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      Neural Correlates of Deficits in Humor Appreciation in Gelotophobics

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      Scientific Reports
      Nature Publishing Group

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          Abstract

          Gelotophobics have social deficits in the form of relative humorlessness and heightened sensitivity to aggressive humor; however, little is known about the neural reward mechanisms for this group. The present study attempted to identify the neural substrates of responses to hostile and non-hostile jokes in gelotophobics and non-gelotophobics. Gelotophobics showed greater activation than did non-gelotophobics in the dorsal corticostriatal system, which comprises the dorsolateral prefrontal cortex and dorsal striatum, suggesting a higher degree of voluntary top-down cognitive control of emotion. As expected, gelotophobics showed less activation in the ventral mesocorticolimbic system (MCL) in response to both hostile and non-hostile jokes, suggesting a relative deficit in the reward system. Conversely, non-gelotophobics displayed greater activation than gelotophobics did in the MCL system, particularly for non-hostile jokes, which suggests a more robust bottom-up emotional response. In response to non-hostile jokes, non-gelotophobics showed greater activation in the ventral MCL reward system, which comprises the midbrain, amygdalae, nucleus accumbens, ventral anterior cingulate cortex, and insula. Psychophysiological interaction analyses further showed that gelotophobics exhibited diminished MCL activation in response to hostile jokes. These group differences may have important implications for our understanding of the neural correlates of social motivation and humor appreciation.

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          Most cited references38

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          Neurobiology of emotion perception I: The neural basis of normal emotion perception.

          There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.
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            Neurobiology of emotion perception II: Implications for major psychiatric disorders.

            To date, there has been little investigation of the neurobiological basis of emotion processing abnormalities in psychiatric populations. We have previously discussed two neural systems: 1) a ventral system, including the amygdala, insula, ventral striatum, ventral anterior cingulate gyrus, and prefrontal cortex, for identification of the emotional significance of a stimulus, production of affective states, and automatic regulation of emotional responses; and 2) a dorsal system, including the hippocampus, dorsal anterior cingulate gyrus, and prefrontal cortex, for the effortful regulation of affective states and subsequent behavior. In this critical review, we have examined evidence from studies employing a variety of techniques for distinct patterns of structural and functional abnormalities in these neural systems in schizophrenia, bipolar disorder, and major depressive disorder. In each psychiatric disorder, the pattern of abnormalities may be associated with specific symptoms, including emotional flattening, anhedonia, and persecutory delusions in schizophrenia, prominent mood swings, emotional lability, and distractibility in bipolar disorder during depression and mania, and with depressed mood and anhedonia in major depressive disorder. We suggest that distinct patterns of structural and functional abnormalities in neural systems important for emotion processing are associated with specific symptoms of schizophrenia and bipolar and major depressive disorder.
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              Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition.

              Functional magnetic resonance imaging (fMRI) studiesofemotion, personality, and social cognition have drawn much attention in recent years, with high-profile studies frequently reporting extremely high (e.g., >.8) correlations between brain activation and personality measures. We show that these correlations are higher than should be expected given the (evidently limited) reliability of both fMRI and personality measures. The high correlations are all the more puzzling because method sections rarely contain much detail about how the correlations were obtained. We surveyed authors of 55 articles that reported findings of this kind to determine a few details on how these correlations were computed. More than half acknowledged using a strategy that computes separate correlations for individual voxels and reports means of only those voxels exceeding chosen thresholds. We show how this nonindependent analysis inflates correlations while yielding reassuring-looking scattergrams. This analysis technique was used to obtain the vast majority of the implausibly high correlations in our survey sample. In addition, we argue that, in some cases, other analysis problems likely created entirely spurious correlations. We outline how the data from these studies could be reanalyzed with unbiased methods to provide accurate estimates of the correlations in question and urge authors to perform such reanalyses. The underlying problems described here appear to be common in fMRI research of many kinds-not just in studies of emotion, personality, and social cognition.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                03 October 2016
                2016
                : 6
                : 34580
                Affiliations
                [1 ]Institute of Learning Sciences, National Tsing Hua University , Hsinchu, Taiwan
                Author notes
                Article
                srep34580
                10.1038/srep34580
                5046107
                27694969
                a958ee18-56a7-4a18-9b8e-acca631e2f8f
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 09 May 2016
                : 15 September 2016
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