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      Impaired naming performance in temporal lobe epilepsy: language fMRI responses are modulated by disease characteristics

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          Abstract

          Objective

          To investigate alterations of language networks and their relation to impaired naming performance in temporal lobe epilepsy (TLE) using functional MRI.

          Methods

          Seventy-two adult TLE patients (41 left) and 36 controls were studied with overt auditory and picture naming fMRI tasks to assess temporal lobe language areas, and a covert verbal fluency task to probe frontal lobe language regions. Correlation of fMRI activation with clinical naming scores, and alteration of language network patterns in relation to epilepsy duration, age at onset and seizure frequency, were investigated with whole-brain multiple regression analyses.

          Results

          Auditory and picture naming fMRI activated the left posterior temporal lobe, and stronger activation correlated with better clinical naming scores. Verbal fluency MRI mainly activated frontal lobe regions. In left and right TLE, a later age of epilepsy onset related to stronger temporal lobe activations, while earlier age of onset was associated with impaired deactivation of extratemporal regions. In left TLE patients, longer disease duration and higher seizure frequency were associated with reduced deactivation. Frontal lobe language networks were unaffected by disease characteristics.

          Conclusions

          While frontal lobe language regions appear spared, temporal lobe language areas are susceptible to dysfunction and reorganisation, particularly in left TLE. Early onset and long duration of epilepsy, and high seizure frequency, were associated with compromised activation and deactivation patterns of task-associated regions, which might account for impaired naming performance in individuals with TLE.

          Electronic supplementary material

          The online version of this article (10.1007/s00415-020-10116-x) contains supplementary material, which is available to authorized users.

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          Most cited references44

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          The assessment and analysis of handedness: The Edinburgh inventory

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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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              Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies.

              Semantic memory refers to knowledge about people, objects, actions, relations, self, and culture acquired through experience. The neural systems that store and retrieve this information have been studied for many years, but a consensus regarding their identity has not been reached. Using strict inclusion criteria, we analyzed 120 functional neuroimaging studies focusing on semantic processing. Reliable areas of activation in these studies were identified using the activation likelihood estimate (ALE) technique. These activations formed a distinct, left-lateralized network comprised of 7 regions: posterior inferior parietal lobe, middle temporal gyrus, fusiform and parahippocampal gyri, dorsomedial prefrontal cortex, inferior frontal gyrus, ventromedial prefrontal cortex, and posterior cingulate gyrus. Secondary analyses showed specific subregions of this network associated with knowledge of actions, manipulable artifacts, abstract concepts, and concrete concepts. The cortical regions involved in semantic processing can be grouped into 3 broad categories: posterior multimodal and heteromodal association cortex, heteromodal prefrontal cortex, and medial limbic regions. The expansion of these regions in the human relative to the nonhuman primate brain may explain uniquely human capacities to use language productively, plan, solve problems, and create cultural and technological artifacts, all of which depend on the fluid and efficient retrieval and manipulation of semantic knowledge.
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                Author and article information

                Contributors
                k.trimmel@ucl.ac.uk
                Journal
                J Neurol
                J Neurol
                Journal of Neurology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0340-5354
                1432-1459
                3 August 2020
                3 August 2020
                2021
                : 268
                : 1
                : 147-160
                Affiliations
                [1 ]GRID grid.452379.e, ISNI 0000 0004 0386 7187, Epilepsy Society MRI Unit, , Chalfont Centre for Epilepsy, ; Chalfont St Peter, SL9 0LR UK
                [2 ]GRID grid.83440.3b, ISNI 0000000121901201, Department of Clinical and Experimental Epilepsy, , UCL Queen Square Institute of Neurology, ; Queen Square, London, WC1N 3BG UK
                [3 ]GRID grid.22937.3d, ISNI 0000 0000 9259 8492, Department of Neurology, , Medical University of Vienna, ; 1090 Vienna, Austria
                Author information
                http://orcid.org/0000-0002-9203-5344
                Article
                10116
                10.1007/s00415-020-10116-x
                7815622
                32747979
                cabad974-57f0-4da4-8b85-2582690a26b8
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 12 May 2020
                : 23 July 2020
                : 24 July 2020
                Funding
                Funded by: NIHR UCLH Biomedical Research Centre
                Funded by: Epilepsy Society Chalfont St. Peter
                Funded by: European Academy of Neurology
                Funded by: Austrian Society of Neurology
                Funded by: Brain Research UK
                Categories
                Original Communication
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2021

                Neurology
                language fmri,reorganisation,temporal lobe epilepsy,naming impairment,disease characteristics,deactivation

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