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      The middle cingulate cortex and dorso-central insula: A mirror circuit encoding observation and execution of vitality forms

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          Vitality forms represent the different ways in which actions are performed (e.g., gentle, rude). They express the agent’s attitudes toward others. Previous data indicated that vitality forms of hand actions depend on the dorso-central insula. In the present study, we show that in addition to the insula, the middle cingulate cortex is also involved in hand action modulation. A voxel-based analysis highlighted that voxels showing a similar BOLD signal trend in both action observation and execution are present in both regions. Using a multifiber tractography investigation, we demonstrated that the dorso-central insula and middle cingulate cortex are anatomically connected. These data indicate that the modulation of the parieto-frontal circuit controlling hand actions relies on both the insula and cingulate sectors.

          Abstract

          Actions with identical goals can be executed in different ways (gentle, rude, vigorous, etc.), which D. N. Stern called vitality forms [D. N. