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      Enhanced Positive Emotional Reactivity Undermines Empathy in Behavioral Variant Frontotemporal Dementia

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          Abstract

          Behavioral variant frontotemporal dementia (bvFTD) is a neurodegenerative disease characterized by profound changes in emotions and empathy. Although most patients with bvFTD become less sensitive to negative emotional cues, some patients become more sensitive to positive emotional stimuli. We investigated whether dysregulated positive emotions in bvFTD undermine empathy by making it difficult for patients to share (emotional empathy), recognize (cognitive empathy), and respond (real-world empathy) to emotions in others. Fifty-one participants (26 patients with bvFTD and 25 healthy controls) viewed photographs of neutral, positive, negative, and self-conscious emotional faces and then identified the emotions displayed in the photographs. We used facial electromyography to measure automatic, sub-visible activity in two facial muscles during the task: Zygomaticus major ( ZM), which is active during positive emotional reactions (i.e., smiling), and Corrugator supercilii ( CS), which is active during negative emotional reactions (i.e., frowning). Participants rated their baseline positive and negative emotional experience before the task, and informants rated participants' real-world empathic behavior on the Interpersonal Reactivity Index. The majority of participants also underwent structural magnetic resonance imaging. A mixed effects model found a significant diagnosis X trial interaction: patients with bvFTD showed greater ZM reactivity to neutral, negative (disgust and surprise), self-conscious (proud), and positive (happy) faces than healthy controls. There was no main effect of diagnosis or diagnosis X trial interaction on CS reactivity. Compared to healthy controls, patients with bvFTD had impaired emotion recognition. Multiple regression analyses revealed that greater ZM reactivity predicted worse negative emotion recognition and worse real-world empathy. At baseline, positive emotional experience was higher in bvFTD than healthy controls and also predicted worse negative emotion recognition. Voxel-based morphometry analyses found that smaller volume in the thalamus, midcingulate cortex, posterior insula, anterior temporal pole, amygdala, precentral gyrus, and inferior frontal gyrus—structures that support emotion generation, interoception, and emotion regulation—was associated with greater ZM reactivity in bvFTD. These findings suggest that dysregulated positive emotional reactivity may relate to reduced empathy in bvFTD by making patients less likely to tune their reactions to the social context and to share, recognize, and respond to others' feelings and needs.

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          The broaden-and-build theory of positive emotions.

          The broaden-and-build theory describes the form and function of a subset of positive emotions, including joy, interest, contentment and love. A key proposition is that these positive emotions broaden an individual's momentary thought-action repertoire: joy sparks the urge to play, interest sparks the urge to explore, contentment sparks the urge to savour and integrate, and love sparks a recurring cycle of each of these urges within safe, close relationships. The broadened mindsets arising from these positive emotions are contrasted to the narrowed mindsets sparked by many negative emotions (i.e. specific action tendencies, such as attack or flee). A second key proposition concerns the consequences of these broadened mindsets: by broadening an individual's momentary thought-action repertoire--whether through play, exploration or similar activities--positive emotions promote discovery of novel and creative actions, ideas and social bonds, which in turn build that individual's personal resources; ranging from physical and intellectual resources, to social and psychological resources. Importantly, these resources function as reserves that can be drawn on later to improve the odds of successful coping and survival. This chapter reviews the latest empirical evidence supporting the broaden-and-build theory and draws out implications the theory holds for optimizing health and well-being.
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            The functional architecture of human empathy.

            Empathy accounts for the naturally occurring subjective experience of similarity between the feelings expressed by self and others without loosing sight of whose feelings belong to whom. Empathy involves not only the affective experience of the other person's actual or inferred emotional state but also some minimal recognition and understanding of another's emotional state. In light of multiple levels of analysis ranging from developmental psychology, social psychology, cognitive neuroscience, and clinical neuropsychology, this article proposes a model of empathy that involves parallel and distributed processing in a number of dissociable computational mechanisms. Shared neural representations, self-awareness, mental flexibility, and emotion regulation constitute the basic macrocomponents of empathy, which are underpinned by specific neural systems. This functional model may be used to make specific predictions about the various empathy deficits that can be encountered in different forms of social and neurological disorders.
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              Contributions of anterior cingulate cortex to behaviour

