Syntactic and Semantic Specialization and Integration in 5- to 6-Year-Old Children during Auditory Sentence Processing

Previous studies have found specialized syntactic and semantic processes in the adult brain during language comprehension. Young children have sophisticated semantic and syntactic aspects of language, yet many previous fMRI studies failed to detect this specialization, possibly due to experimental design and analytical methods. In this current study, 5- to 6-year-old children completed a syntactic task and a semantic task to dissociate these two processes. Multivoxel pattern analysis was used to examine the correlation of patterns within a task (between runs) or across tasks. We found that the left middle temporal gyrus showed more similar patterns within the semantic task compared with across tasks, whereas there was no difference in the correlation within the syntactic task compared with across tasks, suggesting its specialization in semantic processing. Moreover, the left superior temporal gyrus showed more similar patterns within both the semantic task and the syntactic task as compared with across tasks, suggesting its role in integration of semantic and syntactic information. In contrast to the temporal lobe, we did not find specialization or integration effects in either the opercular or triangular part of the inferior frontal gyrus. Overall, our study showed that 5- to 6-year-old children have already developed specialization and integration in the temporal lobe, but not in the frontal lobe, consistent with developmental neurocognitive models of language comprehension in typically developing young children.

[1]  Michael W. Spratling,et al.  Précis of neuroconstructivism: how the brain constructs cognition. , 2008, The Behavioral and brain sciences.

[2]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[3]  Eun Sook Park,et al.  Diffusion-tensor magnetic resonance imaging in children with language impairment , 2006, Neuroreport.

[4]  Pauline Dibbets,et al.  Functional MRI of Task Switching in Children with Specific Language Impairment (SLI) , 2006, Neurocase.

[5]  G. Conti-Ramsden,et al.  Language Development and Assessment in the Preschool Period , 2012, Neuropsychology Review.

[6]  Angela D. Friederici,et al.  The ontogeny of the cortical language network , 2016, Nature Reviews Neuroscience.

[7]  Rebecca Treiman,et al.  The English Lexicon Project , 2007, Behavior research methods.

[8]  Mirjana Bozic,et al.  Syntactic Complexity and Frequency in the Neurocognitive Language System , 2017, Journal of Cognitive Neuroscience.

[9]  U. Hasson,et al.  On the Same Wavelength: Predictable Language Enhances Speaker–Listener Brain-to-Brain Synchrony in Posterior Superior Temporal Gyrus , 2014, The Journal of Neuroscience.

[10]  Jill de Villiers,et al.  Early judgments of semantic and syntactic acceptability by children , 1972 .

[11]  Angela D. Friederici,et al.  Functional Neural Networks of Semantic and Syntactic Processes in the Developing Brain , 2007, Journal of Cognitive Neuroscience.

[12]  Angela D. Friederici,et al.  Left prefrontal cortex activation during sentence comprehension covaries with grammatical knowledge in children , 2012, NeuroImage.

[13]  Mark H. Johnson.  Functional brain development in humans , 2001, Nature Reviews Neuroscience.

[14]  S. Scott,et al.  Retrieving meaning after temporal lobe infarction: The role of the basal language area , 2004, Annals of neurology.

[15]  D. Entwisle,et al.  Semantic and syntactic development in children. , 1973 .

[16]  A. Friederici.  Towards a neural basis of auditory sentence processing , 2002, Trends in Cognitive Sciences.

[17]  A. Morgan,et al.  Neural correlates of childhood language disorder: a systematic review , 2015, Developmental medicine and child neurology.

[18]  Jennifer M. Rodd,et al.  Brain structures underlying lexical processing of speech: Evidence from brain imaging , 2011 .

[19]  Russell A. Poldrack,et al.  Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses , 2012, NeuroImage.

[20]  Eric Wanner,et al.  Language acquisition: the state of the art , 1982 .

[21]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[22]  Angela D. Friederici,et al.  Who did what to whom? The neural basis of argument hierarchies during language comprehension , 2005, NeuroImage.

[23]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[24]  Angela D. Friederici,et al.  Preschoolers' brains rely on semantic cues prior to the mastery of syntax during sentence comprehension , 2016, NeuroImage.

