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      Neural correlates of specific musical anhedonia

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          Significance

          This study provides direct evidence supporting the model of reward–auditory cortex interaction as underlying musical pleasure: People who do not experience that pleasure have selectively reduced responses in that system. People who are especially sensitive to musical reward conversely seem to show an enhanced interaction. Our paper offers insights into the neurobiological basis of music-induced pleasure that could also provide the basis for thinking more broadly about other types of aesthetic rewards. Our results also provide an important step toward the understanding of how music may have acquired reward value through evolution.

          Abstract

          Although music is ubiquitous in human societies, there are some people for whom music holds no reward value despite normal perceptual ability and preserved reward-related responses in other domains. The study of these individuals with specific musical anhedonia may be crucial to understand better the neural correlates underlying musical reward. Previous neuroimaging studies have shown that musically induced pleasure may arise from the interaction between auditory cortical networks and mesolimbic reward networks. If such interaction is critical for music-induced pleasure to emerge, then those individuals who do not experience it should show alterations in the cortical-mesolimbic response. In the current study, we addressed this question using fMRI in three groups of 15 participants, each with different sensitivity to music reward. We demonstrate that the music anhedonic participants showed selective reduction of activity for music in the nucleus accumbens (NAcc), but normal activation levels for a monetary gambling task. Furthermore, this group also exhibited decreased functional connectivity between the right auditory cortex and ventral striatum (including the NAcc). In contrast, individuals with greater than average response to music showed enhanced connectivity between these structures. Thus, our results suggest that specific musical anhedonia may be associated with a reduction in the interplay between the auditory cortex and the subcortical reward network, indicating a pivotal role of this interaction for the enjoyment of music.

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          Most cited references42

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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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              Changes in brain activity related to eating chocolate: from pleasure to aversion.

              D M Small (2001)
              We performed successive H(2)(15)O-PET scans on volunteers as they ate chocolate to beyond satiety. Thus, the sensory stimulus and act (eating) were held constant while the reward value of the chocolate and motivation of the subject to eat were manipulated by feeding. Non-specific effects of satiety (such as feelings of fullness and autonomic changes) were also present and probably contributed to the modulation of brain activity. After eating each piece of chocolate, subjects gave ratings of how pleasant/unpleasant the chocolate was and of how much they did or did not want another piece of chocolate. Regional cerebral blood flow was then regressed against subjects' ratings. Different groups of structures were recruited selectively depending on whether subjects were eating chocolate when they were highly motivated to eat and rated the chocolate as very pleasant [subcallosal region, caudomedial orbitofrontal cortex (OFC), insula/operculum, striatum and midbrain] or whether they ate chocolate despite being satiated (parahippocampal gyrus, caudolateral OFC and prefrontal regions). As predicted, modulation was observed in cortical chemosensory areas, including the insula and caudomedial and caudolateral OFC, suggesting that the reward value of food is represented here. Of particular interest, the medial and lateral caudal OFC showed opposite patterns of activity. This pattern of activity indicates that there may be a functional segregation of the neural representation of reward and punishment within this region. The only brain region that was active during both positive and negative compared with neutral conditions was the posterior cingulate cortex. Therefore, these results support the hypothesis that there are two separate motivational systems: one orchestrating approach and another avoidance behaviours.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                15 November 2016
                31 October 2016
                : 113
                : 46
                : E7337-E7345
                Affiliations
                [1] aDepartment of Cognition, Development and Educational Psychology, University of Barcelona , L’Hospitalet de Llobregat , 08097 Barcelona, Spain;
                [2] bMontreal Neurological Institute, McGill University , Montreal, QC, Canada H3A 2B4;
                [3] cCognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute , L’Hospitalet de Llobregat , 08097 Barcelona, Spain;
                [4] d Institució Catalana de Recerca i Estudis Avançats , 08010 Barcelona, Spain;
                [5] e International Laboratory for Brain, Music, and Sound Research , Montreal, QC, Canada H3C 3J7;
                [6] f Institute of Neurosciences, University of Barcelona , 08035 Barcelona, Spain
                Author notes
                2To whom correspondence should be addressed. Email: josepmarco@ 123456gmail.com .

                Edited by Dale Purves, Duke University, Durham, NC, and approved September 27, 2016 (received for review July 8, 2016)

                Author contributions: N.M.-M., E.M.-H., A.R.-F., R.J.Z., and J.M.-P. designed research; N.M.-M., E.M.-H., and J.M.-P. performed research; N.M.-M. and E.M.-H. analyzed data; and N.M.-M., E.M.-H., A.R.-F., R.J.Z., and J.M.-P. wrote the paper.

                1N.M.-M. and E.M.-H. contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-9175-1480
                Article
                PMC5135354 PMC5135354 5135354 201611211
                10.1073/pnas.1611211113
                5135354
                27799544
                57ffab71-8e94-402d-83b0-f94797322c4d
                History
                Page count
                Pages: 9
                Funding
                Funded by: Departament d'Innovació, Universitats i Empresa, Generalitat de Catalunya (Department of Innovation, Education and Enterprise, Government of Catalonia) 501100002943
                Award ID: 2014SGR1413
                Funded by: Ministry of Economy and Competitiveness | Consejo Superior de Investigaciones Científicas (Spanish National Research Council) 501100003339
                Award ID: PSI2012-37472
                Funded by: Ministry of Economy and Competitiveness | Consejo Superior de Investigaciones Científicas (Spanish National Research Council) 501100003339
                Award ID: PSI2015-69664-P
                Funded by: Departament d'Innovació, Universitats i Empresa, Generalitat de Catalunya (Department of Innovation, Education and Enterprise, Government of Catalonia) 501100002943
                Award ID: 2013-FI_B2 00133
                Funded by: Ministry of Economy and Competitiveness | Consejo Superior de Investigaciones Científicas (Spanish National Research Council) 501100003339
                Award ID: BES-2010-032702
                Categories
                PNAS Plus
                Biological Sciences
                Psychological and Cognitive Sciences
                PNAS Plus

                reward,music,emotion,anhedonia
                reward, music, emotion, anhedonia

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