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      The auditory cortex hosts network nodes influential for emotion processing: An fMRI study on music-evoked fear and joy

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      1 , * , 2 , 3 , 4
      PLoS ONE
      Public Library of Science

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          Abstract

          Sound is a potent elicitor of emotions. Auditory core, belt and parabelt regions have anatomical connections to a large array of limbic and paralimbic structures which are involved in the generation of affective activity. However, little is known about the functional role of auditory cortical regions in emotion processing. Using functional magnetic resonance imaging and music stimuli that evoke joy or fear, our study reveals that anterior and posterior regions of auditory association cortex have emotion-characteristic functional connectivity with limbic/paralimbic (insula, cingulate cortex, and striatum), somatosensory, visual, motor-related, and attentional structures. We found that these regions have remarkably high emotion-characteristic eigenvector centrality, revealing that they have influential positions within emotion-processing brain networks with “small-world” properties. By contrast, primary auditory fields showed surprisingly strong emotion-characteristic functional connectivity with intra-auditory regions. Our findings demonstrate that the auditory cortex hosts regions that are influential within networks underlying the affective processing of auditory information. We anticipate our results to incite research specifying the role of the auditory cortex—and sensory systems in general—in emotion processing, beyond the traditional view that sensory cortices have merely perceptual functions.

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          Most cited references52

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          The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.

          The human orbitofrontal cortex is an important brain region for the processing of rewards and punishments, which is a prerequisite for the complex and flexible emotional and social behaviour which contributes to the evolutionary success of humans. Yet much remains to be discovered about the functions of this key brain region, and new evidence from functional neuroimaging and clinical neuropsychology is affording new insights into the different functions of the human orbitofrontal cortex. We review the neuroanatomical and neuropsychological literature on the human orbitofrontal cortex, and propose two distinct trends of neural activity based on a meta-analysis of neuroimaging studies. One is a mediolateral distinction, whereby medial orbitofrontal cortex activity is related to monitoring the reward value of many different reinforcers, whereas lateral orbitofrontal cortex activity is related to the evaluation of punishers which may lead to a change in ongoing behaviour. The second is a posterior-anterior distinction with more complex or abstract reinforcers (such as monetary gain and loss) represented more anteriorly in the orbitofrontal cortex than simpler reinforcers such as taste or pain. Finally, we propose new neuroimaging methods for obtaining further evidence on the localisation of function in the human orbitofrontal cortex.
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            Brain correlates of music-evoked emotions.

            Music is a universal feature of human societies, partly owing to its power to evoke strong emotions and influence moods. During the past decade, the investigation of the neural correlates of music-evoked emotions has been invaluable for the understanding of human emotion. Functional neuroimaging studies on music and emotion show that music can modulate activity in brain structures that are known to be crucially involved in emotion, such as the amygdala, nucleus accumbens, hypothalamus, hippocampus, insula, cingulate cortex and orbitofrontal cortex. The potential of music to modulate activity in these structures has important implications for the use of music in the treatment of psychiatric and neurological disorders.
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              Investigating emotion with music: an fMRI study.

              The present study used pleasant and unpleasant music to evoke emotion and functional magnetic resonance imaging (fMRI) to determine neural correlates of emotion processing. Unpleasant (permanently dissonant) music contrasted with pleasant (consonant) music showed activations of amygdala, hippocampus, parahippocampal gyrus, and temporal poles. These structures have previously been implicated in the emotional processing of stimuli with (negative) emotional valence; the present data show that a cerebral network comprising these structures can be activated during the perception of auditory (musical) information. Pleasant (contrasted to unpleasant) music showed activations of the inferior frontal gyrus (IFG, inferior Brodmann's area (BA) 44, BA 45, and BA 46), the anterior superior insula, the ventral striatum, Heschl's gyrus, and the Rolandic operculum. IFG activations appear to reflect processes of music-syntactic analysis and working memory operations. Activations of Rolandic opercular areas possibly reflect the activation of mirror-function mechanisms during the perception of the pleasant tunes. Rolandic operculum, anterior superior insula, and ventral striatum may form a motor-related circuitry that serves the formation of (premotor) representations for vocal sound production during the perception of pleasant auditory information. In all of the mentioned structures, except the hippocampus, activations increased over time during the presentation of the musical stimuli, indicating that the effects of emotion processing have temporal dynamics; the temporal dynamics of emotion have so far mainly been neglected in the functional imaging literature. Copyright 2005 Wiley-Liss, Inc.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – review & editing
                Role: SoftwareRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2018
                31 January 2018
                : 13
                : 1
                : e0190057
                Affiliations
                [1 ] Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway
                [2 ] Department of Education and Psychology, Freie Universität Berlin, Berlin, Germany
                [3 ] Department of Biomedical Magnetic Resonance, University Clinic Tübingen, Tübingen, Germany
                [4 ] Magnetic Resonance Center, Max Planck Institute for Biological Cybernetics, Tübingen, Germany
                University of Texas at Austin, UNITED STATES
                Author notes

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

                Author information
                http://orcid.org/0000-0002-8714-3404
                Article
                PONE-D-16-51619
                10.1371/journal.pone.0190057
                5791961
                29385142
                5f6c7bee-0dba-4c87-ab5d-ce7fe6130643
                © 2018 Koelsch et al

                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
                : 31 December 2016
                : 7 December 2017
                Page count
                Figures: 4, Tables: 6, Pages: 22
                Funding
                The study was funded by the Cluster of Excellence "Languages of Emotion" of the Freie Universität Berlin.
                Categories
                Research Article
                Biology and Life Sciences
                Psychology
                Emotions
                Fear
                Social Sciences
                Psychology
                Emotions
                Fear
                Biology and Life Sciences
                Psychology
                Emotions
                Social Sciences
                Psychology
                Emotions
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Auditory System
                Auditory Cortex
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Auditory System
                Auditory Cortex
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Auditory System
                Auditory Cortex
                Biology and Life Sciences
                Anatomy
                Brain
                Auditory Cortex
                Medicine and Health Sciences
                Anatomy
                Brain
                Auditory Cortex
                Computer and Information Sciences
                Network Analysis
                Centrality
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                Neural Networks
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                Neuroscience
                Neural Networks
                Physical Sciences
                Physics
                Acoustics
                Bioacoustics
                Biology and Life Sciences
                Bioacoustics
                Biology and Life Sciences
                Anatomy
                Brain
                Cingulate Cortex
                Medicine and Health Sciences
                Anatomy
                Brain
                Cingulate Cortex
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Functional Magnetic Resonance Imaging
                Medicine and Health Sciences
                Diagnostic Medicine
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                Research and Analysis Methods
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                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
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                Research and Analysis Methods
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                Neuroimaging
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                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Functional Magnetic Resonance Imaging
                Custom metadata
                At the time the data for this study were collected, participant consent forms did not include approval to share data beyond members of the research team. Additionally, the data contain potentially identifying participant information. After consulting with members of the ethics committee of the University of Sussex, the authors confirm that the data cannot be made available due to limitations of participant consent.

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