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      Hyperacusis is associated with smaller gray matter volumes in the supplementary motor area

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          Highlights

          • Hyperacusis is characterized by hypersensitivity to ordinary environmental sounds.

          • Gray matter in the supplementary motor area is reduced in hyperacusis.

          • Sound-evoked responses are increased in the same brain region.

          • Our results suggest impaired motor responses to sound in hyperacusis.

          Abstract

          Hyperacusis is a disorder in loudness perception characterized by increased sensitivity to ordinary environmental sounds and associated with otologic conditions, including hearing loss and tinnitus (the phantom perception of sound) as well as neurologic and neuropsychiatric conditions. Hyperacusis is believed to arise centrally in the brain; however, the underlying causes are unknown. To gain insight into differences in brain morphology associated with hyperacusis, we undertook a retrospective case-control study comparing whole-brain gray matter morphology in participants with sensorineural hearing loss and tinnitus who either scored above or below the threshold for hyperacusis based on a standard questionnaire. We found that participants reporting hyperacusis had smaller gray matter volumes and cortical sheet thicknesses in the right supplementary motor area (SMA), independent of anxiety, depression, tinnitus burden, or sex. In fact, the right SMA volumes extracted from an independently defined volume of interest could accurately classify participants. Finally, in a subset of participants where functional data were also available, we found that individuals with hyperacusis showed increased sound-evoked responses in the right SMA compared to individuals without hyperacusis. Given the role of the SMA in initiating motion, these results suggest that in hyperacusis the SMA is involved in a motor response to sounds.

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              This paper describes DARTEL, which is an algorithm for diffeomorphic image registration. It is implemented for both 2D and 3D image registration and has been formulated to include an option for estimating inverse consistent deformations. Nonlinear registration is considered as a local optimisation problem, which is solved using a Levenberg-Marquardt strategy. The necessary matrix solutions are obtained in reasonable time using a multigrid method. A constant Eulerian velocity framework is used, which allows a rapid scaling and squaring method to be used in the computations. DARTEL has been applied to intersubject registration of 471 whole brain images, and the resulting deformations were evaluated in terms of how well they encode the shape information necessary to separate male and female subjects and to predict the ages of the subjects.
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                29 April 2023
                2023
                29 April 2023
                : 38
                : 103425
                Affiliations
                [a ]Department of Otorhinolaryngology-Head and Neck Surgery, University of Groningen, University Medical Centre Groningen, P.O. Box 30.001, 9700 RB Groningen, the Netherlands
                [b ]Graduate School of Medical Sciences (Research School of Behavioural and Cognitive Neurosciences), University of Groningen, FA30, P.O. Box 196, 9700 AD Groningen, the Netherlands
                [c ]Department of Radiology, Massachusetts General Hospital-Harvard Medical School, Boston, USA
                Author notes
                [* ]Corresponding author at: Department of Otorhinolaryngology-Head and Neck Surgery, University of Groningen, University Medical Centre Groningen, P.O. Box 30.001, 9700 RB Groningen, the Netherlands. p.makani@ 123456umcg.nl
                [1]

                These authors contributed equally to this work.

                Article
                S2213-1582(23)00114-6 103425
                10.1016/j.nicl.2023.103425
                10176058
                232c03ec-e6cf-4386-bd32-69be8f9df3df
                © 2023 The Author(s)

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

                History
                : 2 March 2023
                : 21 April 2023
                : 26 April 2023
                Categories
                Regular Article

                audition,hearing loss,hypersensitivity,sound-evoked functional mri,surface-based morphometry,tinnitus,voxel-based morphometry

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