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      The role of functional and structural interhemispheric auditory connectivity for language lateralization - A combined EEG and DTI study

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          Abstract

          Interhemispheric connectivity between auditory areas is highly relevant for normal auditory perception and alterations are a major factor for the development of auditory verbal hallucinations. Surprisingly, there is no combined EEG-DTI study directly addressing the role of functional and structural connectivity in the same group of subjects. Accordingly, nothing is known about the relationship between functional connectivity such as gamma-band synchrony, structural integrity of the interhemispheric auditory pathways (IAPs) and language lateralization as well as whether the gamma-band synchrony is configured on the backbone of IAPs. By applying multimodal imaging of 64-channel EEG and DTI tractography, we investigated in 27 healthy volunteers the functional gamma-band synchrony between either bilateral primary or secondary auditory cortices from eLORETA source-estimation during dichotic listening, as well as the correspondent IAPs from which fractional anisotropy (FA) values were extracted. Correlation and regression analyses revealed highest values for gamma-band synchrony, followed by FA for secondary auditory cortices, which were both significantly related to a reduced language lateralization. There was no such association between the white-matter microstructure and gamma-band synchrony, suggesting that structural connectivity might also be relevant for other (minor) aspects of information transfer in addition to gamma-band synchrony, which are not detected in the present coupling analyses. The combination of multimodal EEG-DTI imaging provides converging evidence of neural correlates by showing that both stronger pathways and increased gamma-band synchrony within one cohort of subjects are related to a reduced leftward-lateralization for language.

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          Gamma rhythms are commonly observed in many brain regions during both waking and sleep states, yet their functions and mechanisms remain a matter of debate. Here we review the cellular and synaptic mechanisms underlying gamma oscillations and outline empirical questions and controversial conceptual issues. Our main points are as follows: First, gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition. Second, gamma oscillations are short-lived and typically emerge from the coordinated interaction of excitation and inhibition, which can be detected as local field potentials. Third, gamma rhythm typically concurs with irregular firing of single neurons, and the network frequency of gamma oscillations varies extensively depending on the underlying mechanism. To document gamma oscillations, efforts should be made to distinguish them from mere increases of gamma-band power and/or increased spiking activity. Fourth, the magnitude of gamma oscillation is modulated by slower rhythms. Such cross-frequency coupling may serve to couple active patches of cortical circuits. Because of their ubiquitous nature and strong correlation with the "operational modes" of local circuits, gamma oscillations continue to provide important clues about neuronal population dynamics in health and disease.
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            Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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              The brain contains more than 100 billion neurons that communicate with each other via axons for the formation of complex neural networks. The structural mapping of such networks during health and disease states is essential for understanding brain function. However, our understanding of brain structural connectivity is surprisingly limited, due in part to the lack of noninvasive methodologies to study axonal anatomy. Diffusion tensor imaging (DTI) is a recently developed MRI technique that can measure macroscopic axonal organization in nervous system tissues. In this article, the principles of DTI methodologies are explained, and several applications introduced, including visualization of axonal tracts in myelin and axonal injuries as well as human brain and mouse embryonic development. The strengths and limitations of DTI and key areas for future research and development are also discussed.
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                Author and article information

                Contributors
                s.steinmann@uke.uni-hamburg.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                18 October 2018
                18 October 2018
                2018
                : 8
                : 15428
                Affiliations
                [1 ]ISNI 0000 0001 2180 3484, GRID grid.13648.38, Psychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, , University Medical Center Hamburg-Eppendorf, ; Hamburg, Germany
                [2 ]ISNI 0000 0001 2180 3484, GRID grid.13648.38, Department of Neurology, , University Medical Center Hamburg- Eppendorf, ; 20246 Hamburg, Germany
                [3 ]ISNI 0000 0001 2180 3484, GRID grid.13648.38, Department of Neurophysiology and Pathophysiology, , University Medical Center Hamburg-Eppendorf, ; 20246 Hamburg, Germany
                [4 ]ISNI 0000 0001 2165 8627, GRID grid.8664.c, Centre for Psychiatry and Psychotherapy, Justus-Liebig-University, ; Giessen, Germany
                Author information
                http://orcid.org/0000-0003-2434-1822
                Article
                33586
                10.1038/s41598-018-33586-6
                6194074
                30337548
                1e2fe6f6-326b-4fd8-b5df-c7a4f19ffdcd
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 2 May 2018
                : 1 October 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: SFB936
                Award ID: SFB 936
                Award ID: SFB 936
                Award ID: SFB 936
                Award ID: SFB 936
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