The chaotic morphology of the left superior temporal sulcus is genetically constrained

ABSTRACT The asymmetry of the superior temporal sulcus (STS) has been identified as a species‐specific feature of the human brain. The so‐called superior temporal asymmetrical pit (STAP) area is observed from the last trimester of gestation onwards and is far less pronounced in the chimpanzee brain. This asymmetry is associated with more frequent sulcal interruptions, named plis de passage (PPs), leading to the irregular morphology of the left sulcus. In this paper, we aimed to characterize the variability, asymmetry, and heritability of these interruptions in the STS in comparison with the other main sulci. We developed an automated method to extract PPs across the cortex based on a highly reproducible grid of sulcal pits across individuals, which we applied to a subset of Human Connectome Project (HCP) subjects (N=820). We report that only a few PPs across the cortex are genetically constrained, namely in the collateral, postcentral and superior temporal sulci and the calcarine fissure. Moreover, some PPs occur more often in one hemisphere than the other, namely in the precentral, postcentral, intraparietal sulci, as well as in both inferior and superior temporal sulci. Most importantly, we found that only the interruptions within the STAP region are both asymmetric and genetically constrained. Because this morphological pattern is located in an area of the left hemisphere related to speech, our results suggest structural constraints on the architecture of the linguistic network. HIGHLIGHTSSuperior temporal sulcus (STS) asymmetry is confirmed in a cohort of 820 subjects.Sulcal interruptions named plis de passage (PPs) are a specific human trait.The STS presents a leftward asymmetry of PPs and is the most asymmetric sulcus.The presence of PPs in the left STS is under moderate genetic control.These properties suggest structural constraints on the linguistic network.

[1]  Jean-Francois Mangin,et al.  Larger is twistier: Spectral analysis of gyrification (SPANGY) applied to adult brain size polymorphism , 2012, NeuroImage.

[2]  C. Sherwood,et al.  Relaxed genetic control of cortical organization in human brains compared with chimpanzees , 2015, Proceedings of the National Academy of Sciences.

[3]  Rutvik H. Desai,et al.  Specialization along the Left Superior Temporal Sulcus for Auditory Categorization , 2010, Cerebral cortex.

[4]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[5]  Marc Brysbaert,et al.  New human-specific brain landmark: The depth asymmetry of superior temporal sulcus , 2015, Proceedings of the National Academy of Sciences.

[6]  J. Lefévre,et al.  On the growth and form of cortical convolutions , 2016, Nature Physics.

[7]  L. Almasy,et al.  Multipoint quantitative-trait linkage analysis in general pedigrees. , 1998, American journal of human genetics.

[8]  Vincent Frouin,et al.  Genetic Influence on the Sulcal Pits: On the Origin of the First Cortical Folds , 2018, Cerebral cortex.

[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]  M. Petrides,et al.  Morphological patterns of the postcentral sulcus in the human brain , 2010, The Journal of comparative neurology.

[11]  Steen Moeller,et al.  The Human Connectome Project: A data acquisition perspective , 2012, NeuroImage.

[12]  N. Gaab,et al.  Atypical Sulcal Pattern in Children with Developmental Dyslexia and At-Risk Kindergarteners. , 2016, Cerebral cortex.

[13]  J. Gilmore,et al.  Spatial Patterns, Longitudinal Development, and Hemispheric Asymmetries of Cortical Thickness in Infants from Birth to 2 Years of Age , 2015, The Journal of Neuroscience.

[14]  Bernard J. Ransil,et al.  Associations of handedness with hair color and learning disabilities , 1987, Neuropsychologia.

[15]  O. Houdé,et al.  Early Cerebral Constraints on Reading Skills in School‐Age Children: An MRI Study , 2016 .

[16]  Michael Petrides,et al.  Morphological patterns of the intraparietal sulcus and the anterior intermediate parietal sulcus of Jensen in the human brain , 2014, Proceedings of the Royal Society B: Biological Sciences.

[17]  Jean-Francois Mangin,et al.  Sulcal pattern and morphology of the superior temporal sulcus , 2004, NeuroImage.

[18]  Michael Petrides,et al.  Morphological patterns of the collateral sulcus in the human brain , 2012, The European journal of neuroscience.

[19]  T. R. Kumar The spatial distribution , 2000 .

