequence Learning , 2013, Journal of Cognitive Neuroscience.

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

[40]  P. Peigneux,et al.  Pathophysiology of sleep-dependent memory consolidation processes in children. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[42]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[43]  Karl J. Friston,et al.  MEG source localization under multiple constraints: An extended Bayesian framework , 2006, NeuroImage.

[44]  Manuel Munz,et al.  Sleep restores daytime deficits in procedural memory in children with attention-deficit/hyperactivity disorder. , 2011, Research in developmental disabilities.

[45]  Erkki Oja,et al.  Independent component approach to the analysis of EEG and MEG recordings , 2000, IEEE Transactions on Biomedical Engineering.

[46]  Jan Born,et al.  Sleep's function in the spontaneous recovery and consolidation of memories. , 2007, Journal of experimental psychology. General.

[47]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[48]  Eve V. Clark,et al.  Language and Conceptual Development series How language acquisition builds on cognitive development , 2004 .

[49]  Patrick Van Bogaert,et al.  Is sleep-related consolidation impaired in focal idiopathic epilepsies of childhood? A pilot study , 2011, Epilepsy & Behavior.

[50]  O. Bruni,et al.  The Sleep Disturbance Scale for Children (SDSC) Construct ion and validation of an instrument to evaluate sleep disturbances in childhood and adolescence , 1996, Journal of sleep research.

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

[52]  Andreas Buchmann,et al.  Mapping the electrophysiological marker of sleep depth reveals skill maturation in children and adolescents , 2012, NeuroImage.

[53]  Manuel Schabus,et al.  Sleep transforms the cerebral trace of declarative memories , 2007, Proceedings of the National Academy of Sciences.

[54]  Guillén Fernández,et al.  Shift from Hippocampal to Neocortical Centered Retrieval Network with Consolidation , 2009, The Journal of Neuroscience.

[55]  Seppo P. Ahlfors,et al.  Head movements of children in MEG: Quantification, effects on source estimation, and compensation , 2008, NeuroImage.

[56]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

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

[58]  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.

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

[60]  G. Nolte.  The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

[61]  D. Jean,et al.  Random-effect analysis. , 2014 .