Consistent anterior-posterior segregation of the insula during the first 2 years of life.

The human insula is a complex region characterized by heterogeneous cytoarchitecture, connectivity, and function. Subregional parcellation of the insula in adults has revealed an interesting anterior-posterior subdivision pattern that is highly consistent with its functional differentiation. However, the development of the insula's subregional segregation during the first 2 years of life remains unknown. The aim of this study was to test the hypothesis that similar segregation of the insula exists during this critical time period based on the resting-state functional magnetic resonance imaging study of a large cohort of infants (n = 143) with longitudinal scans. Our results confirmed a consistent anterior-posterior subdivision of the insula during the first 2 years of life with dissociable connectivity patterns associated with each cluster. Specifically, the anterior insula coupled more with frontal association areas, whereas the posterior insula integrated more with sensorimotor-related regions. More importantly, dramatic development of each subregion's functional network was observed, providing important neuronal correlates for the rapid advancement of its related functions during this time period.

[1]  Franco Cauda,et al.  How many clusters in the insular cortex? , 2013, Cerebral cortex.

[2]  Dinggang Shen,et al.  Cerebral Cortex doi:10.1093/cercor/bhs043 Cerebral Cortex Advance Access published February 24, 2012 The Synchronization within and Interaction between the Default and Dorsal Attention Networks in Early Infancy , 2022 .

[3]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[4]  E. W. Lauer,et al.  Somatovisceral motor patterns in the insula , 1961, The Journal of comparative neurology.

[5]  William W. Seeley,et al.  Anterior insula degeneration in frontotemporal dementia , 2010, Brain Structure and Function.

[6]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

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

[8]  Remco J. Renken,et al.  Group analyses of connectivity-based cortical parcellation using repeated k-means clustering , 2009, NeuroImage.

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

[10]  N. Volkow,et al.  Abnormal Functional Connectivity in Children with Attention-Deficit/Hyperactivity Disorder , 2012, Biological Psychiatry.

[11]  Dongchuan Yu.  Additional Brain Functional Network in Adults with Attention-Deficit/Hyperactivity Disorder: A Phase Synchrony Analysis , 2013, PloS one.

[12]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[13]  Marvin D. Nelson,et al.  Somatosensory lateralization in the newborn brain , 2006, NeuroImage.

[14]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

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

[16]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[17]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[18]  Hugo Lagercrantz,et al.  Pain activates cortical areas in the preterm newborn brain , 2006, PAIN.

[19]  Jonathan C. W. Brooks,et al.  Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging , 2005, NeuroImage.

[20]  Mark H. Johnson,et al.  Early Specialization for Voice and Emotion Processing in the Infant Brain , 2011, Current Biology.

[21]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[22]  E. Pihko,et al.  Magnetoencephalography in neonatology , 2012, Neurophysiologie Clinique/Clinical Neurophysiology.

[23]  C. Nilsson,et al.  von Economo neurones are selectively targeted in frontotemporal dementia , 2013, Neuropathology and applied neurobiology.

[24]  B. Peterson,et al.  Normal Development of Brain Circuits , 2010, Neuropsychopharmacology.

[25]  Anil K. Jain,et al.  Bootstrap Techniques for Error Estimation , 1987, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[26]  András Jakab,et al.  Connectivity-based parcellation reveals interhemispheric differences in the insula , 2011, Brain Topography.

[27]  Lumy Sawaki,et al.  Roles of the Insular Cortex in the Modulation of Pain: Insights from Brain Lesions , 2009, The Journal of Neuroscience.

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

[29]  Amanda Elton,et al.  Divergent task-dependent functional connectivity of executive control and salience networks , 2014, Cortex.

[30]  Deborah Yurgelun-Todd,et al.  Reduced insular volume in attention deficit hyperactivity disorder , 2012, Psychiatry Research: Neuroimaging.

[31]  Gabriel S. Dichter,et al.  Functional magnetic resonance imaging of autism spectrum disorders , 2012, Dialogues in clinical neuroscience.

[32]  C. Keysers,et al.  Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex , 2011, Human brain mapping.

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

[34]  J K Smith,et al.  Temporal and Spatial Development of Axonal Maturation and Myelination of White Matter in the Developing Brain , 2008, American Journal of Neuroradiology.

[35]  M. Styner,et al.  Longitudinal development of cortical and subcortical gray matter from birth to 2 years. , 2012, Cerebral cortex.

[36]  Stefan A. Carp,et al.  Somatosensory evoked changes in cerebral oxygen consumption measured non-invasively in premature neonates , 2014, NeuroImage.

