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      Diffusion tractography reveals pervasive asymmetry of cerebral white matter tracts in the bottlenose dolphin ( Tursiops truncatus)

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          Abstract

          Brain enlargement is associated with concomitant growth of interneuronal distance, increased conduction time, and reduced neuronal interconnectivity. Recognition of these functional constraints led to the hypothesis that large-brained mammals should exhibit greater structural and functional brain lateralization. As a taxon with the largest brains in the animal kingdom, Cetacea provides a unique opportunity to examine asymmetries of brain structure and function. In the present study, diffusion tensor imaging and tractography were used to investigate cerebral white matter asymmetry in the bottlenose dolphin ( Tursiops truncatus). Widespread white matter asymmetries were observed with the preponderance of tracts exhibiting leftward structural asymmetries. Leftward lateralization may reflect differential processing and execution of behaviorally variant sensory and motor functions by the cerebral hemispheres. The arcuate fasciculus, an association tract linked to human language evolution, was isolated and exhibited rightward asymmetry suggesting a right hemisphere bias for conspecific communication unlike that of most mammals. This study represents the first examination of cetacean white matter asymmetry and constitutes an important step toward understanding potential drivers of structural asymmetry and its role in underpinning functional and behavioral lateralization in cetaceans.

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          The online version of this article (doi:10.1007/s00429-017-1525-9) contains supplementary material, which is available to authorized users.

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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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            DTI tractography of the human brain's language pathways.

            Diffusion Tensor Imaging (DTI) tractography has been used to detect leftward asymmetries in the arcuate fasciculus, a pathway that links temporal and inferior frontal language cortices. In this study, we more specifically define this asymmetry with respect to both anatomy and function. Twenty right-handed male subjects were scanned with DTI, and the arcuate fasciculus was reconstructed using deterministic tractography. The arcuate was divided into 2 segments with different hypothesized functions, one terminating in the posterior superior temporal gyrus (STG) and another terminating in the middle temporal gyrus (MTG). Tractography results were compared with peak activation coordinates from prior functional neuroimaging studies of phonology, lexical-semantic processing, and prosodic processing to assign putative functions to these pathways. STG terminations were strongly left lateralized and overlapped with phonological activations in the left but not the right hemisphere, suggesting that only the left hemisphere phonological cortex is directly connected with the frontal lobe via the arcuate fasciculus. MTG terminations were also strongly left lateralized, overlapping with left lateralized lexical-semantic activations. Smaller right hemisphere MTG terminations overlapped with right lateralized prosodic activations. We combine our findings with a recent model of brain language processing to explain 6 aphasia syndromes.
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              Laterality index in functional MRI: methodological issues☆

              In functional magnetic resonance imaging (fMRI), hemispheric dominance is generally indicated by a measure called the laterality index (LI). The assessment of a meaningful LI measure depends on several methodological factors that should be taken into account when interpreting LI values or comparing between subjects. Principally, these include the nature of the quantification of left and right hemispheres contributions, localisation of volumes of interest within each hemisphere, dependency on statistical threshold, thresholding LI values, choice of activation and baseline conditions and reproducibility of LI values. This review discusses such methodological factors and the different approaches that have been suggested to deal with them. Although these factors are common to a range of fMRI domains, they are discussed here in the context of fMRI of the language system.
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                Author and article information

                Contributors
                alexandrakwright@gmail.com
                Journal
                Brain Struct Funct
                Brain Struct Funct
                Brain Structure & Function
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1863-2653
                1863-2661
                30 November 2017
                30 November 2017
                2018
                : 223
                : 4
                : 1697-1711
                Affiliations
                [1 ]ISNI 0000 0004 0627 2787, GRID grid.217200.6, Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, , University of California-San Diego, ; La Jolla, CA 92093 USA
                [2 ]ISNI 0000 0004 0627 2787, GRID grid.217200.6, Department of Radiology, , University of California-San Diego, ; La Jolla, CA 92093 USA
                [3 ]ISNI 0000 0004 0611 5554, GRID grid.419692.1, National Marine Mammal Foundation, ; San Diego, CA 92106 USA
                [4 ]ISNI 0000 0004 0627 2787, GRID grid.217200.6, Center for Functional MRI, Department of Radiology, , University of California-San Diego, ; La Jolla, CA 92093 USA
                Author information
                http://orcid.org/0000-0002-7794-5008
                Article
                1525
                10.1007/s00429-017-1525-9
                5884918
                29189908
                f0022671-0b98-4a7b-bc51-6a483ae0c876
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 28 June 2016
                : 6 July 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: Graduate Research Fellowship Program
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007911, University of California, San Diego;
                Award ID: Graduate Division Fellowship
                Award Recipient :
                Funded by: Scripps Institution of Oceanography
                Award ID: Graduate Fellowship
                Award Recipient :
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                Neurology
                arcuate fasciculus,asymmetry,bottlenose dolphin (tursiops truncatus),diffusion tensor imaging (dti),tractography,white matter

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