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      Facial Emotion Recognition in Parkinson's Disease: An fMRI Investigation

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          Abstract

          Background

          Findings of behavioral studies on facial emotion recognition in Parkinson’s disease (PD) are very heterogeneous. Therefore, the present investigation additionally used functional magnetic resonance imaging (fMRI) in order to compare brain activation during emotion perception between PD patients and healthy controls.

          Methods and Findings

          We included 17 nonmedicated, nondemented PD patients suffering from mild to moderate symptoms and 22 healthy controls. The participants were shown pictures of facial expressions depicting disgust, fear, sadness, and anger and they answered scales for the assessment of affective traits. The patients did not report lowered intensities for the displayed target emotions, and showed a comparable rating accuracy as the control participants. The questionnaire scores did not differ between patients and controls. The fMRI data showed similar activation in both groups except for a generally stronger recruitment of somatosensory regions in the patients.

          Conclusions

          Since somatosensory cortices are involved in the simulation of an observed emotion, which constitutes an important mechanism for emotion recognition, future studies should focus on activation changes within this region during the course of disease.

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          Neural systems for recognizing emotion.

          Ralph Adolphs (2002)
          Recognition of emotion draws on a distributed set of structures that include the occipitotemporal neocortex, amygdala, orbitofrontal cortex and right frontoparietal cortices. Recognition of fear may draw especially on the amygdala and the detection of disgust may rely on the insula and basal ganglia. Two important mechanisms for recognition of emotions are the construction of a simulation of the observed emotion in the perceiver, and the modulation of sensory cortices via top-down influences.
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            Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies.

            Paolo Fusar-Poli, Anna Placentino, Francesco Carletti … (2009)
            Most of our social interactions involve perception of emotional information from the faces of other people. Furthermore, such emotional processes are thought to be aberrant in a range of clinical disorders, including psychosis and depression. However, the exact neurofunctional maps underlying emotional facial processing are not well defined. Two independent researchers conducted separate comprehensive PubMed (1990 to May 2008) searches to find all functional magnetic resonance imaging (fMRI) studies using a variant of the emotional faces paradigm in healthy participants. The search terms were: "fMRI AND happy faces," "fMRI AND sad faces," "fMRI AND fearful faces," "fMRI AND angry faces," "fMRI AND disgusted faces" and "fMRI AND neutral faces." We extracted spatial coordinates and inserted them in an electronic database. We performed activation likelihood estimation analysis for voxel-based meta-analyses. Of the originally identified studies, 105 met our inclusion criteria. The overall database consisted of 1785 brain coordinates that yielded an overall sample of 1600 healthy participants. Quantitative voxel-based meta-analysis of brain activation provided neurofunctional maps for 1) main effect of human faces; 2) main effect of emotional valence; and 3) modulatory effect of age, sex, explicit versus implicit processing and magnetic field strength. Processing of emotional faces was associated with increased activation in a number of visual, limbic, temporoparietal and prefrontal areas; the putamen; and the cerebellum. Happy, fearful and sad faces specifically activated the amygdala, whereas angry or disgusted faces had no effect on this brain region. Furthermore, amygdala sensitivity was greater for fearful than for happy or sad faces. Insular activation was selectively reported during processing of disgusted and angry faces. However, insular sensitivity was greater for disgusted than for angry faces. Conversely, neural response in the visual cortex and cerebellum was observable across all emotional conditions. Although the activation likelihood estimation approach is currently one of the most powerful and reliable meta-analytical methods in neuroimaging research, it is insensitive to effect sizes. Our study has detailed neurofunctional maps to use as normative references in future fMRI studies of emotional facial processing in psychiatric populations. We found selective differences between neural networks underlying the basic emotions in limbic and insular brain regions.
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              Neuroanatomical correlates of impaired decision-making and facial emotion recognition in early Parkinson's disease.

              Francesc Valldeoriola, Naroa Ibarretxe-Bilbao, Eduardo Tolosa … (2009)
              Decision-making and recognition of emotions are often impaired in patients with Parkinson's disease (PD). The orbitofrontal cortex (OFC) and the amygdala are critical structures subserving these functions. This study was designed to test whether there are any structural changes in these areas that might explain the impairment of decision-making and recognition of facial emotions in early PD. We used the Iowa Gambling Task (IGT) and the Ekman 60 faces test which are sensitive to the integrity of OFC and amygdala dysfunctions in 24 early PD patients and 24 controls. High-resolution structural magnetic resonance images (MRI) were also obtained. Group analysis using voxel-based morphometry (VBM) showed significant and corrected (P < 0.05 FEW-small volume correction) gray matter (GM) loss in the right amygdala and bilaterally in the OFC in PD patients. Volumetric analyses were also performed but did not yield significant differences between groups. Left lateral GM volume in OFC showed a slight correlation with the IGT, and bilateral OFC GM was strongly correlated with Ekman test performance in PD patients. We conclude that: (i) impairment in decision-making and recognition of facial emotions occurs at the early stages of PD, (ii) these neuropsychological deficits are accompanied by degeneration of OFC and amygdala, and (iii) bilateral OFC reductions are associated with impaired recognition of emotions, and GM volume loss in left lateral OFC is related to decision-making impairment in PD.
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                Author and article information

                Contributors
                Marco Tamietto: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 18 August 2015
                Publication date Collection: 2015
                Volume: 10
                Issue: 8
                Electronic Location Identifier: e0136110
                Affiliations
                [1 ]Clinical Psychology, University of Graz, BioTechMedGraz, Graz, Austria
                [2 ]Department of Neurology, Medical University of Graz, Graz, Austria
                Tilburg University, NETHERLANDS
                Author notes

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

                Conceived and designed the experiments: AS. Performed the experiments: RI PS PK MK KW. Analyzed the data: AW AS RI. Contributed reagents/materials/analysis tools: AW. Wrote the paper: AS RI.

                Article
                Publisher ID: PONE-D-15-04306
                DOI: 10.1371/journal.pone.0136110
                PMC ID: 4540566
                PubMed ID: 26285212
                SO-VID: 6c26b18b-9f0a-4464-a832-abe8f011936a
                Copyright statement: Copyright @ 2015
                License:

                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
                Date received : 2 February 2015
                Date accepted : 29 July 2015
                Page count
                Figures: 1, Tables: 2, Pages: 9
                Funding
                This work was supported by the Austrian Science Fund (P 23258-B18).
                Categories
                Subject: Research Article
                Custom metadata
                Data Availability Data cannot be made publicly available due to ethical restrictions defined in the informed consent form for the patients and implemented by the ethics committee. Data are available upon request to anne.schienle@ 123456uni-graz.at .

                ScienceOpen disciplines: Uncategorized
                Data availability:
                ScienceOpen disciplines: Uncategorized

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