Neural synchrony and the development of cortical networks

Recent data indicate that the synchronisation of oscillatory activity is relevant for the development of cortical circuits as demonstrated by the involvement of neural synchrony in synaptic plasticity and changes in the frequency and synchronisation of neural oscillations during development. Analyses of resting-state and task-related neural synchrony indicate that gamma-oscillations emerge during early childhood and precise temporal coordination through neural synchrony continues to mature until early adulthood. The late maturation of neural synchrony is compatible with changes in the myelination of cortico-cortical connections and with late development of GABAergic neurotransmission. These findings highlight the role of neural synchrony for normal brain development as well as its potential importance for understanding neurodevelopmental disorders, such as autism spectrum disorders (ASDs) and schizophrenia.

[1]  D. Halliday,et al.  Changes in EMG coherence between long and short thumb abductor muscles during human development , 2007, The Journal of physiology.

[2]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[3]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[4]  W. Singer,et al.  Precisely Synchronized Oscillatory Firing Patterns Require Electroencephalographic Activation , 1999, The Journal of Neuroscience.

[5]  Robert W Thatcher,et al.  Development of cortical connections as measured by EEG coherence and phase delays , 2008, Human brain mapping.

[6]  W. Singer,et al.  Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. , 1992, Science.

[7]  P. Teale,et al.  Development of the 40Hz steady state auditory evoked magnetic field from ages 5 to 52 , 2006, Clinical Neurophysiology.

[8]  P. Somogyi,et al.  Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus , 2002, The Journal of Neuroscience.

[9]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[10]  K. Grill-Spector,et al.  Differential development of high-level visual cortex correlates with category-specific recognition memory , 2007, Nature Neuroscience.

[11]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Hare,et al.  The Adolescent Brain , 2008, Annals of the New York Academy of Sciences.

[13]  Y. Ben-Ari.  Developing networks play a similar melody , 2001, Trends in Neurosciences.

[14]  W. Klimesch,et al.  Lifespan differences in cortical dynamics of auditory perception. , 2009, Developmental science.

[15]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[16]  T. Picton,et al.  Age-related changes in transient and oscillatory brain responses to auditory stimulation during early adolescence. , 2009, Developmental science.

[17]  D. Halliday,et al.  On the development of human corticospinal oscillations: age‐related changes in EEG–EMG coherence and cumulant , 2008, The European journal of neuroscience.

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

[19]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[20]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[21]  P. Fries.  Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[22]  A. Toga,et al.  Mapping brain maturation , 2006, Trends in Neurosciences.

[23]  G. Buzsáki.  Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory , 2005, Hippocampus.

[24]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[25]  Wolf Singer,et al.  What Do Disturbances in Neural Synchrony Tell Us About Autism? , 2007, Biological Psychiatry.

[26]  J. Lisman,et al.  Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state , 1993, Nature.

[27]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[28]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[29]  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.

[30]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[31]  T. Tsumoto,et al.  Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[33]  W. Singer,et al.  Phase Sensitivity of Synaptic Modifications in Oscillating Cells of Rat Visual Cortex , 2004, The Journal of Neuroscience.

[34]  J. Knott.  The organization of behavior: A neuropsychological theory , 1951 .

[35]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[36]  W. Singer.  Development and plasticity of cortical processing architectures. , 1995, Science.

[37]  M. Kahana,et al.  Comparison of spectral analysis methods for characterizing brain oscillations , 2007, Journal of Neuroscience Methods.

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

[39]  Michael W. Spratling,et al.  Gamma oscillations and object processing in the infant brain. , 2000, Science.

[40]  Carter Wendelken,et al.  Neurocognitive development of the ability to manipulate information in working memory. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Eugenio Rodriguez,et al.  The development of neural synchrony reflects late maturation and restructuring of functional networks in humans , 2009, Proceedings of the National Academy of Sciences.

[42]  Heiko J. Luhmann,et al.  Early patterns of electrical activity in the developing cerebral cortex of humans and rodents , 2006, Trends in Neurosciences.

[43]  J. Yordanova,et al.  Developmental changes in the alpha response system. , 1996, Electroencephalography and clinical neurophysiology.

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

[45]  Takanori Hashimoto,et al.  Protracted Developmental Trajectories of GABA A Receptor α1 and α2 Subunit Expression in Primate Prefrontal Cortex , 2009, Biological Psychiatry.

[46]  Ramesh Srinivasan,et al.  Spatial structure of the human alpha rhythm: global correlation in adults and local correlation in children , 1999, Clinical Neurophysiology.

[47]  R. Traub,et al.  Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro , 1998, Nature.

[48]  T. Paus,et al.  Sex differences in the growth of white matter during adolescence , 2009, NeuroImage.

[49]  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.

[50]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[51]  S. Hestrin,et al.  Electrical synapses define networks of neocortical GABAergic neurons , 2005, Trends in Neurosciences.

[52]  M. Poo,et al.  Spike Timing-Dependent LTP/LTD Mediates Visual Experience-Dependent Plasticity in a Developing Retinotectal System , 2006, Neuron.

[53]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[54]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[55]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[56]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[58]  Rafael Yuste,et al.  Gap junctions in developing neocortex: a review , 2004, Brain Research Reviews.

[59]  Viktor Müller,et al.  EEG gamma-band synchronization in visual coding from childhood to old age: Evidence from evoked power and inter-trial phase locking , 2009, Clinical Neurophysiology.

[60]  N. Lazar,et al.  Maturation of cognitive processes from late childhood to adulthood. , 2004, Child development.

[61]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[62]  E. Gordon,et al.  Brain maturation in adolescence: Concurrent changes in neuroanatomy and neurophysiology , 2007, Human brain mapping.

[63]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[64]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[65]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[66]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[67]  M. Brammer,et al.  Linear age‐correlated functional development of right inferior fronto‐striato‐cerebellar networks during response inhibition and anterior cingulate during error‐related processes , 2007, Human brain mapping.

[68]  Kenneth D. Harris,et al.  Early cognitive and language skills are linked to resting frontal gamma power across the first 3 years , 2008, Behavioural Brain Research.

[69]  P. Jonas,et al.  Postnatal Differentiation of Basket Cells from Slow to Fast Signaling Devices , 2008, The Journal of Neuroscience.

[70]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.