Sleep Spindle Density Predicts the Effect of Prior Knowledge on Memory Consolidation

Information that relates to a prior knowledge schema is remembered better and consolidates more rapidly than information that does not. Another factor that influences memory consolidation is sleep and growing evidence suggests that sleep-related processing is important for integration with existing knowledge. Here, we perform an examination of how sleep-related mechanisms interact with schema-dependent memory advantage. Participants first established a schema over 2 weeks. Next, they encoded new facts, which were either related to the schema or completely unrelated. After a 24 h retention interval, including a night of sleep, which we monitored with polysomnography, participants encoded a second set of facts. Finally, memory for all facts was tested in a functional magnetic resonance imaging scanner. Behaviorally, sleep spindle density predicted an increase of the schema benefit to memory across the retention interval. Higher spindle densities were associated with reduced decay of schema-related memories. Functionally, spindle density predicted increased disengagement of the hippocampus across 24 h for schema-related memories only. Together, these results suggest that sleep spindle activity is associated with the effect of prior knowledge on memory consolidation. SIGNIFICANCE STATEMENT Episodic memories are gradually assimilated into long-term memory and this process is strongly influenced by sleep. The consolidation of new information is also influenced by its relationship to existing knowledge structures, or schemas, but the role of sleep in such schema-related consolidation is unknown. We show that sleep spindle density predicts the extent to which schemas influence the consolidation of related facts. This is the first evidence that sleep is associated with the interaction between prior knowledge and long-term memory formation.

[1]  M. Ferrara,et al.  Sleep spindles: an overview. , 2003, Sleep medicine reviews.

[2]  Ronald E. Johnson Recall of prose as a function of the structural importance of the linguistic units. , 1970 .

[3]  M. Hasselmo Neuromodulation: acetylcholine and memory consolidation , 1999, Trends in Cognitive Sciences.

[4]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[5]  Philippe Peigneux,et al.  Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping , 2006, The Journal of Neuroscience.

[6]  B. Rasch,et al.  Differential Effects of Non-REM and REM Sleep on Memory Consolidation? , 2014, Current Neurology and Neuroscience Reports.

[7]  P. Lewis,et al.  Schema-conformant memories are preferentially consolidated during REM sleep , 2015, Neurobiology of Learning and Memory.

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

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

[10]  Marijn C. W. Kroes,et al.  Initial Investigation of the Effects of an Experimentally Learned Schema on Spatial Associative Memory in Humans , 2014, The Journal of Neuroscience.

[11]  Marvin Minsky,et al.  A framework for representing knowledge , 1974 .

[12]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[13]  N. S. Johnson,et al.  Remembrance of things parsed: Story structure and recall , 1977, Cognitive Psychology.

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

[15]  Manuel Schabus,et al.  Sleep spindles and their significance for declarative memory consolidation. , 2004, Sleep.

[16]  R. Henson,et al.  How schema and novelty augment memory formation , 2012, Trends in Neurosciences.

[17]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[18]  Hartwig R. Siebner,et al.  Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations , 2012, NeuroImage.

[19]  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.

[20]  M. Czisch,et al.  Sleep Spindles and Hippocampal Functional Connectivity in Human NREM Sleep , 2011, The Journal of Neuroscience.

[21]  Peter Achermann,et al.  Individual ‘Fingerprints’ in Human Sleep EEG Topography , 2001, Neuropsychopharmacology.

[22]  J. Csicsvari,et al.  Communication between neocortex and hippocampus during sleep in rodents , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

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

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

[26]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

[27]  G. A. Kerkkof Differences between morning-types and evening-types in the dynamics of EEG slow wave activity during night sleep , 1991 .

[28]  Maxim Bazhenov,et al.  Short‐ and medium‐term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo , 2002, The Journal of physiology.

[29]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[30]  M. Walker,et al.  Daytime Naps, Motor Memory Consolidation and Regionally Specific Sleep Spindles , 2007, PloS one.

[31]  Fabrizio Vecchio,et al.  An electroencephalographic fingerprint of human sleep , 2005, NeuroImage.

[32]  G. Fernández,et al.  Retrieval of Associative Information Congruent with Prior Knowledge Is Related to Increased Medial Prefrontal Activity and Connectivity , 2010, The Journal of Neuroscience.

[33]  G. Tononi,et al.  Reduced sleep spindle activity in schizophrenia patients. , 2007, The American journal of psychiatry.

[34]  Manuel Schabus,et al.  Sleep spindle‐related activity in the human EEG and its relation to general cognitive and learning abilities , 2006, The European journal of neuroscience.

