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      Decreased Gray-Matter Volume in Insular Cortex as a Correlate of Singers’ Enhanced Sensorimotor Control of Vocal Production

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          Abstract

          Accumulating evidence has shown enhanced sensorimotor control of vocal production as a consequence of extensive singing experience. The neural basis of this ability, however, is poorly understood. Given that the insula mediates motor aspects of vocal production, the present study investigated structural plasticity in insula induced by singing experience and its link to auditory feedback control of vocal production. Voxel-based morphometry (VBM) was used to examine the differences in gray matter (GM) volume in the insula of 21 singers and 21 non-singers. An auditory feedback perturbation paradigm was used to examine the differences in auditory-motor control of vocal production between singers and non-singers. Both groups vocalized sustained vowels while hearing their voice unexpectedly pitch-shifted −50 or −200 cents (200 ms duration). VBM analyses showed that singers exhibited significantly lower GM volumes in the bilateral insula than non-singers. When exposed to pitch perturbations in voice auditory feedback, singers involuntarily compensated for pitch perturbations in voice auditory feedback to a significantly lesser degree than non-singers. Moreover, across the two sizes of pitch perturbations, the magnitudes of vocal compensations were positively correlated with the total regional GM volumes in the bilateral insula. These results indicate that extensive singing training leads to decreased GM volumes in insula and suggest that morphometric plasticity in insula contributes to the enhanced sensorimotor control of vocal production observed in singers.

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          Most cited references67

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          Three Systems of Insular Functional Connectivity Identified with Cluster Analysis

          Despite much research on the function of the insular cortex, few studies have investigated functional subdivisions of the insula in humans. The present study used resting-state functional connectivity magnetic resonance imaging (MRI) to parcellate the human insular lobe based on clustering of functional connectivity patterns. Connectivity maps were computed for each voxel in the insula based on resting-state functional MRI (fMRI) data and segregated using cluster analysis. We identified 3 insular subregions with distinct patterns of connectivity: a posterior region, functionally connected with primary and secondary somatomotor cortices; a dorsal anterior to middle region, connected with dorsal anterior cingulate cortex, along with other regions of a previously described control network; and a ventral anterior region, primarily connected with pregenual anterior cingulate cortex. Applying these regions to a separate task data set, we found that dorsal and ventral anterior insula responded selectively to disgusting images, while posterior insula did not. These results demonstrate that clustering of connectivity patterns can be used to subdivide cerebral cortex into anatomically and functionally meaningful subregions; the insular regions identified here should be useful in future investigations on the function of the insula.
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            A new brain region for coordinating speech articulation.

            Human speech requires complex planning and coordination of mouth and tongue movements. Certain types of brain injury can lead to a condition known as apraxia of speech, in which patients are impaired in their ability to coordinate speech movements but their ability to perceive speech sounds, including their own errors, is unaffected. The brain regions involved in coordinating speech, however, remain largely unknown. In this study, brain lesions of 25 stroke patients with a disorder in the motor planning of articulatory movements were compared with lesions of 19 patients without such deficits. A robust double dissociation was found between these two groups. All patients with articulatory planning deficits had lesions that included a discrete region of the left precentral gyrus of the insula, a cortical area beneath the frontal and temporal lobes. This area was completely spared in all patients without these articulation deficits. Thus this area seems to be specialized for the motor planning of speech.
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              Brain structures differ between musicians and non-musicians.

              From an early age, musicians learn complex motor and auditory skills (e.g., the translation of visually perceived musical symbols into motor commands with simultaneous auditory monitoring of output), which they practice extensively from childhood throughout their entire careers. Using a voxel-by-voxel morphometric technique, we found gray matter volume differences in motor, auditory, and visual-spatial brain regions when comparing professional musicians (keyboard players) with a matched group of amateur musicians and non-musicians. Although some of these multiregional differences could be attributable to innate predisposition, we believe they may represent structural adaptations in response to long-term skill acquisition and the repetitive rehearsal of those skills. This hypothesis is supported by the strong association we found between structural differences, musician status, and practice intensity, as well as the wealth of supporting animal data showing structural changes in response to long-term motor training. However, only future experiments can determine the relative contribution of predisposition and practice.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                02 August 2019
                2019
                : 13
                : 815
                Affiliations
                [1] 1Department of Rehabilitation Medicine, The First Affiliated Hospital, Sun Yat-sen University , Guangzhou, China
                [2] 2Department of Rehabilitation, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University , Guangzhou, China
                [3] 3Department of Music, Guangdong University of Education , Guangzhou, China
                [4] 4Department of Rehabilitation, Zhujiang Hospital, Southern Medical University , Guangzhou, China
                [5] 5Psychology Department and Laurier Centre for Cognitive Neuroscience, Wilfrid Laurier University , Waterloo, ON, Canada
                [6] 6State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University , Beijing, China
                [7] 7Guangdong Provincial Key Laboratory of Brain Function and Disease, Zhongshan School of Medicine, Sun Yat-sen University , Guangzhou, China
                Author notes

                Edited by: Yi Du, Institute of Psychology (CAS), China

                Reviewed by: Boris Kleber, Aarhus University, Denmark; Xing Tian, New York University Shanghai, China

                *Correspondence: Gaolang Gong, gaolang.gong@ 123456bnu.edu.cn

                These authors have contributed equally to this work

                This article was submitted to Auditory Cognitive Neuroscience, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2019.00815
                6688740
                30906246
                c481bd48-202d-4321-8414-4ba07920f6cc
                Copyright © 2019 Wang, Wei, Chen, Jones, Gong and Liu.

                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) and the copyright owner(s) 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
                : 27 January 2019
                : 22 July 2019
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 93, Pages: 12, Words: 0
                Categories
                Neuroscience
                Original Research

                Neurosciences
                auditory feedback,speech motor control,voxel-based morphology,insula,singing
                Neurosciences
                auditory feedback, speech motor control, voxel-based morphology, insula, singing

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