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      Differential Signatures of Second Language Syntactic Performance and Age on the Structural Properties of the Left Dorsal Pathway

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          Abstract

          In adult second language (L2) acquisition, individual differences are considerably large even among people with similar experiences. The neural mechanisms underlying this variability would include structural plasticity of language-related pathways. To elucidate such neuroplasticity, we focused on the transitional period of adolescence, which is associated with certain plasticity toward maturation following the sensitive period of language acquisition (≤12 years old). The adolescent brain would thus be influenced by age-dependent factors, as well as performances in L2. Here, we examined individual differences in L2 performances controlling the duration of experience to reveal the differential signatures of performances and age on the plasticity of structural properties in major language-related pathways. We recruited Japanese students at two ages, i.e., junior (age: 13–14) and senior (age: 16–17) high-school students, all of whom started to expose to English at age 12 or 13. We divided them into subgroups, so that either L2 performance [Junior (High)/Senior (Low)] or age [Senior (Low)/Senior (High)] was matched in group comparisons; the duration of L2 experience was also controlled between the Senior (Low) and Senior (High) groups. We then examined the thickness and fractional anisotropy (FA) of the dorsal and ventral pathways, i.e., the arcuate fasciculus (Arcuate) and inferior fronto-occipital fasciculus (IFOF), respectively, using semi-automatic methods for selecting regions without branches. Regarding FA in the left Arcuate, the Senior (High) group showed significantly higher FA than the other two groups, indicating performance-related group differences. Further, FA in the left Arcuate was selectively correlated with the accuracy of a syntactic task. Regarding the thickness of the left Arcuate, the Senior (High) and Senior (Low) groups showed significantly larger thickness than the Junior (High) group, indicating age-related group differences. These differential performance-related and age-related signatures were evident on the left Arcuate alone, in contrast to the right Arcuate that showed only mild differences in thickness, and to the bilateral IFOF that lacked either signature. Our results suggest that the left dorsal pathway continued to develop to adolescence, and that performance differences in a syntactic task can be predicted by its FA, independent of age and the duration of experience.

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          Perisylvian language networks of the human brain.

          Early anatomically based models of language consisted of an arcuate tract connecting Broca's speech and Wernicke's comprehension centers; a lesion of the tract resulted in conduction aphasia. However, the heterogeneous clinical presentations of conduction aphasia suggest a greater complexity of perisylvian anatomical connections than allowed for in the classical anatomical model. This article re-explores perisylvian language connectivity using in vivo diffusion tensor magnetic resonance imaging tractography. Diffusion tensor magnetic resonance imaging data from 11 right-handed healthy male subjects were averaged, and the arcuate fasciculus of the left hemisphere reconstructed from this data using an interactive dissection technique. Beyond the classical arcuate pathway connecting Broca's and Wernicke's areas directly, we show a previously undescribed, indirect pathway passing through inferior parietal cortex. The indirect pathway runs parallel and lateral to the classical arcuate fasciculus and is composed of an anterior segment connecting Broca's territory with the inferior parietal lobe and a posterior segment connecting the inferior parietal lobe to Wernicke's territory. This model of two parallel pathways helps explain the diverse clinical presentations of conduction aphasia. The anatomical findings are also relevant to the evolution of language, provide a framework for Lichtheim's symptom-based neurological model of aphasia, and constrain, anatomically, contemporary connectionist accounts of language.
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            Longitudinal development of human brain wiring continues from childhood into adulthood.

            Healthy human brain development is a complex process that continues during childhood and adolescence, as demonstrated by many cross-sectional and several longitudinal studies. However, whether these changes end in adolescence is not clear. We examined longitudinal white matter maturation using diffusion tensor tractography in 103 healthy subjects aged 5-32 years; each volunteer was scanned at least twice, with 221 total scans. Fractional anisotropy (FA) and mean diffusivity (MD), parameters indicative of factors including myelination and axon density, were assessed in 10 major white matter tracts. All tracts showed significant nonlinear development trajectories for FA and MD. Significant within-subject changes occurred in the vast majority of children and early adolescents, and these changes were mostly complete by late adolescence for projection and commissural tracts. However, association tracts demonstrated postadolescent within-subject maturation of both FA and MD. Diffusion parameter changes were due primarily to decreasing perpendicular diffusivity, although increasing parallel diffusivity contributed to the prolonged increases of FA in association tracts. Volume increased significantly with age for most tracts, and longitudinal measures also demonstrated postadolescent volume increases in several association tracts. As volume increases were not directly associated with either elevated FA or reduced MD between scans, the observed diffusion parameter changes likely reflect microstructural maturation of brain white matter tracts rather than just gross anatomy.
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              Sexual dimorphism of brain developmental trajectories during childhood and adolescence.

              Human total brain size is consistently reported to be approximately 8-10% larger in males, although consensus on regionally specific differences is weak. Here, in the largest longitudinal pediatric neuroimaging study reported to date (829 scans from 387 subjects, ages 3 to 27 years), we demonstrate the importance of examining size-by-age trajectories of brain development rather than group averages across broad age ranges when assessing sexual dimorphism. Using magnetic resonance imaging (MRI) we found robust male/female differences in the shapes of trajectories with total cerebral volume peaking at age 10.5 in females and 14.5 in males. White matter increases throughout this 24-year period with males having a steeper rate of increase during adolescence. Both cortical and subcortical gray matter trajectories follow an inverted U shaped path with peak sizes 1 to 2 years earlier in females. These sexually dimorphic trajectories confirm the importance of longitudinal data in studies of brain development and underline the need to consider sex matching in studies of brain development.
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                Author and article information

                Contributors
                Journal
                Front Psychol
                Front Psychol
                Front. Psychol.
                Frontiers in Psychology
                Frontiers Media S.A.
                1664-1078
                23 May 2017
                2017
                : 8
                : 829
                Affiliations
                [1] 1Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo Tokyo, Japan
                [2] 2Japan Society for the Promotion of Science Saitama, Japan
                [3] 3Japan Agency for Medical Research and Development – Core Research for Evolutional Science and Technology Tokyo, Japan
                Author notes

                Edited by: Niels O. Schiller, Leiden University, Netherlands

                Reviewed by: Bencie Woll, University College London, United Kingdom; Yang Zhang, University of Minnesota, United States

                *Correspondence: Kuniyoshi L. Sakai, sakai@ 123456mind.c.u-tokyo.ac.jp

                This article was submitted to Language Sciences, a section of the journal Frontiers in Psychology

                Article
                10.3389/fpsyg.2017.00829
                5440582
                851f838a-25b3-4f59-a3b7-07746aaa87de
                Copyright © 2017 Yamamoto and Sakai.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 December 2016
                : 08 May 2017
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 35, Pages: 13, Words: 0
                Categories
                Psychology
                Original Research

                Clinical Psychology & Psychiatry
                diffusion mri,white matter,dorsal and ventral pathways,language acquisition,syntax

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