[20]  Nancy Kanwisher,et al.  Functional Organization of Social Perception and Cognition in the Superior Temporal Sulcus , 2015, Cerebral cortex.

[21]  C. Frith,et al.  Social Cognition in Humans , 2007, Current Biology.

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

[23]  Elia Formisano,et al.  Processing of Natural Sounds in Human Auditory Cortex: Tonotopy, Spectral Tuning, and Relation to Voice Sensitivity , 2012, The Journal of Neuroscience.

[24]  Mert R. Sabuncu,et al.  A Surface-based Analysis of Language Lateralization and Cortical Asymmetry , 2013, Journal of Cognitive Neuroscience.

[25]  Denis Rivière,et al.  Sulcus Identification and Labeling , 2015 .

[26]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[27]  William D. Hopkins,et al.  Evolution of the Central Sulcus Morphology in Primates , 2014, Brain, Behavior and Evolution.

[28]  J. Rauschecker,et al.  Phoneme and word recognition in the auditory ventral stream , 2012, Proceedings of the National Academy of Sciences.

[29]  Robert T. Knight,et al.  Superior Temporal SulcusIt's My Area: Or Is It? , 2008, Journal of Cognitive Neuroscience.

[30]  C. Walsh,et al.  Molecular approaches to brain asymmetry and handedness , 2006, Nature Reviews Neuroscience.

[31]  J. McClure,et al.  Time is of the essence , 2004, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[32]  Bertrand Thirion,et al.  Exploring the Early Organization and Maturation of Linguistic Pathways in the Human Infant Brain. , 2016, Cerebral cortex.

[33]  Antonio Moreno,et al.  Brain correlates of constituent structure in sign language comprehension , 2018, NeuroImage.

[34]  D. Geschwind,et al.  Functional and Evolutionary Insights into Human Brain Development through Global Transcriptome Analysis , 2009, Neuron.

[35]  N. A. Borghese,et al.  A functional-anatomical model for lipreading. , 2003, Journal of neurophysiology.

[36]  Jean-Baptiste Poline,et al.  Genetic Variants of FOXP2 and KIAA0319/TTRAP/THEM2 Locus Are Associated with Altered Brain Activation in Distinct Language-Related Regions , 2012, The Journal of Neuroscience.

[37]  Otto W. Witte,et al.  Cortical representation of the anal canal , 1998 .

[38]  Elizabeth Redcay,et al.  Perceived communicative intent in gesture and language modulates the superior temporal sulcus , 2016, Human brain mapping.

[39]  R. Kahn,et al.  Genetic influences on human brain structure: A review of brain imaging studies in twins , 2007, Human brain mapping.

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

[41]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[42]  D. V. von Cramon,et al.  Deep sulcal landmarks provide an organizing framework for human cortical folding. , 2008, Cerebral cortex.

[43]  C. Francks,et al.  Left–Right Asymmetry of Maturation Rates in Human Embryonic Neural Development , 2017, Biological Psychiatry.

[44]  D Bavelier,et al.  Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Christine Chiarello,et al.  Structural asymmetry of the human cerebral cortex: Regional and between-subject variability of surface area, cortical thickness, and local gyrification , 2016, Neuropsychologia.

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

[47]  Paul M. Thompson,et al.  Genetics of Primary Cerebral Gyrification: Heritability of Length, Depth and Area of Primary Sulci in an Extended Pedigree of Papio Baboons , 2022 .

[48]  David C. Van Essen,et al.  Human Connectome Project , 2014, Encyclopedia of Computational Neuroscience.

[49]  Bertrand Thirion,et al.  Early Maturation of the Linguistic Dorsal Pathway in Human Infants , 2011, The Journal of Neuroscience.

[50]  T. Paus,et al.  Brain size and folding of the human cerebral cortex. , 2008, Cerebral cortex.

[51]  D. Woods,et al.  Hemispheric asymmetries in cortical and subcortical anatomy , 2015, Laterality.

[52]  Jean-Francois Mangin,et al.  Cortical sulci recognition and spatial normalization , 2011, Medical Image Anal..

[53]  Paul M. Thompson,et al.  On the Genetic Architecture of Cortical Folding and Brain Volume in Primates , 2022 .

