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      The Neural Correlates of Chronic Symptoms of Vertigo Proneness in Humans

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          Abstract

          Vestibular signals are of significant importance for variable functions including gaze stabilization, spatial perception, navigation, cognition, and bodily self-consciousness. The vestibular network governs functions that might be impaired in patients affected with vestibular dysfunction. It is currently unclear how different brain regions/networks process vestibular information and integrate the information into a unified spatial percept related to somatosensory awareness and whether people with recurrent balance complaints have a neural signature as a trait affecting their development of chronic symptoms of vertigo. Pivotal evidence points to a vestibular-related brain network in humans that is widely distributed in nature. By using resting state source localized electroencephalography in non-vertiginous state, electrophysiological changes in activity and functional connectivity of 23 patients with balance complaints where chronic symptoms of vertigo and dizziness are among the most common reported complaints are analyzed and compared to healthy subjects. The analyses showed increased alpha2 activity within the posterior cingulate cortex and the precuneues/cuneus and reduced beta3 and gamma activity within the pregenual and subgenual anterior cingulate cortex for the subjects with balance complaints. These electrophysiological variations were correlated with reported chronic symptoms of vertigo intensity. A region of interest analysis found reduced functional connectivity for gamma activity within the vestibular cortex, precuneus, frontal eye field, intra-parietal sulcus, orbitofrontal cortex, and the dorsal anterior cingulate cortex. In addition, there was a positive correlation between chronic symptoms of vertigo intensity and increased alpha-gamma nesting in the left frontal eye field. When compared to healthy subjects, there is evidence of electrophysiological changes in the brain of patients with balance complaints even outside chronic symptoms of vertigo episodes. This suggests that these patients have a neural signature or trait that makes them prone to developing chronic balance problems.

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          Emotion, decision making and the orbitofrontal cortex.

          The somatic marker hypothesis provides a systems-level neuroanatomical and cognitive framework for decision making and the influence on it by emotion. The key idea of this hypothesis is that decision making is a process that is influenced by marker signals that arise in bioregulatory processes, including those that express themselves in emotions and feelings. This influence can occur at multiple levels of operation, some of which occur consciously and some of which occur non-consciously. Here we review studies that confirm various predictions from the hypothesis. The orbitofrontal cortex represents one critical structure in a neural system subserving decision making. Decision making is not mediated by the orbitofrontal cortex alone, but arises from large-scale systems that include other cortical and subcortical components. Such structures include the amygdala, the somatosensory/insular cortices and the peripheral nervous system. Here we focus only on the role of the orbitofrontal cortex in decision making and emotional processing, and the relationship between emotion, decision making and other cognitive functions of the frontal lobe, namely working memory.
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            10/20, 10/10, and 10/5 systems revisited: their validity as relative head-surface-based positioning systems.

            With the advent of multi-channel EEG hardware systems and the concurrent development of topographic and tomographic signal source localization methods, the international 10/20 system, a standard system for electrode positioning with 21 electrodes, was extended to higher density electrode settings such as 10/10 and 10/5 systems, allowing more than 300 electrode positions. However, their effectiveness as relative head-surface-based positioning systems has not been examined. We previously developed a virtual 10/20 measurement algorithm that can analyze any structural MR head and brain image. Extending this method to the virtual 10/10 and 10/5 measurement algorithms, we analyzed the MR images of 17 healthy subjects. The acquired scalp positions of the 10/10 and 10/5 systems were normalized to the Montreal Neurological Institute (MNI) stereotactic coordinates and their spatial variability was assessed. We described and examined the effects of spatial variability due to the selection of positioning systems and landmark placement strategies. As long as a detailed rule for a particular system was provided, it yielded precise landmark positions on the scalp. Moreover, we evaluated the effective spatial resolution of 329 scalp landmark positions of the 10/5 system for multi-subject studies. As long as a detailed rule for landmark setting was provided, 241 scalp positions could be set effectively when there was no overlapping of two neighboring positions. Importantly, 10/10 positions could be well separated on a scalp without overlapping. This study presents a referential framework for establishing the effective spatial resolutions of 10/20, 10/10, and 10/5 systems as relative head-surface-based positioning systems.
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              Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization.