[25]  Jarrod A. Lewis-Peacock,et al.  Multi-Voxel Pattern Analysis of fMRI Data , 2014 .

[26]  Angela D. Friederici,et al.  Reviewing the functional basis of the syntactic Merge mechanism for language: A coordinate-based activation likelihood estimation meta-analysis , 2017, Neuroscience & Biobehavioral Reviews.

[27]  Jonas Obleser,et al.  Disentangling syntax and intelligibility in auditory language comprehension , 2009, Human brain mapping.

[28]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Angela D. Friederici,et al.  Phonotactic Knowledge and Lexical-Semantic Processing in One-year-olds: Brain Responses to Words and Nonsense Words in Picture Contexts , 2005, Journal of Cognitive Neuroscience.

[30]  James R. Booth,et al.  Task dependent lexicality effects support interactive models of reading: A meta-analytic neuroimaging review , 2015, Neuropsychologia.

[31]  A. Friederici,et al.  Syntactic event-related potential components in 24-month-olds’ sentence comprehension , 2006, Neuroreport.

[32]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[33]  Angela D Friederici,et al.  The neural basis for human syntax: Broca's area and beyond , 2018, Current Opinion in Behavioral Sciences.

[34]  J. Obleser,et al.  Expectancy constraints in degraded speech modulate the language comprehension network. , 2010, Cerebral cortex.

[35]  Morag Stuart,et al.  Children's printed word database: continuities and changes over time in children's early reading vocabulary. , 2010, British journal of psychology.

[36]  G. Glover,et al.  Methods and Software for fMRI Analysis of Clinical Subjects , 2009, NeuroImage.

[37]  M. Rice.  Toward epigenetic and gene regulation models of specific language impairment: looking for links among growth, genes, and impairments , 2012, Journal of Neurodevelopmental Disorders.

[38]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[39]  A. Karmiloff-Smith.  Development itself is the key to understanding developmental disorders , 1998, Trends in Cognitive Sciences.

[40]  Jens Brauer,et al.  Brain Functional and Structural Predictors of Language Performance. , 2016, Cerebral cortex.

[41]  Paul A. Taylor,et al.  AFNI and Clustering: False Positive Rates Redux , 2016, bioRxiv.

[42]  Angela D. Friederici,et al.  Neural Correlates of Syntactic Processing in Two-Year-Olds , 2005, Journal of Cognitive Neuroscience.

[43]  Angela D. Friederici,et al.  The language skeleton after dissecting meaning: A functional segregation within Broca's Area , 2015, NeuroImage.

[44]  Mark H. Johnson.  Interactive Specialization: A domain-general framework for human functional brain development? , 2011, Developmental Cognitive Neuroscience.

[45]  H. Tager-Flusberg,et al.  Present and future possibilities for defining a phenotype for specific language impairment. , 1999, Journal of speech, language, and hearing research : JSLHR.

[46]  A. Friederici.  The cortical language circuit: from auditory perception to sentence comprehension , 2012, Trends in Cognitive Sciences.

[47]  Angela D. Friederici,et al.  Syntax gradually segregates from semantics in the developing brain , 2014, NeuroImage.

[48]  P. Kuhl.  Brain Mechanisms in Early Language Acquisition , 2010, Neuron.

[49]  Sylvia Vitello,et al.  Localising semantic and syntactic processing in spoken and written language comprehension: An Activation Likelihood Estimation meta-analysis , 2015, Brain and Language.

[50]  Scott Holland,et al.  CerebroMatic: A Versatile Toolbox for Spline-Based MRI Template Creation , 2017, Front. Comput. Neurosci..

[51]  Jens Timmer,et al.  Network modulation during complex syntactic processing , 2012, NeuroImage.

[52]  Peter Hagoort,et al.  The neurobiology of language beyond single words. , 2014, Annual review of neuroscience.

[53]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[54]  N. Kanwisher,et al.  Lexical and syntactic representations in the brain: An fMRI investigation with multi-voxel pattern analyses , 2011, Neuropsychologia.

[55]  F. Liégeois,et al.  Brain basis of childhood speech and language disorders: are we closer to clinically meaningful MRI markers? , 2016, Current opinion in pediatrics.