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      Disrupted connectivity within visual, attentional and salience networks in the visual snow syndrome

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          Abstract

          Here we investigate brain functional connectivity in patients with visual snow syndrome (VSS). Our main objective was to understand more about the underlying pathophysiology of this neurological syndrome. Twenty‐four patients with VSS and an equal number of gender and age‐matched healthy volunteers attended MRI sessions in which whole‐brain maps of functional connectivity were acquired under two conditions: at rest while watching a blank screen and during a visual paradigm consisting of a visual‐snow like stimulus. Eight unilateral seed regions were selected a priori based on previous observations and hypotheses; four seeds were placed in key anatomical areas of the visual pathways and the remaining were derived from a pre‐existing functional analysis. The between‐group analysis showed that patients with VSS had hyper and hypoconnectivity between key visual areas and the rest of the brain, both in the resting state and during a visual stimulation, compared with controls. We found altered connectivity internally within the visual network; between the thalamus/basal ganglia and the lingual gyrus; between the visual motion network and both the default mode and attentional networks. Further, patients with VSS presented decreased connectivity during external sensory input within the salience network, and between V5 and precuneus. Our results suggest that VSS is characterised by a widespread disturbance in the functional connectivity of several brain systems. This dysfunction involves the pre‐cortical and cortical visual pathways, the visual motion network, the attentional networks and finally the salience network; further, it represents evidence of ongoing alterations both at rest and during visual stimulus processing.

          Abstract

          This study investigates the functional connectivity of visual snow syndrome, compared to that of healthy controls. The results suggest that VSS is characterised by a widespread dysfunction in the functional connectivity of several brain systems, mostly the pre‐cortical and cortical visual pathways, the visual motion network, the attentional networks and the salience network. The investigation shows evidence of ongoing alterations both at rest and during visual stimulus processing in this poorly‐known and disabling neurological condition.

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          Most cited references52

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          Headache Classification Committee of the International Headache Society (IHS) The International Classification of Headache Disorders, 3rd edition

          (2018)
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            Parallel organization of functionally segregated circuits linking basal ganglia and cortex.

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              A default mode of brain function.

              A baseline or control state is fundamental to the understanding of most complex systems. Defining a baseline state in the human brain, arguably our most complex system, poses a particular challenge. Many suspect that left unconstrained, its activity will vary unpredictably. Despite this prediction we identify a baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF. The OEF is defined as the ratio of oxygen used by the brain to oxygen delivered by flowing blood and is remarkably uniform in the awake but resting state (e.g., lying quietly with eyes closed). Local deviations in the OEF represent the physiological basis of signals of changes in neuronal activity obtained with functional MRI during a wide variety of human behaviors. We used quantitative metabolic and circulatory measurements from positron-emission tomography to obtain the OEF regionally throughout the brain. Areas of activation were conspicuous by their absence. All significant deviations from the mean hemisphere OEF were increases, signifying deactivations, and resided almost exclusively in the visual system. Defining the baseline state of an area in this manner attaches meaning to a group of areas that consistently exhibit decreases from this baseline, during a wide variety of goal-directed behaviors monitored with positron-emission tomography and functional MRI. These decreases suggest the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
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                Author and article information

                Contributors
                francesca.puledda@kcl.ac.uk
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                15 January 2021
                May 2021
                : 42
                : 7 ( doiID: 10.1002/hbm.v42.7 )
                : 2032-2044
                Affiliations
                [ 1 ] Headache Group, Department of Basic and Clinical Neuroscience King's College London London United Kingdom
                [ 2 ] NIHR‐Wellcome Trust King's Clinical Research Facility SLaM NIHR Biomedical Research Centre, King's College Hospital London United Kingdom
                [ 3 ] Centre for Neuroimaging Sciences, Department of Neuroimaging King's College London London United Kingdom
                [ 4 ] Department of Neurology Inselspital, Bern University Hospital, University of Bern Bern Switzerland
                [ 5 ] Department of Old Age Psychiatry Institute of Psychiatry, Psychology & Neuroscience, King's College London London United Kingdom
                Author notes
                [*] [* ] Correspondence

                Francesca Puledda, King's College London, London SE5 9PJ, UK.

                Email: francesca.puledda@ 123456kcl.ac.uk

                Author information
                https://orcid.org/0000-0002-1933-4049
                https://orcid.org/0000-0003-3260-5904
                Article
                HBM25343
                10.1002/hbm.25343
                8046036
                33448525
                749e8bb4-4fb2-42b8-9686-d1fbfc6355db
                © 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 December 2020
                : 07 September 2020
                : 04 January 2021
                Page count
                Figures: 4, Tables: 3, Pages: 13, Words: 10160
                Funding
                Funded by: National Institute for Health Research , open-funder-registry 10.13039/501100000272;
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                May 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.2 mode:remove_FC converted:14.04.2021

                Neurology
                functional connectivity,magnetic resonance imaging,migraine,photophobia,prolonged visual disturbance,salience network,visual motion network,visual snow syndrome

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