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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 references 73

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          How do you feel--now? The anterior insula and human awareness.

          The anterior insular cortex (AIC) is implicated in a wide range of conditions and behaviours, from bowel distension and orgasm, to cigarette craving and maternal love, to decision making and sudden insight. Its function in the re-representation of interoception offers one possible basis for its involvement in all subjective feelings. New findings suggest a fundamental role for the AIC (and the von Economo neurons it contains) in awareness, and thus it needs to be considered as a potential neural correlate of consciousness.
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            The mirror-neuron system.

            A category of stimuli of great importance for primates, humans in particular, is that formed by actions done by other individuals. If we want to survive, we must understand the actions of others. Furthermore, without action understanding, social organization is impossible. In the case of humans, there is another faculty that depends on the observation of others' actions: imitation learning. Unlike most species, we are able to learn by imitation, and this faculty is at the basis of human culture. In this review we present data on a neurophysiological mechanism--the mirror-neuron mechanism--that appears to play a fundamental role in both action understanding and imitation. We describe first the functional properties of mirror neurons in monkeys. We review next the characteristics of the mirror-neuron system in humans. We stress, in particular, those properties specific to the human mirror-neuron system that might explain the human capacity to learn by imitation. We conclude by discussing the relationship between the mirror-neuron system and language.
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              Thresholding of statistical maps in functional neuroimaging using the false discovery rate.

              Finding objective and effective thresholds for voxelwise statistics derived from neuroimaging data has been a long-standing problem. With at least one test performed for every voxel in an image, some correction of the thresholds is needed to control the error rates, but standard procedures for multiple hypothesis testing (e.g., Bonferroni) tend to not be sensitive enough to be useful in this context. This paper introduces to the neuroscience literature statistical procedures for controlling the false discovery rate (FDR). Recent theoretical work in statistics suggests that FDR-controlling procedures will be effective for the analysis of neuroimaging data. These procedures operate simultaneously on all voxelwise test statistics to determine which tests should be considered statistically significant. The innovation of the procedures is that they control the expected proportion of the rejected hypotheses that are falsely rejected. We demonstrate this approach using both simulations and functional magnetic resonance imaging data from two simple experiments. (C)2002 Elsevier Science (USA).
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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
                © 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.

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                Original Research

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