Correspondence Between Aberrant Intrinsic Network Connectivity and Gray-Matter Volume in the Ventral Brain of Preterm Born Adults.

Widespread brain changes are present in preterm born infants, adolescents, and even adults. While neurobiological models of prematurity facilitate powerful explanations for the adverse effects of preterm birth on the developing brain at microscale, convincing linking principles at large-scale level to explain the widespread nature of brain changes are still missing. We investigated effects of preterm birth on the brain's large-scale intrinsic networks and their relation to brain structure in preterm born adults. In 95 preterm and 83 full-term born adults, structural and functional magnetic resonance imaging at-rest was used to analyze both voxel-based morphometry and spatial patterns of functional connectivity in ongoing blood oxygenation level-dependent activity. Differences in intrinsic functional connectivity (iFC) were found in cortical and subcortical networks. Structural differences were located in subcortical, temporal, and cingulate areas. Critically, for preterm born adults, iFC-network differences were overlapping and correlating with aberrant regional gray-matter (GM) volume specifically in subcortical and temporal areas. Overlapping changes were predicted by prematurity and in particular by neonatal medical complications. These results provide evidence that preterm birth has long-lasting effects on functional connectivity of intrinsic networks, and these changes are specifically related to structural alterations in ventral brain GM.

[1]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[2]  Rebecca D. Folkerth,et al.  Gray matter injury associated with periventricular leukomalacia in the premature infant , 2007, Acta Neuropathologica.

[3]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[4]  H. Kinney,et al.  The Cerebral Cortex Overlying Periventricular Leukomalacia: Analysis of Pyramidal Neurons , 2010, Brain pathology.

[5]  F. Jensen,et al.  Regional Differences in Susceptibility to Hypoxic-Ischemic Injury in the Preterm Brain: Exploring the Spectrum from White Matter Loss to Selective Grey Matter Injury in a Rat Model , 2012, Neurology research international.

[6]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[7]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[8]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[9]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Allsop,et al.  Quantification of Deep Gray Matter in Preterm Infants at Term-Equivalent Age Using Manual Volumetry of 3-Tesla Magnetic Resonance Images , 2007, Pediatrics.

[12]  Peter Fransson,et al.  Spontaneous Brain Activity in the Newborn Brain During Natural Sleep—An fMRI Study in Infants Born at Full Term , 2009, Pediatric Research.

[13]  Michelle Hampson,et al.  Functional connectivity to a right hemisphere language center in prematurely born adolescents , 2010, NeuroImage.

[14]  Michelle Hampson,et al.  Preterm birth results in alterations in neural connectivity at age 16 years , 2011, NeuroImage.

[15]  V. Calhoun,et al.  Selective changes of resting-state networks in individuals at risk for Alzheimer's disease , 2007, Proceedings of the National Academy of Sciences.

[16]  Philip J. Brittain,et al.  Dysconnectivity of neurocognitive networks at rest in very-preterm born adults☆ , 2014, NeuroImage: Clinical.

[17]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[18]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[19]  N. Bargalló,et al.  Gray Matter Volume Decrements in Preterm Children With Periventricular Leukomalacia , 2011, Pediatric Research.

[20]  F. Vaccarino,et al.  Neurobiology of premature brain injury , 2014, Nature Neuroscience.

[21]  H. Prechtl,et al.  Neurological sequelae of prenatal and perinatal complications. , 1967, British medical journal.

[22]  Franz Petermann,et al.  Wechsler Intelligenztest für Erwachsene (WIE). , 2007 .

[23]  Junming Shao,et al.  Aberrant topology of striatum's connectivity is associated with the number of episodes in depression. , 2014, Brain : a journal of neurology.

[24]  Ingeborg Krägeloh-Mann,et al.  Specific impairment of functional connectivity between language regions in former early preterms , 2014, Human brain mapping.

[25]  Klaus F. Riegel,et al.  Effects of gestation and birth weight on the growth and development of very low birthweight small for gestational age infants: a matched group comparison , 2000, Archives of disease in childhood. Fetal and neonatal edition.