              Assessments of anterior cingulate cortex in experimental animals and humans have led to unifying theories of its structural organization and contributions to mammalian behaviour. The anterior cingulate cortex forms a large region around the rostrum of the corpus callosum that is termed the anterior executive region. This region has numerous projections into motor systems, however, since these projections originate from different parts of anterior cingulate cortex and because functional studies have shown that it does not have a uniform contribution to brain functions, the anterior executive region is further subdivided into 'affect' and 'cognition' components. The affect division includes areas 25, 33 and rostral area 24, and has extensive connections with the amygdala and periaqueductal grey, and parts of it project to autonomic brainstem motor nuclei. In addition to regulating autonomic and endocrine functions, it is involved in conditioned emotional learning, vocalizations associated with expressing internal states, assessments of motivational content and assigning emotional valence to internal and external stimuli, and maternal-infant interactions. The cognition division includes caudal areas 24' and 32', the cingulate motor areas in the cingulate sulcus and nociceptive cortex. The cingulate motor areas project to the spinal cord and red nucleus and have premotor functions, while the nociceptive area is engaged in both response selection and cognitively demanding information processing. The cingulate epilepsy syndrome provides important support of experimental animal and human functional imaging studies for the role of anterior cingulate cortex in movement, affect and social behaviours. Excessive cingulate activity in cases with seizures confirmed in anterior cingulate cortex with subdural electrode recordings, can impair consciousness, alter affective state and expression, and influence skeletomotor and autonomic activity. Interictally, patients with anterior cingulate cortex epilepsy often display psychopathic or sociopathic behaviours. In other clinical examples of elevated anterior cingulate cortex activity it may contribute to tics, obsessive-compulsive behaviours, and aberrent social behaviour. Conversely, reduced cingulate activity following infarcts or surgery can contribute to behavioural disorders including akinetic mutism, diminished self-awareness and depression, motor neglect and impaired motor initiation, reduced responses to pain, and aberrent social behaviour. The role of anterior cingulate cortex in pain responsiveness is suggested by cingulumotomy results and functional imaging studies during noxious somatic stimulation. The affect division of anterior cingulate cortex modulates autonomic activity and internal emotional responses, while the cognition division is engaged in response selection associated with skeletomotor activity and responses to noxious stimuli. Overall, anterior cingulate cortex appears to play a crucial role in initiation, motivation, and goal-directed behaviours.(ABSTRACT TRUNCATED AT 400 WORDS)
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                Author and article information

                Contributors
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                04 June 2018
                2018
                : 9
                : 402
                Affiliations
                [1] 1Department of Psychology, University of California, Berkeley , Berkeley, CA, United States
                [2] 2Department of Neurology, Memory and Aging Center, University of California, San Francisco , San Francisco, CA, United States
                Author notes

                Edited by: Kathrin Reetz, RWTH Aachen Universität, Germany

                Reviewed by: Mario F. Mendez, UCLA David Geffen School of Medicine, United States; Janelle Beadle, University of Nebraska Omaha, United States

                *Correspondence: Virginia E. Sturm virginia.sturm@ 123456ucsf.edu

                This article was submitted to Applied Neuroimaging, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2018.00402
                5994409
                29915557
                4c4d5532-aa87-4a5c-ae59-00cff459c6b3
                Copyright © 2018 Hua, Sible, Perry, Rankin, Kramer, Miller, Rosen and Sturm.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 March 2018
                : 15 May 2018
                Page count
                Figures: 4, Tables: 3, Equations: 0, References: 94, Pages: 14, Words: 10844
                Funding
                Funded by: National Institute on Aging 10.13039/100000049
                Award ID: P50AG023501
                Award ID: P01AG019724
                Award ID: R01AG052496
                Award ID: R01AG032306
                Award ID: R01AG057204
                Award ID: 1K23AG040127
                Award ID: 1K23AG045289
                Funded by: Larry L. Hillblom Foundation 10.13039/100001167
                Award ID: 2013-A-029-SUP
                Award ID: 2005/2T
                Funded by: National Institute of Mental Health 10.13039/100000025
                Award ID: MH020006-16A1
                Categories
                Neurology
                Original Research

                Neurology
                facial electromyography,positive emotion,empathy,dysregulation,emotion recognition,frontotemporal dementia

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