Developmental changes in brain connectivity assessed using the sleep EEG

Adolescence represents a time of significant cortical restructuring. Current theories posit that during this period connections between frequently utilized neural networks are strengthened while underutilized synaptic connections are discarded. The aim of the present study was to examine the developmental evolution of connectivity between brain regions using the sleep EEG. All-night sleep EEG recordings in two longitudinal cohorts (children and teens) followed at 1.5-3 year intervals and one cross-sectional cohort (adults) were analyzed. The children and teen cohorts were 9/10 and 15/16 years at the initial assessment; ages of the adults were 20 to 23 years. Intrahemispheric, interhemispheric, and diagonal coherence was measured between all six possible pairings of two central (C3/A2 and C4/A1) and two occipital (O2/A1 and O1/A2) derivations during slow wave, stage 2, and, REM sleep. Within-subjects analyses were performed for the children and teen cohorts, and a linear regression analysis was performed across every assessment of all cohorts. Within-subject analyses revealed a maturational increase in coherence for both age cohorts, though the frequencies, sleep states, and regions differed between cohorts. Regression analysis across all age cohorts showed an overall linear increase in left and right intrahemispheric coherence for all sleep states across frequencies. Furthermore, coherence between diagonal electrode pairs also increased in a linear manner for stage 2 and REM sleep. No age-related trend was found in interhemispheric coherence. Our results indicate that sleep EEG coherence increases with age and that these increases are confined to specific brain regions. This analysis highlights the utility of the sleep EEG to measure developmental changes in brain maturation.

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

[2]  R. Barry,et al.  Age and gender effects in EEG coherence: I. Developmental trends in normal children , 2004, Clinical Neurophysiology.

[3]  P. Nunez.  Toward a quantitative description of large-scale neocortical dynamic function and EEG , 2000, Behavioral and Brain Sciences.

[4]  M. Knyazeva,et al.  The EEG in acallosal children. Coherence values in the resting state: left hemisphere compensatory mechanism? , 1995, Electroencephalography and clinical neurophysiology.

[5]  I. Fried,et al.  Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex , 2008, Nature Neuroscience.

[6]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[7]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[8]  Robert W. Thatcher,et al.  Cyclic cortical reorganization during early childhood , 1992, Brain and Cognition.

[9]  D. Lindsley,et al.  The human brain in figures and tables : a quantitative handbook , 1968 .

[10]  T. Gasser,et al.  Development of the EEG of school-age children and adolescents. I. Analysis of band power. , 1988, Electroencephalography and clinical neurophysiology.

[11]  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.

[12]  James M. Tanner,et al.  Growth at Adolescence , 1956 .

[13]  P. Huttenlocher.  Synapse elimination and plasticity in developing human cerebral cortex. , 1984, American journal of mental deficiency.

[14]  R. Armitage,et al.  Sleep Microarchitecture in Childhood and Adolescent Depression: Temporal Coherence , 2006, Clinical EEG and neuroscience.

[15]  J. Carrier,et al.  Age‐related modifications of NREM sleep EEG: from childhood to middle age , 2001, Journal of sleep research.

[16]  Michael C. Stevens,et al.  The developmental cognitive neuroscience of functional connectivity , 2009, Brain and Cognition.

[17]  Vincent J Schmithorst,et al.  Development of effective connectivity for narrative comprehension in children , 2007, Neuroreport.

[18]  T. Sejnowski,et al.  Irresistible environment meets immovable neurons , 1997, Behavioral and Brain Sciences.

[19]  Wolf Singer,et al.  Distributed processing and temporal codes in neuronal networks , 2009, Cognitive Neurodynamics.

[20]  I. Feinberg,et al.  Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? , 1982, Journal of psychiatric research.

[21]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[22]  Visualization of maturation of the corpus callosum during childhood and adolescence using T2 relaxometry , 2007, International Journal of Developmental Neuroscience.

[23]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

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

[25]  P. Achermann,et al.  Coherence analysis of the human sleep electroencephalogram , 1998, Neuroscience.

[26]  Khader M. Hasan,et al.  White matter development during late adolescence in healthy males: A cross-sectional diffusion tensor imaging study , 2007, NeuroImage.

[27]  Jan Karbowski,et al.  How Does Connectivity Between Cortical Areas Depend on Brain Size? Implications for Efficient Computation , 2003, Journal of Computational Neuroscience.

[28]  I Tobler,et al.  Interhemispheric coherence of the sleep electroencephalogram in mice with congenital callosal dysgenesis , 2004, Neuroscience.

[29]  M. Carskadon,et al.  Developmental changes in the human sleep EEG during early adolescence. , 2010, Sleep.

[30]  Braitenberg,et al.  The Human Cortical White Matter: Quantitative Aspects of Cortico-Cortical Long-Range Connectivity , 2002 .

[31]  John P. Allen,et al.  Measuring Alcohol Consumption: Psychosocial and Biochemical Methods , 1992 .

[32]  E. Harth,et al.  Electric Fields of the Brain: The Neurophysics of Eeg , 2005 .

[33]  A. Schüz.  Cortical areas : unity and diversity , 2002 .

[34]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  D.G.M. Dijk,et al.  Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[37]  M. Brazier,et al.  Architectonics of the cerebral cortex , 1978 .

[38]  R. Thatcher,et al.  Human cerebral hemispheres develop at different rates and ages. , 1987, Science.

[39]  Kiralee M. Hayashi,et al.  Dynamically spreading frontal and cingulate deficits mapped in adolescents with schizophrenia. , 2006, Archives of general psychiatry.

[40]  P. Achermann,et al.  Sleep Homeostasis and Models of Sleep Regulation , 1999 .

[41]  M. Carskadon,et al.  Sleep electroencephalogram in children with a parental history of alcohol abuse/dependence , 2010, Journal of sleep research.

[42]  Irwin Feinberg,et al.  Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation , 2009, Proceedings of the National Academy of Sciences.

[43]  M. Bertini,et al.  Slow eye movements and EEG power spectra during wake-sleep transition , 2000, Clinical Neurophysiology.

[44]  Michelle K. Jetha,et al.  Electrophysiological changes during adolescence: A review , 2010, Brain and Cognition.

[45]  Braitenberg,et al.  Cortical architectonics: General and areal , 1978 .

[46]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  P. Nunez,et al.  Spatial filtering and neocortical dynamics: estimates of EEG coherence , 1998, IEEE Transactions on Biomedical Engineering.

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

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

[50]  W E Reddick,et al.  Age-related changes in the pediatric brain: quantitative MR evidence of maturational changes during adolescence. , 1997, AJNR. American journal of neuroradiology.

[51]  H. Jasper.  Report of the committee on methods of clinical examination in electroencephalography , 1958 .

[52]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[53]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[54]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[55]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[56]  The onset of the adolescent delta power decline occurs after age 11 years: a comment on Tarokh and Carskadon. , 2010, Sleep.

[57]  D. Dijk,et al.  Circadian variation of EEG power spectra in NREM and REM sleep in humans: Dissociation from body temperature , 1999, Journal of sleep research.

[58]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[59]  Linda C. Sobell,et al.  Timeline Follow-Back A Technique for Assessing Self-Reported Alcohol Consumption , 1992 .

[60]  Peter Achermann,et al.  Temporal evolution of coherence and power in the human sleep electroencephalogram , 1998, Journal of sleep research.

[61]  EEG Delta Power Decline Can Begin Before Age 11: A Reply to Campbell and Feinberg. , 2010 .

[62]  P. Nunez,et al.  Neocortical Dynamics and Human EEG Rhythms , 1995 .