              Cortical activity and perception are not driven by the external stimulus alone; rather sensory information has to be integrated with various other internal constraints such as expectations, recent memories, planned actions, etc. The question is how large scale integration over many remote and size-varying processes might be performed by the brain. We have conducted a series of EEG recordings during processes thought to involve neuronal assemblies of varying complexity. While local synchronization during visual processing evolved in the gamma frequency range, synchronization between neighboring temporal and parietal cortex during multimodal semantic processing evolved in a lower, the beta1 (12-18 Hz) frequency range, and long range fronto-parietal interactions during working memory retention and mental imagery evolved in the theta and alpha (4-8 Hz, 8-12 Hz) frequency range. Thus, a relationship seems to exist between the extent of functional integration and the synchronization-frequency. In particular, long-range interactions in the alpha and theta ranges seem specifically involved in processing of internal mental context, i.e. for top-down processing. We propose that large scale integration is performed by synchronization among neurons and neuronal assemblies evolving in different frequency ranges.
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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
                18 April 2016
                2016
                : 11
                : 4
                : e0152309
                Affiliations
                [1 ]Lab for Clinical & Integrative Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Dallas, United States of America
                [2 ]BRAI 2N, Sint Augustinus Hospital Antwerp, Antwerp, Belgium
                [3 ]ENT Department, Sint Augustinus Hospital Antwerp, European Institute for ORL-HNS, Antwerp, Belgium
                [4 ]Department of Surgical Sciences, Section of Neurosurgery, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand
                UMR8194, FRANCE
                Author notes

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

                Performed the experiments: JO RV CB. Analyzed the data: OA JO DDR SV. Wrote the paper: OA DDR SV. Collected the data: RV CB.

                Article
                PONE-D-15-46956
                10.1371/journal.pone.0152309
                4835222
                27089185
                f3e98c9f-1379-4171-a889-9d16f9b3c7e3
                © 2016 Alsalman 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
                : 26 October 2015
                : 11 March 2016
                Page count
                Figures: 5, Tables: 2, Pages: 20
                Funding
                The authors have no support or funding to report.
                Categories
                Research Article
                Medicine and Health Sciences
                Otorhinolaryngology
                Otology
                Vertigo
                Biology and Life Sciences
                Anatomy
                Brain
                Cingulate Cortex
                Medicine and Health Sciences
                Anatomy
                Brain
                Cingulate Cortex
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Geriatrics
                Balance and Falls
                Engineering and Technology
                Civil Engineering
                Transportation Infrastructure
                Canals
                Engineering and Technology
                Transportation
                Transportation Infrastructure
                Canals
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Brain Electrophysiology
                Electroencephalography
                Medicine and Health Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Neurophysiology
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Electroencephalography
                Medicine and Health Sciences
                Diagnostic Medicine
                Clinical Neurophysiology
                Electroencephalography
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Electroencephalography
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Brain Electrophysiology
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Brain Electrophysiology
                Medicine and Health Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Brain Electrophysiology
                Biology and Life Sciences
                Neuroscience
                Neurophysiology
                Brain Electrophysiology
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
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                Sensory Perception
                Vision
                Custom metadata
                This study was approved by the local ethical committee (Sint Augustinus Hospital Antwerp) and was in accordance with the declaration of Helsinki. Collection of the data was under approval of IRB GZA OGA85 and all patients gave written informed consent. Data are available for researchers who meet the criteria for access to confidential data as indicated by the IRB GZA OGA85 ethics committee. For more information you may contact the authors at: ola.alsalman@ 123456utdallas.edu , and/or sven.vanneste@ 123456utdallas.edu .

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