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      Multimodal MR-imaging reveals large-scale structural and functional connectivity changes in profound early blindness

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          Abstract

          In the setting of profound ocular blindness, numerous lines of evidence demonstrate the existence of dramatic anatomical and functional changes within the brain. However, previous studies based on a variety of distinct measures have often provided inconsistent findings. To help reconcile this issue, we used a multimodal magnetic resonance (MR)-based imaging approach to provide complementary structural and functional information regarding this neuroplastic reorganization. This included gray matter structural morphometry, high angular resolution diffusion imaging (HARDI) of white matter connectivity and integrity, and resting state functional connectivity MRI (rsfcMRI) analysis. When comparing the brains of early blind individuals to sighted controls, we found evidence of co-occurring decreases in cortical volume and cortical thickness within visual processing areas of the occipital and temporal cortices respectively. Increases in cortical volume in the early blind were evident within regions of parietal cortex. Investigating white matter connections using HARDI revealed patterns of increased and decreased connectivity when comparing both groups. In the blind, increased white matter connectivity (indexed by increased fiber number) was predominantly left-lateralized, including between frontal and temporal areas implicated with language processing. Decreases in structural connectivity were evident involving frontal and somatosensory regions as well as between occipital and cingulate cortices. Differences in white matter integrity (as indexed by quantitative anisotropy, or QA) were also in general agreement with observed pattern changes in the number of white matter fibers. Analysis of resting state sequences showed evidence of both increased and decreased functional connectivity in the blind compared to sighted controls. Specifically, increased connectivity was evident between temporal and inferior frontal areas. Decreases in functional connectivity were observed between occipital and frontal and somatosensory-motor areas and between temporal (mainly fusiform and parahippocampus) and parietal, frontal, and other temporal areas. Correlations in white matter connectivity and functional connectivity observed between early blind and sighted controls showed an overall high degree of association. However, comparing the relative changes in white matter and functional connectivity between early blind and sighted controls did not show a significant correlation. In summary, these findings provide complimentary evidence, as well as highlight potential contradictions, regarding the nature of regional and large scale neuroplastic reorganization resulting from early onset blindness.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 March 2017
                2017
                : 12
                : 3
                : e0173064
                Affiliations
                [1 ]Laboratory for Visual Neuroplasticity. Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, MA, United States of America
                [2 ]Center for Biomedical Imaging. Boston University School of Medicine, Boston, MA, United States of America
                [3 ]Crossmodal Perception and Plasticity Laboratory. University of Trento, Trento, Italy
                Chinese Academy of Sciences, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: LBM.

                • Data curation: CMB GVH.

                • Formal analysis: CMB GVH LZ BBK LBM.

                • Funding acquisition: LBM.

                • Investigation: CMB LBM.

                • Methodology: LBM.

                • Project administration: LBM.

                • Resources: CMB LBM.

                • Software: BBK.

                • Supervision: LBM.

                • Validation: LBM.

                • Visualization: CMB GVH LZ LBM.

                • Writing – original draft: LBM.

                • Writing – review & editing: CMB GVH LZ OC LBM.

                Author information
                http://orcid.org/0000-0002-8094-9536
                Article
                PONE-D-16-28241
                10.1371/journal.pone.0173064
                5362049
                28328939
                71bd0386-6def-4cdd-a84e-f3a3af75fdef
                © 2017 Bauer et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 14 July 2016
                : 14 February 2017
                Page count
                Figures: 5, Tables: 4, Pages: 26
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: EY019924
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100001818, Research to Prevent Blindness;
                Award Recipient :
                This work was supported by grants from the NIH/NEI (RO1 EY019924), the Low Vision Research Award from Research to Prevent Blindness (RPB), and the Lions Clubs International Foundation (LCIF) to LBM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Ophthalmology
                Visual Impairments
                Blindness
                Biology and Life Sciences
                Anatomy
                Nervous System
                Central Nervous System
                Medicine and Health Sciences
                Anatomy
                Nervous System
                Central Nervous System
                Research and Analysis Methods
                Imaging Techniques
                Morphometry
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Biology and Life Sciences
                Anatomy
                Brain
                Cerebral Cortex
                Parietal Lobe
                Medicine and Health Sciences
                Anatomy
                Brain
                Cerebral Cortex
                Parietal Lobe
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Brain Morphometry
                Surface-Based Morphometry
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Surface-Based Morphometry
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Surface-Based Morphometry
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Surface-Based Morphometry
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Brain Morphometry
                Surface-Based Morphometry
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Brain Morphometry
                Surface-Based Morphometry
                Research and Analysis Methods
                Imaging Techniques
                Morphometry
                Surface-Based Morphometry
                Biology and Life Sciences
                Anatomy
                Brain
                Cerebral Cortex
                Occipital Lobe
                Medicine and Health Sciences
                Anatomy
                Brain
                Cerebral Cortex
                Occipital Lobe
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognition
                Custom metadata
                Data are available from the MEEI-Harvard Institutional Data Access / Ethics Committee for researchers who meet the criteria for access to confidential data. Restrictions are imposed to protect patient identities and not to prohibit public sharing of any or all data. Any questions can be addressed to Fariba_Houman@ 123456meei.harvard.edu of the MEEI-Harvard Institutional Data Access / Ethics Committee or the corresponding author.

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