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      Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

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          Abstract

          Empathy is thought to engage mental simulation, which in turn is known to rely on hippocampal-neocortical processing. Here, we tested how hippocampal-neocortical pattern similarity and connectivity contributed to pain empathy. Using this approach, we analyzed a data set of 102 human participants who underwent functional MRI while painful and non-painful electrical stimulation was delivered to themselves or to a confederate. As hypothesized, results revealed increased pattern similarity between first-hand pain and pain empathy (compared to non-painful control conditions) within the hippocampus, retrosplenial cortex, the temporo-parietal junction and anterior insula. While representations in these regions were unaffected by confederate similarity, pattern similarity in the dorsal medial prefrontal cortex was increased the more dissimilar the other individual was perceived. Hippocampal-neocortical connectivity during first-hand pain and pain empathy engaged largely distinct but neighboring primary motor regions, and empathy-related hippocampal coupling with the fusiform gyrus positively scaled with trait measures of perspective taking. These findings suggest that shared representations and mental simulation might contribute to pain empathy via hippocampal-neocortical pattern similarity and connectivity, partially affected by personality traits and the similarity of the observed individual.

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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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            Information-based functional brain mapping.

            The development of high-resolution neuroimaging and multielectrode electrophysiological recording provides neuroscientists with huge amounts of multivariate data. The complexity of the data creates a need for statistical summary, but the local averaging standardly applied to this end may obscure the effects of greatest neuroscientific interest. In neuroimaging, for example, brain mapping analysis has focused on the discovery of activation, i.e., of extended brain regions whose average activity changes across experimental conditions. Here we propose to ask a more general question of the data: Where in the brain does the activity pattern contain information about the experimental condition? To address this question, we propose scanning the imaged volume with a "searchlight," whose contents are analyzed multivariately at each location in the brain.
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              Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration.

              People can consciously re-experience past events and pre-experience possible future events. This fMRI study examined the neural regions mediating the construction and elaboration of past and future events. Participants were cued with a noun for 20s and instructed to construct a past or future event within a specified time period (week, year, 5-20 years). Once participants had the event in mind, they made a button press and for the remainder of the 20s elaborated on the event. Importantly, all events generated were episodic and did not differ on a number of phenomenological qualities (detail, emotionality, personal significance, field/observer perspective). Conjunction analyses indicated the left hippocampus was commonly engaged by past and future event construction, along with posterior visuospatial regions, but considerable neural differentiation was also observed during the construction phase. Future events recruited regions involved in prospective thinking and generation processes, specifically right frontopolar cortex and left ventrolateral prefrontal cortex, respectively. Furthermore, future event construction uniquely engaged the right hippocampus, possibly as a response to the novelty of these events. In contrast to the construction phase, elaboration was characterized by remarkable overlap in regions comprising the autobiographical memory retrieval network, attributable to the common processes engaged during elaboration, including self-referential processing, contextual and episodic imagery. This striking neural overlap is consistent with findings that amnesic patients exhibit deficits in both past and future thinking, and confirms that the episodic system contributes importantly to imagining the future.
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                Author and article information

                Journal
                Soc Cogn Affect Neurosci
                Soc Cogn Affect Neurosci
                scan
                Social Cognitive and Affective Neuroscience
                Oxford University Press
                1749-5016
                1749-5024
                March 2020
                04 April 2020
                04 April 2020
                : 15
                : 3
                : 273-284
                Affiliations
                [1] Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna , Liebiggasse 5, Vienna 1010, Austria
                Author notes
                Correspondence should be addressed to Isabella C. Wagner, Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Liebiggasse 5, Vienna 1010, Austria. E-mail: isabella.wagner@ 123456univie.ac.at .
                Author information
                http://orcid.org/0000-0002-4383-8204
                Article
                nsaa045
                10.1093/scan/nsaa045
                7235961
                32248233
                e4f57fb2-be10-4116-a3f7-29da1cd288a6
                © The Author(s) 2020. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution NonCommercial-NoDerivs licence ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 4 November 2019
                : 23 March 2020
                : 24 March 2020
                Page count
                Pages: 12
                Funding
                Funded by: Vienna Science and Technology Fund, DOI 10.13039/501100001821;
                Award ID: CS11-016
                Funded by: Austrian Science Fund, DOI 10.13039/501100002428;
                Award ID: P32686
                Categories
                Original Manuscript

                Neurosciences
                empathy,fmri,functional connectivity,hippocampus,representational similarity analysis (rsa)

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