[37]  I. Tracey,et al.  The insula: A multidimensional integration site for pain , 2007, Pain.

[38]  K. Okanoya,et al.  Broad cortical activation in response to tactile stimulation in newborns , 2012, Neuroreport.

[39]  Dinggang Shen,et al.  Measuring temporal morphological changes robustly in brain MR images via 4-dimensional template warping , 2004, NeuroImage.

[40]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[41]  P. Liddle,et al.  Appreciating symptoms and deficits in schizophrenia: Right posterior insula and poor insight , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[42]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[43]  P. Huttenlocher.  Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[44]  A. Schulze-Bonhage,et al.  Functional organization of the human anterior insular cortex , 2009, Neuroscience Letters.

[45]  Simon Baron-Cohen,et al.  Reduced functional connectivity within and between ‘social’ resting state networks in autism spectrum conditions , 2012, Social cognitive and affective neuroscience.

[46]  Joachim M. Buhmann,et al.  Stability-Based Validation of Clustering Solutions , 2004, Neural Computation.

[47]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[48]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[49]  D. Willshaw,et al.  Principles of Computational Modelling in Neuroscience: The development of the nervous system , 2011 .

[50]  Siddheswar Ray,et al.  Determination of Number of Clusters in K-Means Clustering and Application in Colour Image Segmentation , 2000 .

[51]  Martin Styner,et al.  Associations between white matter microstructure and infants' working memory , 2013, NeuroImage.

[52]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

[53]  J. Changeux,et al.  Basic consciousness of the newborn. , 2010, Seminars in perinatology.

[54]  P. Mertens,et al.  Development of the human fetal insular cortex: study of the gyration from 13 to 28 gestational weeks , 2007, Brain Structure and Function.

[55]  Dinggang Shen,et al.  Temporal and Spatial Evolution of Brain Network Topology during the First Two Years of Life , 2011, PloS one.

[56]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

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

[58]  J. Allman,et al.  Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans , 2009, The Journal of comparative neurology.

[59]  Rebecca D Folkerth,et al.  Axonal development in the cerebral white matter of the human fetus and infant , 2005, The Journal of comparative neurology.

[60]  Dinggang Shen,et al.  Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects , 2009, Proceedings of the National Academy of Sciences.

[61]  M. Steriade.  Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[62]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[63]  Alan C. Evans,et al.  Multi-level bootstrap analysis of stable clusters in resting-state fMRI , 2009, NeuroImage.

[64]  R. Porter,et al.  Breast odour as the only maternal stimulus elicits crawling towards the odour source , 2001, Acta paediatrica.

[65]  Rudolf Nieuwenhuys,et al.  The insular cortex: a review. , 2012, Progress in brain research.

[66]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[67]  Martin Styner,et al.  White Matter Heritability Using Diffusion Tensor Imaging in Neonatal Brains , 2012, Twin Research and Human Genetics.

[68]  E Burdet,et al.  Computer-controlled stimulation for functional magnetic resonance imaging studies of the neonatal olfactory system , 2013, Acta paediatrica.

[69]  A. Bechara,et al.  A neurocognitive approach to understanding the neurobiology of addiction , 2013, Current Opinion in Neurobiology.

[70]  P. Hof,et al.  Von Economo Neurons , 2015 .

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

[72]  Lucina Q. Uddin,et al.  The anterior insula in autism: Under-connected and under-examined , 2009, Neuroscience & Biobehavioral Reviews.

[73]  Jürgen Baudewig,et al.  The Role of the Amygdala in Atypical Gaze on Emotional Faces in Autism Spectrum Disorders , 2012, The Journal of Neuroscience.

[74]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[75]  Christine L. Cox,et al.  The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. , 2012, Social cognitive and affective neuroscience.

[76]  Soyoung Q. Park,et al.  Annals of the New York Academy of Sciences the Von Economo Neurons in the Frontoinsular and Anterior Cingulate Cortex , 2022 .

[77]  J. A. Payne,et al.  The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation , 1999, Nature.

[78]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[79]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[80]  Patrick R Hof,et al.  Von Economo Neurons in the Elephant Brain , 2009, Anatomical record.

[81]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

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

[83]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[84]  Isabelle Guyon,et al.  A Stability Based Method for Discovering Structure in Clustered Data , 2001, Pacific Symposium on Biocomputing.

[85]  Nikos K. Logothetis,et al.  Von Economo Neurons in the Anterior Insula of the Macaque Monkey , 2012, Neuron.