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      Processing of affective and emotionally neutral tactile stimuli in the insular cortex

      research-article
      a , * , b , c , a , d
      Developmental Cognitive Neuroscience
      Elsevier
      CT, C tactile, IC, insular cortex, pIC, posterior insular cortex, LpIC, left posterior insular cortex, aIC, anterior insular cortex, daIC, dorsal anterior insular cortex, vaIC, ventral anterior insular cortex, RdaIC, right dorsal anterior insular cortex, vmPFC, ventro medial prefrontal cortex, daCC, dorsal anterior cingulate cortex, pCC, posterior cingulate cortex, pgaCC, pregenual anterior cingulate cortex, mTG, medial temporal gyrus, lfrs, low frequency resting state, DMN, default mode network, SN, salience network, CEN, central executive network, VAS, visual analogue scale, BOLD, blood oxygenation level dependent, MRI, magnetic resonance imaging, GM, grey matter, MNI, Montreal Neurological Institute, GLM, general linear model, PPI, psychophysiological interaction, FEW, family-wise error, ROI, region of interest, Touch, fMRI, Insula, Resting state networks

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          Abstract

          The insula is important for the processing of pleasant aspects of touch whereas its role in the processing of emotionally neutral touch has been less explored. Here, we used a network approach to investigate the insular processing of pleasant stroking touch and emotionally neutral vibratory touch, analysing functional magnetic resonance imaging data from 23 healthy adult participants. Vibration and skin stroking activated areas in the posterior, middle and anterior insula. Psychophysiological interaction analyses suggested that skin stroking increased functional connectivity between the posterior and ventral anterior insula. Vibration instead increased functional connectivity between the posterior and dorsal anterior insula, and induced a stronger decrease of the default mode network activity compared to stroking. These results confirmed findings from previous studies showing that the posterior insula processes affective touch information. We suggest that this is accomplished by relaying tactile information from the posterior insula to ventral anterior insula, an area tightly connected to the emotional parts of the brain. However, our results also suggested that the insula processes tactile information with less emotional valence. A central hub in this processing seemed to be the right dorsal anterior insula.

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          Most cited references31

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          Three Systems of Insular Functional Connectivity Identified with Cluster Analysis

          Despite much research on the function of the insular cortex, few studies have investigated functional subdivisions of the insula in humans. The present study used resting-state functional connectivity magnetic resonance imaging (MRI) to parcellate the human insular lobe based on clustering of functional connectivity patterns. Connectivity maps were computed for each voxel in the insula based on resting-state functional MRI (fMRI) data and segregated using cluster analysis. We identified 3 insular subregions with distinct patterns of connectivity: a posterior region, functionally connected with primary and secondary somatomotor cortices; a dorsal anterior to middle region, connected with dorsal anterior cingulate cortex, along with other regions of a previously described control network; and a ventral anterior region, primarily connected with pregenual anterior cingulate cortex. Applying these regions to a separate task data set, we found that dorsal and ventral anterior insula responded selectively to disgusting images, while posterior insula did not. These results demonstrate that clustering of connectivity patterns can be used to subdivide cerebral cortex into anatomically and functionally meaningful subregions; the insular regions identified here should be useful in future investigations on the function of the insula.
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            The skin as a social organ.

            In general, social neuroscience research tends to focus on visual and auditory channels as routes for social information. However, because the skin is the site of events and processes crucial to the way we think about, feel about, and interact with one another, touch can mediate social perceptions in various ways. This review situates cutaneous perception within a social neuroscience framework by discussing evidence for considering touch (and to some extent pain) as a channel for social information. Social information conveys features of individuals or their interactions that have potential bearing on future interactions, and attendant mental and emotional states. Here, we discuss evidence for an affective dimension of touch and explore its wider implications for the exchange of social information. We consider three important roles for this affective dimension of the cutaneous senses in the transmission and processing of social information: first, through affiliative behavior and communication; second, via affective processing in skin-brain pathways; and third, as a basis for intersubjective representation.
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              The neurophysiology of unmyelinated tactile afferents.

              CT (C tactile) afferents are a distinct type of unmyelinated, low-threshold mechanoreceptive units existing in the hairy but not glabrous skin of humans and other mammals. Evidence from patients lacking myelinated tactile afferents indicates that signaling in these fibers activate the insular cortex. Since this system is poor in encoding discriminative aspects of touch, but well-suited to encoding slow, gentle touch, CT fibers in hairy skin may be part of a system for processing pleasant and socially relevant aspects of touch. CT fiber activation may also have a role in pain inhibition. This review outlines the growing evidence for unique properties and pathways of CT afferents.
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                Author and article information

                Contributors
                Journal
                Dev Cogn Neurosci
                Dev Cogn Neurosci
                Developmental Cognitive Neuroscience
                Elsevier
                1878-9293
                1878-9307
                22 December 2017
                February 2019
                22 December 2017
                : 35
                : 94-103
                Affiliations
                [a ]Institute of Neuroscience and Physiology, University of Gothenburg, Gothenburg, Sweden
                [b ]Department of Radiation Physics at the Institute of Clinical Sciences, University of Gothenburg, Gothenburg, Sweden
                [c ]Department of Medical Physics and Biomedical Engineering, Sahlgrenska University Hospital, Gothenburg, Sweden
                [d ]Center for Social and Affective Neuroscience (CSAN), Linköping University, Linköping, Sweden
                Author notes
                [* ]Corresponding author at: Blå Stråket 7, 41345 Gothenburg, Sweden. monika.davidovic@ 123456neuro.gu.se
                Article
                S1878-9293(17)30048-8
                10.1016/j.dcn.2017.12.006
                6968969
                29291986
                c5a979c2-bffa-44d9-bc6c-3f4a57737def
                © 2017 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 28 February 2017
                : 15 November 2017
                : 19 December 2017
                Categories
                Article

                Neurosciences
                ct, c tactile,ic, insular cortex,pic, posterior insular cortex,lpic, left posterior insular cortex,aic, anterior insular cortex,daic, dorsal anterior insular cortex,vaic, ventral anterior insular cortex,rdaic, right dorsal anterior insular cortex,vmpfc, ventro medial prefrontal cortex,dacc, dorsal anterior cingulate cortex,pcc, posterior cingulate cortex,pgacc, pregenual anterior cingulate cortex,mtg, medial temporal gyrus,lfrs, low frequency resting state,dmn, default mode network,sn, salience network,cen, central executive network,vas, visual analogue scale,bold, blood oxygenation level dependent,mri, magnetic resonance imaging,gm, grey matter,mni, montreal neurological institute,glm, general linear model,ppi, psychophysiological interaction,few, family-wise error,roi, region of interest,touch,fmri,insula,resting state networks

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