[35]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[36]  Ulman Lindenberger,et al.  Differences in the neural signature of remembering schema-congruent and schema-incongruent events , 2015, NeuroImage.

[37]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[38]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[39]  John Van Sickle,et al.  ANALYZING CORRELATIONS BETWEEN STREAM AND WATERSHED ATTRIBUTES 1 , 2003 .

[40]  G. Vining,et al.  Data Analysis: A Model-Comparison Approach , 1989 .

[41]  Marvin Minsky,et al.  A framework for representing knowledge" in the psychology of computer vision , 1975 .

[42]  M. Walker,et al.  Sleep and Emotional Memory Processing. , 2011, Sleep medicine clinics.

[43]  P. Achermann,et al.  The Multidimensional Aspects of Sleep Spindles and Their Relationship to Word-Pair Memory Consolidation. , 2015, Sleep.

[44]  J. Born,et al.  Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. , 2006, Journal of neurophysiology.

[45]  Herbert A. Simon,et al.  THE MIND'S EYE IN CHESS , 1988 .

[46]  S. Sara,et al.  Hippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory , 2009, PLoS ONE.

[47]  E. Bigand,et al.  Music, emotion, and time perception: the influence of subjective emotional valence and arousal? , 2013, Front. Psychol..

[48]  Jennifer R. Ramautar,et al.  Individual Differences in White Matter Diffusion Affect Sleep Oscillations , 2013, The Journal of Neuroscience.

[49]  J. Wixted The psychology and neuroscience of forgetting. , 2004, Annual review of psychology.

[50]  Björn Rasch,et al.  No Associations between Interindividual Differences in Sleep Parameters and Episodic Memory Consolidation. , 2015, Sleep.

[51]  G. Kerkhof Differences between morning-types and evening-types in the dynamics of EEG slow wave activity during night sleep. , 1991, Electroencephalography and clinical neurophysiology.

[52]  D. Rumelhart Schemata: The Building Blocks of Cognition , 2017 .

[53]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[54]  C. Smith,et al.  Sleep spindles and learning potential. , 2007, Behavioral neuroscience.

[55]  Elizabeth A. McDevitt,et al.  REM sleep rescues learning from interference , 2015, Neurobiology of Learning and Memory.

[56]  Justin C. Hulbert,et al.  Interfering with Theories of Sleep and Memory: Sleep, Declarative Memory, and Associative Interference , 2006, Current Biology.

[57]  Elizabeth A. McDevitt,et al.  The Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study , 2013, The Journal of Neuroscience.

[58]  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.

[59]  Marijn C. W. Kroes,et al.  Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? , 2014, Trends in Neurosciences.

[60]  Z. Clemens,et al.  Prediction of general mental ability based on neural oscillation measures of sleep , 2005, Journal of sleep research.

[61]  Guillén Fernández,et al.  Building on Prior Knowledge: Schema-dependent Encoding Processes Relate to Academic Performance , 2014, Journal of Cognitive Neuroscience.

[62]  Mario Rosanova,et al.  Pattern-Specific Associative Long-Term Potentiation Induced by a Sleep Spindle-Related Spike Train , 2005, The Journal of Neuroscience.

[63]  S. A. Kiem,et al.  Effects of rapid eye movement sleep deprivation on fear extinction recall and prediction error signaling , 2012, Human brain mapping.

[64]  Manuel Schabus,et al.  Interindividual sleep spindle differences and their relation to learning-related enhancements , 2008, Brain Research.

[65]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

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

[67]  Carlyle T. Smith,et al.  The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation , 2011, Neuroscience & Biobehavioral Reviews.

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

[69]  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 .

[70]  Marcia K. Johnson,et al.  Contextual prerequisites for understanding: Some investigations of comprehension and recall , 1972 .

[71]  Adrián Pótári,et al.  Sleep Spindles and Intelligence: Evidence for a Sexual Dimorphism , 2014, The Journal of Neuroscience.

[72]  F. Bartlett,et al.  Remembering: A Study in Experimental and Social Psychology , 1932 .

[73]  Guillén Fernández,et al.  Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans , 2010, Proceedings of the National Academy of Sciences.

[74]  S. Brent Linguistic unity, list length, and rate of presentation in serial anticipation learning , 1969 .

[75]  J. Born,et al.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. , 2007, Brain : a journal of neurology.

[76]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

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

[78]  P. Achermann,et al.  Trait-like individual differences in the human sleep electroencephalogram , 2006, Neuroscience.