[54]  O. Güntürkün,et al.  Ontogenesis of Lateralization , 2017, Neuron.

[55]  Katrin Amunts,et al.  The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. , 2008, Cerebral cortex.

[56]  A. Turken,et al.  The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses , 2011, Front. Syst. Neurosci..

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

[58]  Mohammed El Amine Bechar,et al.  Semi-automated Method for the Glaucoma Monitoring , 2018 .

[59]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[60]  S. Dehaene,et al.  Cortical representation of the constituent structure of sentences , 2011, Proceedings of the National Academy of Sciences.

[61]  Patrice Y. Simard,et al.  Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. , 1994, Cerebral cortex.

[62]  Glenn D. Rosen,et al.  Planum temporale asymmetry, reappraisal since Geschwind and Levitsky , 1987, Neuropsychologia.

[63]  G. McCarthy,et al.  When Strangers Pass , 2004, Psychological science.

[64]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[65]  Jerry L Prince,et al.  Automated Sulcal Segmentation Using Watersheds on the Cortical Surface , 2002, NeuroImage.

[66]  C. Francks,et al.  Lateralization of gene expression in human language cortex , 2015, Cortex.

[67]  Jean-Francois Mangin,et al.  Regional study of the genetic influence on the sulcal pits , 2017, 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017).

[68]  Hidenao Fukuyama,et al.  The contribution of cortical thickness and surface area to gray matter asymmetries in the healthy human brain , 2014, Human Brain Mapping.

[69]  J. Hutsler The specialized structure of human language cortex: Pyramidal cell size asymmetries within auditory and language-associated regions of the temporal lobes , 2003, Brain and Language.

[70]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[71]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[72]  K. Specht,et al.  The functional and structural asymmetries of the superior temporal sulcus. , 2018, Scandinavian journal of psychology.

[73]  Dinggang Shen,et al.  Spatial distribution and longitudinal development of deep cortical sulcal landmarks in infants , 2014, NeuroImage.

[74]  Dinggang Shen,et al.  Characterization of U-shape streamline fibers: Methods and applications , 2014, Medical Image Anal..

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

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

[77]  P. Belin,et al.  Anatomo-functional correspondence in the superior temporal sulcus , 2017, Brain Structure and Function.

[78]  Alan C. Evans,et al.  Depth potential function for folding pattern representation, registration and analysis , 2009, Medical Image Anal..

[79]  Guillaume Auzias,et al.  Deep sulcal landmarks: Algorithmic and conceptual improvements in the definition and extraction of sulcal pits , 2015, NeuroImage.

[80]  Colin Studholme,et al.  Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. , 2012, Cerebral cortex.

[81]  Camino de Juan Romero,et al.  Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly , 2015, The EMBO journal.

[82]  R. Schweizer,et al.  Revisiting a historic human brain with magnetic resonance imaging – the first description of a divided central sulcus , 2014, Front. Neuroanat..

[83]  Richard M. Leahy,et al.  Article in Press G Model Journal of Neuroscience Methods Semi-automated Method for Delineation of Landmarks on Models of the Cerebral Cortex , 2022 .

[84]  Keith Johnson,et al.  Phonetic Feature Encoding in Human Superior Temporal Gyrus , 2014, Science.

[85]  O. Güntürkün,et al.  FOXP2 variation modulates functional hemispheric asymmetries for speech perception , 2013, Brain and Language.

[86]  D. Weinberger,et al.  Genetic variability of human brain size and cortical gyral patterns. , 1997, Brain : a journal of neurology.

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

[88]  Dacheng Tao,et al.  Variation in longitudinal trajectories of cortical sulci in normal elderly , 2018, NeuroImage.

[89]  Guillaume Auzias,et al.  Automatic sulcal line extraction on cortical surfaces using geodesic path density maps , 2012, NeuroImage.

[90]  Michael S. Beauchamp,et al.  A neural basis for interindividual differences in the McGurk effect, a multisensory speech illusion , 2012, NeuroImage.

[91]  Jean-Francois Mangin,et al.  A robust cerebral asymmetry in the infant brain: The rightward superior temporal sulcus , 2011, NeuroImage.

[92]  B. Mazoyer,et al.  Regional correlations between cortical thickness and surface area asymmetries: A surface-based morphometry study of 250 adults , 2016, Neuropsychologia.