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      Structural and functional asymmetry of the language network emerge in early childhood

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          Highlights

          • Macrostructural asymmetry of the arcuate fasciculus is present by age 2 years.

          • Microstructural and functional asymmetry in the IFG increases across early childhood.

          • Left arcuate microstructure is related to pre-reading language skills.

          • Asymmetry is not related to pre-reading skills in early childhood.

          Abstract

          Structural and functional neuroimaging studies show language and reading processes are left-lateralized, and associated with a dispersed group of left brain regions. However, it is unclear when and how asymmetry of these regions emerges. We characterized the development of structural and functional asymmetry of the language network in 386 datasets from 117 healthy children (58 male) across early childhood (2–7.5 years). Structural asymmetry was investigated using diffusion tensor imaging (DTI) and manual delineation of the arcuate fasciculus. Functional connectivity asymmetry was calculated from seed regions in the inferior frontal gyrus (IFG) and middle temporal gyrus (MTG). We show that macrostructural asymmetry of the arcuate fasciculus is present by age 2 years, while leftward asymmetry of microstructure and functional connectivity with the IFG increases across the age range. This emerging microstructural and functional asymmetry likely underlie the development of language and reading skills during this time.

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          Most cited references44

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          An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data.

          Several recent reports in large, independent samples have demonstrated the influence of motion artifact on resting-state functional connectivity MRI (rsfc-MRI). Standard rsfc-MRI preprocessing typically includes regression of confounding signals and band-pass filtering. However, substantial heterogeneity exists in how these techniques are implemented across studies, and no prior study has examined the effect of differing approaches for the control of motion-induced artifacts. To better understand how in-scanner head motion affects rsfc-MRI data, we describe the spatial, temporal, and spectral characteristics of motion artifacts in a sample of 348 adolescents. Analyses utilize a novel approach for describing head motion on a voxelwise basis. Next, we systematically evaluate the efficacy of a range of confound regression and filtering techniques for the control of motion-induced artifacts. Results reveal that the effectiveness of preprocessing procedures on the control of motion is heterogeneous, and that improved preprocessing provides a substantial benefit beyond typical procedures. These results demonstrate that the effect of motion on rsfc-MRI can be substantially attenuated through improved preprocessing procedures, but not completely removed. Copyright © 2012 Elsevier Inc. All rights reserved.
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            Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language.

            Despite intensive work on language-brain relations, and a fairly impressive accumulation of knowledge over the last several decades, there has been little progress in developing large-scale models of the functional anatomy of language that integrate neuropsychological, neuroimaging, and psycholinguistic data. Drawing on relatively recent developments in the cortical organization of vision, and on data from a variety of sources, we propose a new framework for understanding aspects of the functional anatomy of language which moves towards remedying this situation. The framework posits that early cortical stages of speech perception involve auditory fields in the superior temporal gyrus bilaterally (although asymmetrically). This cortical processing system then diverges into two broad processing streams, a ventral stream, which is involved in mapping sound onto meaning, and a dorsal stream, which is involved in mapping sound onto articulatory-based representations. The ventral stream projects ventro-laterally toward inferior posterior temporal cortex (posterior middle temporal gyrus) which serves as an interface between sound-based representations of speech in the superior temporal gyrus (again bilaterally) and widely distributed conceptual representations. The dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian fissure at the parietal-temporal boundary (area Spt), and ultimately projecting to frontal regions. This network provides a mechanism for the development and maintenance of "parity" between auditory and motor representations of speech. Although the proposed dorsal stream represents a very tight connection between processes involved in speech perception and speech production, it does not appear to be a critical component of the speech perception process under normal (ecologically natural) listening conditions, that is, when speech input is mapped onto a conceptual representation. We also propose some degree of bi-directionality in both the dorsal and ventral pathways. We discuss some recent empirical tests of this framework that utilize a range of methods. We also show how damage to different components of this framework can account for the major symptom clusters of the fluent aphasias, and discuss some recent evidence concerning how sentence-level processing might be integrated into the framework.
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              Ventral and dorsal pathways for language.

              Built on an analogy between the visual and auditory systems, the following dual stream model for language processing was suggested recently: a dorsal stream is involved in mapping sound to articulation, and a ventral stream in mapping sound to meaning. The goal of the study presented here was to test the neuroanatomical basis of this model. Combining functional magnetic resonance imaging (fMRI) with a novel diffusion tensor imaging (DTI)-based tractography method we were able to identify the most probable anatomical pathways connecting brain regions activated during two prototypical language tasks. Sublexical repetition of speech is subserved by a dorsal pathway, connecting the superior temporal lobe and premotor cortices in the frontal lobe via the arcuate and superior longitudinal fascicle. In contrast, higher-level language comprehension is mediated by a ventral pathway connecting the middle temporal lobe and the ventrolateral prefrontal cortex via the extreme capsule. Thus, according to our findings, the function of the dorsal route, traditionally considered to be the major language pathway, is mainly restricted to sensory-motor mapping of sound to articulation, whereas linguistic processing of sound to meaning requires temporofrontal interaction transmitted via the ventral route.
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                Author and article information

                Contributors
                Journal
                Dev Cogn Neurosci
                Dev Cogn Neurosci
                Developmental Cognitive Neuroscience
                Elsevier
                1878-9293
                1878-9307
                21 July 2019
                October 2019
                21 July 2019
                : 39
                : 100682
                Affiliations
                [a ]Department of Radiology, Canada
                [b ]Owerko Centre, Alberta Children Hospital Research Institute, Canada
                [c ]Hotchkiss Brain Institute, Canada
                [d ]Department of Neuroscience, Canada
                [e ]Cumming School of Medicine, Canada
                [f ]Department of Pediatrics, Canada
                [g ]Department of Community Health Sciences, Canada
                Author notes
                [* ]Corresponding Author at: Room B4-513, Alberta Children’s Hospital, 28 Oki Drive NW, Calgary, Alberta, T3B 6A8, Canada. clebel@ 123456ucalgary.ca
                Article
                S1878-9293(19)30107-0 100682
                10.1016/j.dcn.2019.100682
                6969356
                31376589
                02c0c49f-1cb1-4be6-b361-6bd2cca6ace3
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 21 March 2019
                : 18 June 2019
                : 17 July 2019
                Categories
                Original Research

                Neurosciences
                diffusion tensor imaging,resting state fmri,asymmetry,lateralization,prereading,arcuate fasciculus

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