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      What Are You Feeling? Using Functional Magnetic Resonance Imaging to Assess the Modulation of Sensory and Affective Responses during Empathy for Pain

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          Abstract

          Background

          Recent neuroscientific evidence suggests that empathy for pain activates similar neural representations as the first-hand experience of pain. However, empathy is not an all-or-none phenomenon but it is strongly malleable by interpersonal, intrapersonal and situational factors. This study investigated how two different top-down mechanisms – attention and cognitive appraisal - affect the perception of pain in others and its neural underpinnings.

          Methodology/Principal Findings

          We performed one behavioral (N = 23) and two functional magnetic resonance imaging (fMRI) experiments (N = 18). In the first fMRI experiment, participants watched photographs displaying painful needle injections, and were asked to evaluate either the sensory or the affective consequences of these injections. The role of cognitive appraisal was examined in a second fMRI experiment in which participants watched injections that only appeared to be painful as they were performed on an anesthetized hand. Perceiving pain in others activated the affective-motivational and sensory-discriminative aspects of the pain matrix. Activity in the somatosensory areas was specifically enhanced when participants evaluated the sensory consequences of pain. Perceiving non-painful injections into the anesthetized hand also led to signal increase in large parts of the pain matrix, suggesting an automatic affective response to the putatively harmful stimulus. This automatic response was modulated by areas involved in self/other distinction and valence attribution – including the temporo-parietal junction and medial orbitofrontal cortex.

          Conclusions/Significance

          Our findings elucidate how top-down control mechanisms and automatic bottom-up processes interact to generate and modulate other-oriented responses. They stress the role of cognitive processing in empathy, and shed light on how emotional and bodily awareness enable us to evaluate the sensory and affective states of others.

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          Most cited references69

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          Empathy for pain involves the affective but not sensory components of pain.

          Our ability to have an experience of another's pain is characteristic of empathy. Using functional imaging, we assessed brain activity while volunteers experienced a painful stimulus and compared it to that elicited when they observed a signal indicating that their loved one--present in the same room--was receiving a similar pain stimulus. Bilateral anterior insula (AI), rostral anterior cingulate cortex (ACC), brainstem, and cerebellum were activated when subjects received pain and also by a signal that a loved one experienced pain. AI and ACC activation correlated with individual empathy scores. Activity in the posterior insula/secondary somatosensory cortex, the sensorimotor cortex (SI/MI), and the caudal ACC was specific to receiving pain. Thus, a neural response in AI and rostral ACC, activated in common for "self" and "other" conditions, suggests that the neural substrate for empathic experience does not involve the entire "pain matrix." We conclude that only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy.
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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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              Pain and emotion interactions in subregions of the cingulate gyrus.

              Brent Vogt (2005)
              Acute pain and emotion are processed in two forebrain networks, and the cingulate cortex is involved in both. Although Brodmann's cingulate gyrus had two divisions and was not based on any functional criteria, functional imaging studies still use this model. However, recent cytoarchitectural studies of the cingulate gyrus support a four-region model, with subregions, that is based on connections and qualitatively unique functions. Although the activity evoked by pain and emotion has been widely reported, some view them as emergent products of the brain rather than of small aggregates of neurons. Here, we assess pain and emotion in each cingulate subregion, and assess whether pain is co-localized with negative affect. Amazingly, these activation patterns do not simply overlap.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2007
                12 December 2007
                : 2
                : 12
                : e1292
                Affiliations
                [1 ]Department of Psychology and Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois, United States of America
                [2 ]Institute for Learning and Brain Sciences, University of Washington, Seattle, Washington, United States of America
                Lund University, Sweden
                Author notes
                * To whom correspondence should be addressed. E-mail: decety@ 123456uchicago.edu

                Conceived and designed the experiments: JD HN CL. Performed the experiments: JD CL. Analyzed the data: JD CL. Contributed reagents/materials/analysis tools: JD CL. Wrote the paper: JD AM HN CL.

                Article
                07-PONE-RA-02184R1
                10.1371/journal.pone.0001292
                2144768
                18091986
                7873e05f-de40-4107-9ab4-1b45e9eac130
                Lamm 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
                : 6 September 2007
                : 15 November 2007
                Page count
                Pages: 16
                Categories
                Research Article
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Sensory Systems

                Uncategorized
                Uncategorized

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