Towards the “Baby Connectome”: Mapping the Structural Connectivity of the Newborn Brain

Defining the structural and functional connectivity of the human brain (the human “connectome”) is a basic challenge in neuroscience. Recently, techniques for noninvasively characterizing structural connectivity networks in the adult brain have been developed using diffusion and high-resolution anatomic MRI. The purpose of this study was to establish a framework for assessing structural connectivity in the newborn brain at any stage of development and to show how network properties can be derived in a clinical cohort of six-month old infants sustaining perinatal hypoxic ischemic encephalopathy (HIE). Two different anatomically unconstrained parcellation schemes were proposed and the resulting network metrics were correlated with neurological outcome at 6 months. Elimination and correction of unreliable data, automated parcellation of the cortical surface, and assembling the large-scale baby connectome allowed an unbiased study of the network properties of the newborn brain using graph theoretic analysis. In the application to infants with HIE, a trend to declining brain network integration and segregation was observed with increasing neuromotor deficit scores.

[1]  H. Lagercrantz,et al.  The functional architecture of the infant brain as revealed by resting-state fMRI. , 2011, Cerebral cortex.

[2]  Simon J Graham,et al.  Partial k‐space reconstruction in single‐shot diffusion‐weighted echo‐planar imaging , 2007, Magnetic resonance in medicine.

[3]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[4]  Gregory Gutin,et al.  Digraphs - theory, algorithms and applications , 2002 .

[5]  F. Turkheimer,et al.  Emergence of resting state networks in the preterm human brain , 2010, Proceedings of the National Academy of Sciences.

[6]  Maxime Descoteaux,et al.  Quantifying Brain Connectivity: A Comparative Tractography Study , 2009, MICCAI.

[7]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[8]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[9]  Paul C. Leopardi.  A PARTITION OF THE UNIT SPHERE INTO REGIONS OF EQUAL AREA AND SMALL DIAMETER , 2006 .

[10]  Steven C.R. Williams,et al.  Proc. Intl. Soc. Mag. Reson. Med. , 2012 .

[11]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[12]  Dinggang Shen,et al.  Development Trends of White Matter Connectivity in the First Years of Life , 2011, PloS one.

[13]  F. Lazeyras,et al.  Mapping the early cortical folding process in the preterm newborn brain. , 2008, Cerebral cortex.

[14]  Jacobus F. A. Jansen,et al.  The effect and reproducibility of different clinical DTI gradient sets on small world brain connectivity measures , 2010, NeuroImage.

[15]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[16]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[17]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[18]  D. Ferriero,et al.  Early Prediction of Neurological Outcome after Perinatal Depression , 1999 .

[19]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[20]  Olaf Sporns,et al.  MR connectomics: Principles and challenges , 2010, Journal of Neuroscience Methods.

[21]  Marcus Kaiser,et al.  A tutorial in connectome analysis: Topological and spatial features of brain networks , 2011, NeuroImage.

[22]  Steven P. Miller,et al.  MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. , 2006, AJNR. American journal of neuroradiology.

[23]  Derek K. Jones,et al.  The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: A Monte Carlo study † , 2004, Magnetic resonance in medicine.

[24]  Kerstin Pannek,et al.  Comparative mouse brain tractography of diffusion magnetic resonance imaging , 2010, NeuroImage.

[25]  M. Greicius,et al.  Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity , 2009, Brain Structure and Function.

[26]  Abraham Z. Snyder,et al.  Functional connectivity MRI in infants: Exploration of the functional organization of the developing brain , 2011, NeuroImage.

[27]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[28]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[29]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[30]  O. Sporns,et al.  White matter maturation reshapes structural connectivity in the late developing human brain , 2010, Proceedings of the National Academy of Sciences.

[31]  Jun Li,et al.  Brain Anatomical Network and Intelligence , 2009, NeuroImage.

[32]  P. Thiran,et al.  Mapping Human Whole-Brain Structural Networks with Diffusion MRI , 2007, PloS one.

[33]  T P Trouard,et al.  Analysis and comparison of motion‐correction techniques in diffusion‐weighted imaging , 1996, Journal of magnetic resonance imaging : JMRI.

[34]  Derek K. Jones,et al.  Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI , 2003, Magnetic resonance in medicine.

[35]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[36]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[37]  Dinggang Shen,et al.  Brain anatomical networks in early human brain development , 2011, NeuroImage.

[38]  M. Fox,et al.  Noninvasive functional and structural connectivity mapping of the human thalamocortical system. , 2010, Cerebral cortex.

[39]  Fabrice Bartolomei,et al.  Graph theoretical analysis of structural and functional connectivity MRI in normal and pathological brain networks , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.