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      Emotion Processing in Parkinson’s Disease: A Three-Level Study on Recognition, Representation, and Regulation

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          Abstract

          Background

          Parkinson’s disease (PD) is characterised by well-known motor symptoms, whereas the presence of cognitive non-motor symptoms, such as emotional disturbances, is still underestimated. One of the major problems in studying emotion deficits in PD is an atomising approach that does not take into account different levels of emotion elaboration. Our study addressed the question of whether people with PD exhibit difficulties in one or more specific dimensions of emotion processing, investigating three different levels of analyses, that is, recognition, representation, and regulation.

          Methodology

          Thirty-two consecutive medicated patients with PD and 25 healthy controls were enrolled in the study. Participants performed a three-level analysis assessment of emotional processing using quantitative standardised emotional tasks: the Ekman 60-Faces for emotion recognition, the full 36-item version of the Reading the Mind in the Eyes (RME) for emotion representation, and the 20-item Toronto Alexithymia Scale (TAS-20) for emotion regulation.

          Principal Findings

          Regarding emotion recognition, patients obtained significantly worse scores than controls in the total score of Ekman 60-Faces but not in any other basic emotions. For emotion representation, patients obtained significantly worse scores than controls in the RME experimental score but no in the RME gender control task. Finally, on emotion regulation, PD and controls did not perform differently at TAS-20 and no specific differences were found on TAS-20 subscales. The PD impairments on emotion recognition and representation do not correlate with dopamine therapy, disease severity, or with the duration of illness. These results are independent from other cognitive processes, such as global cognitive status and executive function, or from psychiatric status, such as depression, anxiety or apathy.

          Conclusions

          These results may contribute to better understanding of the emotional problems that are often seen in patients with PD and the measures used to test these problems, in particular on the use of different versions of the RME task.

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          Most cited references51

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          Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases.

          Few detailed clinico-pathological correlations of Parkinson's disease have been published. The pathological findings in 100 patients diagnosed prospectively by a group of consultant neurologists as having idiopathic Parkinson's disease are reported. Seventy six had nigral Lewy bodies, and in all of these Lewy bodies were also found in the cerebral cortex. In 24 cases without Lewy bodies, diagnoses included progressive supranuclear palsy, multiple system atrophy, Alzheimer's disease, Alzheimer-type pathology, and basal ganglia vascular disease. The retrospective application of recommended diagnostic criteria improved the diagnostic accuracy to 82%. These observations call into question current concepts of Parkinson's disease as a single distinct morbid entity.
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            Neural bases of the non-conscious perception of emotional signals.

            Many emotional stimuli are processed without being consciously perceived. Recent evidence indicates that subcortical structures have a substantial role in this processing. These structures are part of a phylogenetically ancient pathway that has specific functional properties and that interacts with cortical processes. There is now increasing evidence that non-consciously perceived emotional stimuli induce distinct neurophysiological changes and influence behaviour towards the consciously perceived world. Understanding the neural bases of the non-conscious perception of emotional signals will clarify the phylogenetic continuity of emotion systems across species and the integration of cortical and subcortical activity in the human brain.
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              A modified card sorting test sensitive to frontal lobe defects.

              H Nelson (1976)
              Milner's (1963) report of impaired performance on the Wisconsin Card Sorting Test (WCST) in a group of patients with frontal lobe lesions suggested that this test might be a useful one in the investigation of individual patients with suspected brain lesions. However, for many of our older hospital population the WCST was found to be too difficult and distressing, and also the inherent ambiguities associated with certain responses limited the test's usefulness for research purposes. Therefore, a simpler and less ambiguous modification was devised (MCS) and a new method of measuring perseverative errors proposed. In a group of 53 patients with unilateral cerebral lesions, those with frontal lobe lesions performed less well with the MCST and made a higher proportion of perseverative errors than those with lesions elsewhere: there were no laterality effects in either frontal or non-frontal groups. The usefulness of the MCST for detecting frontal lobe lesions in individual patients was established, and the use of cut-off scores briefly discussed.
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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
                25 June 2015
                2015
                : 10
                : 6
                : e0131470
                Affiliations
                [1 ]Department of Philosophy and Educational Sciences, University of Turin, Turin, Italy
                [2 ]Center for Cognitive Science, University of Turin, Turin, Italy
                [3 ]Neuroscience Institute of Turin, Turin, Italy
                [4 ]Department of Psychology, University of Turin, Turin, Italy
                [5 ]eCampus University, Novedrate, Como, Italy
                [6 ]Azienda Sanitaria Locale Torino 3, Turin, Italy
                [7 ]Department of Neuroscience, University of Turin, Turin, Italy
                Tilburg University, NETHERLANDS
                Author notes

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

                Conceived and designed the experiments: IE MA RBA AM MC MZ LL LC. Performed the experiments: IE MA RBA AM LC. Analyzed the data: IE MA AM MC LC. Contributed reagents/materials/analysis tools: IE MA RBA AM MC MZ LL LC. Wrote the paper: IE MA RBA AM MC MZ LL LC.

                Article
                PONE-D-15-01165
                10.1371/journal.pone.0131470
                4482447
                26110271
                dd083ac4-f769-4162-9319-0421de80ce6a
                Copyright @ 2015

                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
                : 9 January 2015
                : 2 June 2015
                Page count
                Figures: 0, Tables: 3, Pages: 18
                Funding
                Ivan Enrici, Lorys Castelli and Rita B. Ardito were supported by University of Turin grants (“Ricerca scientifica finanziata dall’Università” Linea Generale and Linea Giovani). Mauro Adenzato was supported by MIUR of Italy (FIRB 2012, RBFR12FOBD_001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Funders' websites: http://futuroinricerca.miur.it; www.unito.it
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