[26]  Hong Wang,et al.  Abnormal Cerebral Structure Is Present at Term in Premature Infants , 2005, Pediatrics.

[27]  B. T. Thomas Yeo,et al.  The Organization of Local and Distant Functional Connectivity in the Human Brain , 2010, PLoS Comput. Biol..

[28]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[29]  T. Eichele,et al.  Increased Intrinsic Brain Activity in the Striatum Reflects Symptom Dimensions in Schizophrenia , 2012, Schizophrenia bulletin.

[30]  H. Kinney,et al.  Diffuse Axonal Injury in Periventricular Leukomalacia as Determined by Apoptotic Marker Fractin , 2008, Pediatric Research.

[31]  K. Hugdahl,et al.  fMRI: blood oxygen level–dependent activation during a working memory–selective attention task in children born extremely preterm , 2013, Pediatric Research.

[32]  J. Piva,et al.  [Eyes on the present and looking into the future] , 2001, Jornal de pediatria.

[33]  Tülay Adali,et al.  Comparison of multi‐subject ICA methods for analysis of fMRI data , 2010, Human brain mapping.

[34]  Peter Fransson,et al.  Resting-state networks in the infant brain , 2007, Proceedings of the National Academy of Sciences.

[35]  Ramon Casanova,et al.  Biological parametric mapping: A statistical toolbox for multimodality brain image analysis , 2007, NeuroImage.

[36]  Vince D. Calhoun,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[37]  Eve C Johnstone,et al.  Low birthweight and preterm birth in young people with special educational needs: a magnetic resonance imaging analysis , 2008, BMC medicine.

[38]  Jun Saiki,et al.  Maintaining coherence of dynamic objects requires coordination of neural systems extended from anterior frontal to posterior parietal brain cortices , 2005, NeuroImage.

[39]  W. Deng,et al.  Neurobiology of injury to the developing brain , 2010, Nature Reviews Neurology.

[40]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[41]  L M Dubowitz,et al.  Clinical assessment of gestational age in the newborn infant. , 1970, The Journal of pediatrics.

[42]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[43]  S. Robinson,et al.  Neonatal loss of γ–aminobutyric acid pathway expression after human perinatal brain injury , 2006 .

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

[45]  Maxime Guye,et al.  Basal functional connectivity within the anterior temporal network is associated with performance on declarative memory tasks , 2011, NeuroImage.

[46]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. Volpe Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances , 2009, The Lancet Neurology.

[48]  Chiara Nosarti,et al.  Neural substrates of letter fluency processing in young adults who were born very preterm: Alterations in frontal and striatal regions , 2009, NeuroImage.

[49]  Xiangyu Long,et al.  Functional segmentation of the brain cortex using high model order group PICA , 2009, Human brain mapping.

[50]  S. Robinson,et al.  Neonatal loss of gamma-aminobutyric acid pathway expression after human perinatal brain injury. , 2006, Journal of neurosurgery.

[51]  Gro C. Christensen Løhaugen,et al.  Young adults born preterm with very low birth weight demonstrate widespread white matter alterations on brain DTI , 2011, NeuroImage.

[52]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[53]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[54]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[55]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[56]  Daniel Rueckert,et al.  The Effect of Preterm Birth on Thalamic and Cortical Development , 2011, Cerebral cortex.

[57]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[58]  Rebecca D Folkerth,et al.  Neuron deficit in the white matter and subplate in periventricular leukomalacia , 2012, Annals of neurology.

[59]  Z. J. Huang,et al.  Development of GABA innervation in the cerebral and cerebellar cortices , 2007, Nature Reviews Neuroscience.

[60]  Michelle Hampson,et al.  Alterations in neural connectivity in preterm children at school age , 2009, NeuroImage.

[61]  Chiara Nosarti,et al.  Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. , 2008, Brain : a journal of neurology.

[62]  Kevin Murphy,et al.  How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration , 2007, NeuroImage.

[63]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[64]  Hae-Jeong Park,et al.  Functional connectivity‐based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI , 2013, Human brain mapping.

[65]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

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