Cortical burst dynamics predict clinical outcome early in extremely preterm infants.

Intermittent bursts of electrical activity are a ubiquitous signature of very early brain activity. Previous studies have largely focused on assessing the amplitudes of these transient cortical bursts or the intervals between them. Recent advances in basic neuroscience have identified the presence of scale-free 'avalanche' processes in bursting patterns of cortical activity in other clinical contexts. Here, we hypothesize that cortical bursts in human preterm infants also exhibit scale-free properties, providing new insights into the nature, temporal evolution, and prognostic value of spontaneous brain activity in the days immediately following preterm birth. We examined electroencephalographic recordings from 43 extremely preterm infants (gestational age 22-28 weeks) and demonstrated that their cortical bursts exhibit scale-free properties as early as 12 h after birth. The scaling relationships of cortical bursts correlate significantly with later mental development-particularly within the first 12 h of life. These findings show that early preterm brain activity is characterized by scale-free dynamics which carry developmental significance, hence offering novel means for rapid and early clinical prediction of neurodevelopmental outcomes.

[1]  Ingmar Rosén,et al.  Electroencephalography and brain damage in preterm infants. , 2005, Early human development.

[2]  D. L. Schomer,et al.  Niedermeyer's Electroencephalography: Basic Principles, Clinical Applications, and Related Fields , 2012 .

[3]  L. Brion,et al.  Amplitude-Integrated EEG in Preterm Infants: Maturation of Background Pattern and Amplitude Voltage with Postmenstrual Age and Gestational Age , 2005, Journal of Perinatology.

[4]  Rustem Khazipov,et al.  Spontaneous activity in developing sensory circuits: Implications for resting state fMRI , 2012, NeuroImage.

[5]  Biyu J. He,et al.  The Temporal Structures and Functional Significance of Scale-free Brain Activity , 2010, Neuron.

[6]  D. Plenz,et al.  Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3 , 2008, Proceedings of the National Academy of Sciences.

[7]  Hiroyuki Kidokoro,et al.  Chronologic Changes in Neonatal EEG Findings in Periventricular Leukomalacia , 2009, Pediatrics.

[8]  K. Kaila,et al.  Development of neonatal EEG activity: from phenomenology to physiology. , 2006, Seminars in fetal & neonatal medicine.

[9]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[10]  Sampsa Vanhatalo,et al.  Early Brain Activity Relates to Subsequent Brain Growth in Premature Infants. , 2015, Cerebral cortex.

[11]  Michael Breakspear,et al.  Critical role for resource constraints in neural models , 2014, Front. Syst. Neurosci..

[12]  Edward T. Bullmore,et al.  Failure of Adaptive Self-Organized Criticality during Epileptic Seizure Attacks , 2011, PLoS Comput. Biol..

[13]  C. Shapiro-Mendoza Commentary: Mediation and moderation analyses: a novel approach to exploring the complex pathways between maternal medical conditions, preterm birth and associated newborn morbidity risk. , 2014, International journal of epidemiology.

[14]  John M. Beggs,et al.  Universal critical dynamics in high resolution neuronal avalanche data. , 2012, Physical review letters.

[15]  Leonardo L. Gollo,et al.  Single-neuron criticality optimizes analog dendritic computation , 2013, Scientific Reports.

[16]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

[17]  Patrick O Kanold,et al.  Subplate Neurons Promote Spindle Bursts and Thalamocortical Patterning in the Neonatal Rat Somatosensory Cortex , 2012, The Journal of Neuroscience.

[18]  Sampsa Vanhatalo,et al.  Early development of spatial patterns of power-law frequency scaling in FMRI resting-state and EEG data in the newborn brain. , 2013, Cerebral cortex.

[19]  A. C. Primavesi Neurologic and Developmental Disability after Extremely Preterm Birth , 2000 .

[20]  Karl J. Friston,et al.  Bayesian model selection for group studies (vol 46, pg 1005, 2009) , 2009 .

[21]  Steven P. Miller,et al.  Brain injury in premature neonates: A primary cerebral dysmaturation disorder? , 2014, Annals of neurology.

[22]  A. Okumura,et al.  Background electroencephalographic (EEG) activities of very preterm infants born at less than 27 weeks gestation: a study on the degree of continuity , 2001, Archives of disease in childhood. Fetal and neonatal edition.

[23]  José Meseguer,et al.  Temporal Structures , 1989, Mathematical Structures in Computer Science.

[24]  Paul B. Colditz,et al.  Spatial patterning of the neonatal EEG suggests a need for a high number of electrodes , 2013, NeuroImage.

[25]  G. Vogel,et al.  Drug effects on REM sleep and on endogenous depression , 1990, Neuroscience & Biobehavioral Reviews.

[26]  Richard Coppola,et al.  Neuronal avalanches in the resting MEG of the human brain , 2012 .

[27]  Werner Kilb,et al.  Electrical activity patterns and the functional maturation of the neocortex , 2011, The European journal of neuroscience.

[28]  Sampsa Vanhatalo,et al.  Slow endogenous activity transients and developmental expression of K+–Cl− cotransporter 2 in the immature human cortex , 2005, The European journal of neuroscience.

