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      The highly sensitive brain: an fMRI study of sensory processing sensitivity and response to others' emotions

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          Abstract

          Background

          Theory and research suggest that sensory processing sensitivity (SPS), found in roughly 20% of humans and over 100 other species, is a trait associated with greater sensitivity and responsiveness to the environment and to social stimuli. Self-report studies have shown that high-SPS individuals are strongly affected by others' moods, but no previous study has examined neural systems engaged in response to others' emotions.

          Methods

          This study examined the neural correlates of SPS (measured by the standard short-form Highly Sensitive Person [HSP] scale) among 18 participants (10 females) while viewing photos of their romantic partners and of strangers displaying positive, negative, or neutral facial expressions. One year apart, 13 of the 18 participants were scanned twice.

          Results

          Across all conditions, HSP scores were associated with increased brain activation of regions involved in attention and action planning (in the cingulate and premotor area [PMA]). For happy and sad photo conditions, SPS was associated with activation of brain regions involved in awareness, integration of sensory information, empathy, and action planning (e.g., cingulate, insula, inferior frontal gyrus [IFG], middle temporal gyrus [MTG], and PMA).

          Conclusions

          As predicted, for partner images and for happy facial photos, HSP scores were associated with stronger activation of brain regions involved in awareness, empathy, and self-other processing. These results provide evidence that awareness and responsiveness are fundamental features of SPS, and show how the brain may mediate these traits.

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          Most cited references55

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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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            Coping styles in animals: current status in behavior and stress-physiology.

            This paper summarizes the current views on coping styles as a useful concept in understanding individual adaptive capacity and vulnerability to stress-related disease. Studies in feral populations indicate the existence of a proactive and a reactive coping style. These coping styles seem to play a role in the population ecology of the species. Despite domestication, genetic selection and inbreeding, the same coping styles can, to some extent, also be observed in laboratory and farm animals. Coping styles are characterized by consistent behavioral and neuroendocrine characteristics, some of which seem to be causally linked to each other. Evidence is accumulating that the two coping styles might explain a differential vulnerability to stress mediated disease due to the differential adaptive value of the two coping styles and the accompanying neuroendocrine differentiation.
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              Mirror neurons and the simulation theory of mind-reading.

              V Gallese (1998)
              A new class of visuomotor neuron has been recently discovered in the monkey's premotor cortex: mirror neurons. These neurons respond both when a particular action is performed by the recorded monkey and when the same action, performed by another individual, is observed. Mirror neurons appear to form a cortical system matching observation and execution of goal-related motor actions. Experimental evidence suggests that a similar matching system also exists in humans. What might be the functional role of this matching system? One possible function is to enable an organism to detect certain mental states of observed conspecifics. This function might be part of, or a precursor to, a more general mind-reading ability. Two different accounts of mind-reading have been suggested. According to `theory theory', mental states are represented as inferred posits of a naive theory. According to `simulation theory', other people's mental states are represented by adopting their perspective: by tracking or matching their states with resonant states of one's own. The activity of mirror neurons, and the fact that observers undergo motor facilitation in the same muscular groups as those utilized by target agents, are findings that accord well with simulation theory but would not be predicted by theory theory.
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                Author and article information

                Journal
                Brain Behav
                Brain Behav
                brb3
                Brain and Behavior
                Blackwell Publishing Ltd (Oxford, UK )
                2162-3279
                2162-3279
                July 2014
                23 June 2014
                : 4
                : 4
                : 580-594
                Affiliations
                [1 ]Department of Psychological and Brain Sciences, University of California Santa Barbara, California
                [2 ]Department of Psychology, Stony Brook University New York, New York
                [3 ]Monmouth University Monmouth County, New Jersey
                [4 ]Department of Neurology, Albert Einstein College of Medicine Bronx, New York
                Author notes
                Bianca P. Acevedo, Department of Psychological and Brain Sciences, University of California, Santa Barbara, CA 93106-9660. Tel: 516-298-2422; Fax: 718-565-8728; E-mail: acevedo@ 123456psych.ucsb.edu .

                Funding Information This research was supported by grants from the National Science Foundation (0958171) and the University of California at Santa Barbara's Brain Imaging Center.

                Article
                10.1002/brb3.242
                4086365
                25161824
                d6124a17-0dc7-4d3c-9199-1cd241e7ed6f
                © 2014 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 01 October 2013
                : 30 March 2014
                : 30 April 2014
                Categories
                Original Research

                Neurosciences
                emotion,empathy,highly sensitive person,magnetic resonance imaging,mirror neurons,sensory processing sensitivity

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