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      Frequency-dependent changes in sensorimotor and pain affective systems induced by empathy for pain

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          Abstract

          Background

          Empathy for pain helps us to understand the pain of others indirectly. To better comprehend the processing of empathic pain, we report the frequency-dependent modulation of cortical oscillations induced by watching movies depicting pain using high-density electroencephalography (EEG), magnetoencephalography (MEG), and motor evoked potentials (MEP).

          Methods

          Event-related desynchronization of EEG and MEG was assessed while participants viewed videos of painful (needle) or neutral (cotton swab) situations. The amplitudes of MEPs were also compared between the needle and cotton swab conditions.

          Results

          The degree of suppression in α/β band power was significantly increased, whereas that of γ band power was significantly decreased, in the needle condition compared with the cotton swab condition. EEG revealed that significant differences in α/β band were distributed in the right frontocentral and left parietooccipital regions, whereas significant γ band differences were distributed predominantly over the right hemisphere, which were confirmed by source estimation using MEG. There was a significant positive correlation between the difference in γ power of the two conditions and the visual analog scale subjective rating of aversion, but not in the α/β band. The amplitude of MEPs decreased in the needle condition, which confirmed the inhibition of the primary motor cortex.

          Conclusion

          MEP suppression supports that modulation of cortical oscillations by viewing movies depicting pain involves sensorimotor processing. Our results suggest that α/β oscillations underlie the sensory qualities of others’ pain, whereas the γ band reflects the cognitive aspect. Therefore, α/β and γ band oscillations are differentially involved in empathic pain processing under the condition of motor cortical suppression.

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          Most cited references 32

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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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            Dynamic imaging of coherent sources: Studying neural interactions in the human brain.

            Functional connectivity between cortical areas may appear as correlated time behavior of neural activity. It has been suggested that merging of separate features into a single percept ("binding") is associated with coherent gamma band activity across the cortical areas involved. Therefore, it would be of utmost interest to image cortico-cortical coherence in the working human brain. The frequency specificity and transient nature of these interactions requires time-sensitive tools such as magneto- or electroencephalography (MEG/EEG). Coherence between signals of sensors covering different scalp areas is commonly taken as a measure of functional coupling. However, this approach provides vague information on the actual cortical areas involved, owing to the complex relation between the active brain areas and the sensor recordings. We propose a solution to the crucial issue of proceeding beyond the MEG sensor level to estimate coherences between cortical areas. Dynamic imaging of coherent sources (DICS) uses a spatial filter to localize coherent brain regions and provides the time courses of their activity. Reference points for the computation of neural coupling may be based on brain areas of maximum power or other physiologically meaningful information, or they may be estimated starting from sensor coherences. The performance of DICS is evaluated with simulated data and illustrated with recordings of spontaneous activity in a healthy subject and a parkinsonian patient. Methods for estimating functional connectivities between brain areas will facilitate characterization of cortical networks involved in sensory, motor, or cognitive tasks and will allow investigation of pathological connectivities in neurological disorders.
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              • Abstract: found
              • Article: not found

              The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations.

              The parieto-frontal cortical circuit that is active during action observation is the circuit with mirror properties that has been most extensively studied. Yet, there remains controversy on its role in social cognition and its contribution to understanding the actions and intentions of other individuals. Recent studies in monkeys and humans have shed light on what the parieto-frontal cortical circuit encodes and its possible functional relevance for cognition. We conclude that, although there are several mechanisms through which one can understand the behaviour of other individuals, the parieto-frontal mechanism is the only one that allows an individual to understand the action of others 'from the inside' and gives the observer a first-person grasp of the motor goals and intentions of other individuals.
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                Author and article information

                Journal
                J Pain Res
                J Pain Res
                Journal of Pain Research
                Journal of Pain Research
                Dove Medical Press
                1178-7090
                2017
                29 May 2017
                : 10
                : 1317-1326
                Affiliations
                [1 ]Department of Clinical Neurophysiology, Neurological Institute
                [2 ]Department of Anesthesiology and Critical Care Medicine, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
                Author notes
                Correspondence: Katsuya Ogata, Department of Clinical Neurophysiology, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan, Tel +81 92 642 5543, Fax +81 92 642 5545, Email katuya@ 123456med.kyushu-u.ac.jp
                [*]

                These authors contributed equally to this work

                Article
                jpr-10-1317
                10.2147/JPR.S129791
                5459954
                © 2017 Motoyama et al. This work is published and licensed by Dove Medical Press Limited

                The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed.

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                Original Research

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