Sleep spindle‐related activity in the human EEG and its relation to general cognitive and learning abilities

Stage 2 sleep spindles have been previously viewed as useful markers for the development and integrity of the CNS and were more currently linked to ‘offline re‐processing’ of implicit as well as explicit memory traces. Additionally, it had been discussed if spindles might be related to a more general learning or cognitive ability. In the present multicentre study we examined the relationship of automatically detected slow (< 13 Hz) and fast (> 13 Hz) stage 2 sleep spindles with: (i) the Raven's Advanced Progressive Matrices (testing ‘general cognitive ability’); as well as (ii) the Wechsler Memory scale‐revised (evaluating memory in various subdomains). Forty‐eight healthy subjects slept three times (separated by 1 week) for a whole night in a sleep laboratory with complete polysomnographic montage. Whereas the first night only served adaptation and screening purposes, the two remaining nights were preceded either by an implicit mirror‐tracing or an explicit word‐pair association learning or (corresponding) control task. Robust relationships of slow and fast sleep spindles with both cognitive as well as memory abilities were found irrespectively of whether learning occurred before sleep. Based on the present findings we suggest that besides being involved in shaping neuronal networks after learning, sleep spindles do reflect important aspects of efficient cortical‐subcortical connectivity, and are thereby linked to cognitive‐ and memory‐related abilities alike.

[1]  Intelligence , 1836, The Medico-chirurgical review.

[2]  W. Zung.  A SELF-RATING DEPRESSION SCALE. , 1965, Archives of general psychiatry.

[3]  W W Zung,et al.  A rating instrument for anxiety disorders. , 1971, Psychosomatics.

[4]  E. Ornitz,et al.  Evolution of sleep spindles in childhood. , 1975, Electroencephalography and Clinical Neurophysiology.

[5]  C. Reynolds,et al.  Wechsler memory scale-revised , 1988 .

[6]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[7]  B Saletu,et al.  Automatic Sleep-Spindle Detection Procedure: Aspects of Reliability and Validity , 1994, Clinical EEG.

[8]  Carlyle T. Smith,et al.  Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students , 1994, Journal of sleep research.

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

[10]  P. Achermann,et al.  Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. , 1997, Electroencephalography and clinical neurophysiology.

[11]  Ian J. Deary,et al.  Neuroscience and human intelligence differences , 1997, Trends in Neurosciences.

[12]  P. Anderer,et al.  Topographic distribution of sleep spindles in young healthy subjects , 1997, Journal of sleep research.

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

[14]  M Steriade,et al.  Coalescence of sleep rhythms and their chronology in corticothalamic networks. , 1998, Sleep research online : SRO.

[15]  N. Birbaumer,et al.  Spatiotemporal organization of brain dynamics and intelligence: an EEG study in adolescents. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  Alfred Meier-Koll,et al.  Walking through a Maze Alters the Architecture of Sleep , 1999, Perceptual and motor skills.

[17]  S. Shinomiya,et al.  Development of Sleep Spindles in Young Children and Adolescents , 1999, Clinical EEG.

[18]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[19]  M. Steriade.  Coherent oscillations and short-term plasticity in corticothalamic networks , 1999, Trends in Neurosciences.

[20]  Newell,et al.  A neural basis for general intelligence , 2000, American journal of ophthalmology-glaucoma.

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

[22]  Tyrone D. Cannon,et al.  Genetic influences on brain structure , 2001, Nature Neuroscience.

[23]  G Klösch,et al.  Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex , 2001, Neuroscience.

[24]  Robert Plomin,et al.  Genetics and general cognitive ability (g) , 2002, Trends in Cognitive Sciences.

[25]  Wolfgang Klimesch,et al.  EEG alpha power and intelligence , 2002 .

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

[27]  J. Born,et al.  Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep , 2002, The Journal of Neuroscience.

[28]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[29]  R. Mark Gardiner.  Genetics and the electroencephalogram , 2002, Human Genetics.

[30]  P Achermann,et al.  Power and coherence of sleep spindle frequency activity following hemispheric stroke. , 2002, Brain : a journal of neurology.

[31]  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.

[32]  R. Nader,et al.  A Role For Stage 2 Sleep in Memory Processing , 2003 .

[33]  Pierre Maquet,et al.  Sleep and brain plasticity , 2003 .

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

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

[36]  Justin M Ream,et al.  Neural Basis of Spontaneous thought Processes , 2004, Cortex.

[37]  Jean-François Gagnon,et al.  Sleep and quantitative EEG in neurodegenerative disorders. , 2004, Journal of psychosomatic research.

[38]  P. Thompson,et al.  Neurobiology of intelligence: science and ethics , 2004, Nature Reviews Neuroscience.

[39]  P. Achermann,et al.  Development of the nocturnal sleep electroencephalogram in human infants. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

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

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

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

[43]  A. Schlögl,et al.  An E-Health Solution for Automatic Sleep Classification according to Rechtschaffen and Kales: Validation Study of the Somnolyzer 24 × 7 Utilizing the Siesta Database , 2005, Neuropsychobiology.