[29]  F. Dekker,et al.  Very preterm birth is associated with disabilities in multiple developmental domains. , 2005, Journal of pediatric psychology.

[30]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

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

[32]  P. G. Larsson,et al.  Feasibility of Long-Term Continuous EEG Monitoring During the First Days of Life in Preterm Infants: An Automated Quantification of the EEG Activity , 2011, Pediatric Research.

[33]  Olaf Sporns,et al.  Neurobiologically Realistic Determinants of Self-Organized Criticality in Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

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

[35]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[36]  Sampsa Vanhatalo,et al.  Detection of ‘EEG bursts’ in the early preterm EEG: Visual vs. automated detection , 2010, Clinical Neurophysiology.

[37]  S. Vanhatalo,et al.  Drug effects on endogenous brain activity in preterm babies , 2014, Brain and Development.

[38]  H. Luhmann,et al.  LPS-induced microglial secretion of TNFα increases activity-dependent neuronal apoptosis in the neonatal cerebral cortex. , 2013, Cerebral cortex.

[39]  D. Plenz,et al.  Criticality in neural systems , 2014 .

[40]  A. Okumura,et al.  Absent Cyclicity on aEEG within the First 24 h is Associated with Brain Damage in Preterm Infants , 2010, Neuropediatrics.

[41]  Kuniyoshi Kuno,et al.  Developmental outcome and types of chronic‐stage EEG abnormalities in preterm infants , 2002 .

[42]  C. Klein Nutrient requirements for preterm infant formulas. , 2002, The Journal of nutrition.

[43]  I. Hanganu-Opatz Between molecules and experience: Role of early patterns of coordinated activity for the development of cortical maps and sensory abilities , 2010, Brain Research Reviews.

[44]  Sampsa Vanhatalo,et al.  Sleep wake cycling in early preterm infants: Comparison of polysomnographic recordings with a novel EEG-based index , 2013, Clinical Neurophysiology.

[45]  Francesca Colaiori,et al.  Average shape of a fluctuation: universality in excursions of stochastic processes. , 2003, Physical review letters.

[46]  Michael Breakspear,et al.  Novel features of early burst suppression predict outcome after birth asphyxia , 2014, Annals of clinical and translational neurology.

[47]  C. Shatz,et al.  Activity-dependent cortical target selection by thalamic axons. , 1998, Science.

[48]  Stanley,et al.  Barkhausen noise: Elementary signals, power laws, and scaling relations. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[49]  S. Vanhatalo,et al.  Development of the spontaneous activity transients and ongoing cortical activity in human preterm babies , 2007, Neuroscience.

[50]  J. Oosterlaan,et al.  Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children , 2009, Pediatrics.

[51]  J. Sethna,et al.  Crackling noise , 2001, Nature.

[52]  Average trajectory of returning walks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  Mark E. J. Newman,et al.  Power-Law Distributions in Empirical Data , 2007, SIAM Rev..

[54]  M. Feller,et al.  Mechanisms underlying spontaneous patterned activity in developing neural circuits , 2010, Nature Reviews Neuroscience.

[55]  K. Speechley,et al.  Neonatal morbidity associated with late preterm and early term birth: the roles of gestational age and biological determinants of preterm birth. , 2014, International journal of epidemiology.

[56]  L. Papile,et al.  Neonatal Intensive Care Unit Stress Is Associated with Brain Development in Preterm Infants , 2012 .

[57]  E. Walls-Esquivel,et al.  Electroencephalography (EEG) recording techniques and artefact detection in early premature babies , 2007, Neurophysiologie Clinique/Clinical Neurophysiology.

[58]  S. Vanhatalo,et al.  Measuring brain activity cycling (BAC) in long term EEG monitoring of preterm babies. , 2014, Physiological measurement.

[59]  J. Sethna,et al.  Crackling noise : Complex systems , 2001 .

[60]  Milos Judas,et al.  The development of the subplate and thalamocortical connections in the human foetal brain , 2010, Acta paediatrica.

[61]  Michael Breakspear,et al.  Scale-Free Bursting in Human Cortex following Hypoxia at Birth , 2014, The Journal of Neuroscience.

[62]  J. Sethna,et al.  Universality beyond power laws and the average avalanche shape , 2011 .

[63]  E. Walls-Esquivel,et al.  Electroencephalography in premature and full-term infants. Developmental features and glossary , 2010, Neurophysiologie Clinique/Clinical Neurophysiology.

[64]  Arnold Pollak,et al.  Reference values for amplitude-integrated electroencephalographic activity in preterm infants younger than 30 weeks' gestational age. , 2004, Pediatrics.

[65]  C. Stam,et al.  Scale‐free dynamics of global functional connectivity in the human brain , 2004, Human brain mapping.

[66]  Vineta Fellman,et al.  Early single-channel aEEG/EEG predicts outcome in very preterm infants , 2012, Acta paediatrica.

[67]  Qingming Luo,et al.  Developing neuronal networks: Self-organized criticality predicts the future , 2013, Scientific Reports.