Structural asymmetries of perisylvian regions in the preterm newborn

During the last trimester of human pregnancy, the cerebral cortex of foetuses becomes greatly and quickly gyrified, and post-mortem studies have demonstrated that hemispheres are already asymmetric at the level of Heschl gyrus, planum temporale and superior temporal sulcus (STS). Recently, magnetic resonance imaging (MRI) and dedicated post-processing tools enabled the quantitative study of brain development non-invasively in the preterm newborn. However, previous investigations were conducted either over the whole brain or in specific sulci. These approaches may consequently fail to highlight most cerebral sites, where anatomical landmarks are hard to delineate among individuals. In this cross-sectional study, we aimed to blindly and automatically map early asymmetries over the immature cortex. Voxel-based analyses of cortical and white matter masks were performed over a group of 25 newborns from 26 to 36 weeks of gestational age. Inter-individual variations associated with increasing age were first detected in large cerebral regions, with a prevalence of the right hemisphere in comparison with the left. Asymmetries were further highlighted in three specific cortical regions. Confirming previous studies, we observed deeper STS on the right side and larger posterior region of the sylvian fissure on the left side, close to planum temporale. For the first time, we also detected larger anterior region of the sylvian fissure on the left side, close to Broca's region. This study demonstrated that perisylvian regions are the only regions to be asymmetric from early on, suggesting their anatomical specificity for the emergence of functional lateralization in language processing prior to language exposure.

[1]  Jo Hajnal,et al.  MR imaging methods for assessing fetal brain development , 2008, Developmental neurobiology.

[2]  Daniel Rueckert,et al.  MRI of Moving Subjects Using Multislice Snapshot Images With Volume Reconstruction (SVR): Application to Fetal, Neonatal, and Adult Brain Studies , 2007, IEEE Transactions on Medical Imaging.

[3]  Simon K Warfield,et al.  Early Alteration of Structural and Functional Brain Development in Premature Infants Born with Intrauterine Growth Restriction , 2004, Pediatric Research.

[4]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

[5]  Ron Kikinis,et al.  Adaptive, template moderated, spatially varying statistical classification , 2000, Medical Image Anal..

[6]  D. Le Bihan,et al.  Structural Asymmetries in the Infant Language and Sensori-motor Networks , 2022 .

[7]  F. Cowan,et al.  Reduced development of cerebral cortex in extremely preterm infants , 2000, The Lancet.

[8]  Colin Studholme,et al.  Registration-based approach for reconstruction of high-resolution in utero fetal MR brain images. , 2006, Academic radiology.

[9]  Y. Samson,et al.  "Sulcal root" generic model: a hypothesis to overcome the variability of the human cortex folding patterns. , 2005, Neurologia medico-chirurgica.

[10]  C. Büchel,et al.  White matter asymmetry in the human brain: a diffusion tensor MRI study. , 2004, Cerebral cortex.

[11]  E. Duchesnay,et al.  A framework to study the cortical folding patterns , 2004, NeuroImage.

[12]  F. Lazeyras,et al.  Primary cortical folding in the human newborn: an early marker of later functional development. , 2008, Brain : a journal of neurology.

[13]  F. Gilles,et al.  Gyral development of the human brain. , 1977, Annals of Neurology.

[14]  Alan C. Evans,et al.  Spatial distribution of deep sulcal landmarks and hemispherical asymmetry on the cortical surface. , 2010, Cerebral cortex.

[15]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[16]  D. Van De Ville,et al.  An fMRI comparison of auditory processing between premature infants at term age and term born neonates , 2008 .

[17]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[18]  Alan C. Evans,et al.  Positional and surface area asymmetry of the human cerebral cortex , 2009, NeuroImage.

[19]  S. F. Witelson,et al.  Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. , 1973, Brain : a journal of neurology.

[20]  Katrin Amunts,et al.  Broca’s area: Nomenclature, anatomy, typology and asymmetry , 2009, Brain and Language.

[21]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[22]  C. Boesch,et al.  Structural and Neurobehavioral Delay in Postnatal Brain Development of Preterm Infants1 , 1996, Pediatric Research.

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

[24]  Diana Claassen,et al.  Development of the Human Fetal Brain: An Anatomical Atlas , 1989 .

[25]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[26]  Isabelle Bloch,et al.  A primal sketch of the cortex mean curvature: a morphogenesis based approach to study the variability of the folding patterns , 2003, IEEE Transactions on Medical Imaging.

[27]  F. Gilles,et al.  Left-right asymmetries of the temporal speech areas of the human fetus. , 1977, Archives of neurology.

[28]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[29]  M. Sigman,et al.  Functional organization of perisylvian activation during presentation of sentences in preverbal infants , 2006, Proceedings of the National Academy of Sciences.

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

[31]  Jean-Francois Mangin,et al.  Identification of Growth Seeds in the Neonate Brain through Surfacic Helmholtz Decomposition , 2009, IPMI.

[32]  Simon K Warfield,et al.  Neonate hippocampal volumes: Prematurity, perinatal predictors, and 2‐year outcome , 2008, Annals of neurology.

[33]  Alan C. Evans,et al.  Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. , 2001, Cerebral cortex.

[34]  A. Toga,et al.  Mapping sulcal pattern asymmetry and local cortical surface gray matter distribution in vivo: maturation in perisylvian cortices. , 2002, Cerebral cortex.

[35]  G. Bruyn Atlas of the Cerebral Sulci, M. Ono, S. Kubik, Chad D. Abernathey (Eds.). Georg Thieme Verlag, Stuttgart, New York (1990), 232, DM 298 , 1990 .

[36]  Jessica Dubois,et al.  Brain Development of the Preterm Neonate after Neonatal Hydrocortisone Treatment for Chronic Lung Disease Patients and Methods , 2022 .

[37]  Katrin Amunts,et al.  Broca's region: Cytoarchitectonic asymmetry and developmental changes , 2003, The Journal of comparative neurology.

[38]  J. Hajnal,et al.  Abnormal Cortical Development after Premature Birth Shown by Altered Allometric Scaling of Brain Growth , 2006, PLoS medicine.

[39]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[40]  C. Garel,et al.  Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. , 2001, AJNR. American journal of neuroradiology.

[41]  Lucie Hertz-Pannier,et al.  Nature and nurture in language acquisition: anatomical and functional brain-imaging studies in infants , 2006, Trends in Neurosciences.