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      Erroneously Disgusted: fMRI Study Supports Disgust-Related Neural Reuse in Obsessive-Compulsive Disorder (OCD)

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          Abstract

          Objective: fMRI scans of patients with obsessive-compulsive disorder (OCD) consistently show a hyperactivity of the insular cortex, a region responsible for disgust-processing, when confronted with symptom-triggering stimuli. This asks for an investigation of the role of disgust and the insula in OCD patients.

          Methods: Seventeen inpatients with OCD and 17 healthy controls (HC) underwent fMRI scanning. Whole-brain contrasts were calculated for “Disgust vs. Neutral” for both groups, plus an analysis of variance (ANOVA) to assess the interaction between group and condition. Additionally, the emotional dimensions of valence and arousal, along with the ability to cope, were assessed by picture ratings.

          Results: The picture ratings confirmed the patients’ heightened sensitivity to disgust with higher values for arousal and inability to cope, but not for valence. fMRI scans revealed no hyperactivity of the insula in patients compared to controls for the condition “Disgust vs. Neutral,” indicating no basic hypersensitivity to disgusting stimuli. Increased activity in the precuneus in controls for this condition might correspond to the downregulation of arousal.

          Conclusions: The absent differences in neural activity of the insula in patients compared to controls for the disgust-condition, but heightened activity for symptom-provoking conditions, suggests that the illness is due to an erroneous recruitment of the insula cortex for OCD-stimuli. The finding is interpreted within the framework of the neural reuse hypothesis.

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          Most cited references38

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          Cultural recycling of cortical maps.

          Part of human cortex is specialized for cultural domains such as reading and arithmetic, whose invention is too recent to have influenced the evolution of our species. Representations of letter strings and of numbers occupy reproducible locations within large-scale macromaps, respectively in the left occipito-temporal and bilateral intraparietal cortex. Furthermore, recent fMRI studies reveal a systematic architecture within these areas. To explain this paradoxical cerebral invariance of cultural maps, we propose a neuronal recycling hypothesis, according to which cultural inventions invade evolutionarily older brain circuits and inherit many of their structural constraints.
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            Neural reuse: a fundamental organizational principle of the brain.

            An emerging class of theories concerning the functional structure of the brain takes the reuse of neural circuitry for various cognitive purposes to be a central organizational principle. According to these theories, it is quite common for neural circuits established for one purpose to be exapted (exploited, recycled, redeployed) during evolution or normal development, and be put to different uses, often without losing their original functions. Neural reuse theories thus differ from the usual understanding of the role of neural plasticity (which is, after all, a kind of reuse) in brain organization along the following lines: According to neural reuse, circuits can continue to acquire new uses after an initial or original function is established; the acquisition of new uses need not involve unusual circumstances such as injury or loss of established function; and the acquisition of a new use need not involve (much) local change to circuit structure (e.g., it might involve only the establishment of functional connections to new neural partners). Thus, neural reuse theories offer a distinct perspective on several topics of general interest, such as: the evolution and development of the brain, including (for instance) the evolutionary-developmental pathway supporting primate tool use and human language; the degree of modularity in brain organization; the degree of localization of cognitive function; and the cortical parcellation problem and the prospects (and proper methods to employ) for function to structure mapping. The idea also has some practical implications in the areas of rehabilitative medicine and machine interface design.
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              Remembering pictures: pleasure and arousal in memory.

              Incidental memory performance for pictures that varied along the affective dimensions of pleasantness and arousal was assessed. For both an immediate and delayed (1 year later) free-recall task, only the arousal dimension had a stable effect on memory performance: Pictures rated as highly arousing were remembered better than low-arousal stimuli. This effect was corroborated in a speeded recognition test, in which high-arousal materials encoded earlier in the experiment produced faster reaction times than their low-arousal counterparts. Pleasantness affected reaction time decisions only for pictures not encoded earlier. These results suggest that whereas both the dimensions of pleasantness and arousal are processed at initial encoding, long-term memory performance is mainly affected by arousal.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                24 April 2019
                2019
                : 13
                : 81
                Affiliations
                [1] 1Institute for Synergetics and Psychotherapy Research, Paracelsus Medical University , Salzburg, Austria
                [2] 2Department of Psychosomatics and Inpatient Psychotherapy, Paracelsus Medical University , Salzburg, Austria
                [3] 3Department of Psychology, Ludwig Maximilian University of Munich , Munich, Germany
                [4] 4Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital, Ludwig Maximilian University , Munich, Germany
                [5] 5Department for Psychosomatics and Inpatient Psychotherapy, Paracelsus Medical University , Salzburg, Austria
                [6] 6Centre for Cognitive Neuroscience, University of Salzburg , Salzburg, Austria
                [7] 7Neuroscience Institute, Christian Doppler Clinic, University Hospital Salzburg , Salzburg, Austria
                [8] 8Department for Radiotherapy and Radio-Oncology, Christian Doppler Clinic, University Hospital Salzburg , Salzburg, Austria
                [9] 9Department of Neurology, Christian-Doppler Medical Center, Paracelsus Medical University , Salzburg, Austria
                Author notes

                Edited by: David Belin, University of Cambridge, United Kingdom

                Reviewed by: Alexander Nikolaevich Savostyanov, State Scientific-Research Institute of Physiology & Basic Medicine, Russia; Stephan Bohlhalter, University of Bern, Switzerland

                *Correspondence: Kathrin Viol k.viol@ 123456salk.at
                Article
                10.3389/fnbeh.2019.00081
                6491783
                31068796
                1b96a41c-e36d-4a0f-9875-07f26a6e0869
                Copyright © 2019 Viol, Aas, Kastinger, Kronbichler, Schöller, Reiter, Said-Yürekli, Kronbichler, Kravanja-Spannberger, Stöger-Schmidinger, Aichhorn and Schiepek.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 23 November 2018
                : 03 April 2019
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 50, Pages: 9, Words: 6872
                Categories
                Neuroscience
                Original Research

                Neurosciences
                ocd,fmri,disgust,insular cortex,precuneus,neural reuse,picture rating
                Neurosciences
                ocd, fmri, disgust, insular cortex, precuneus, neural reuse, picture rating

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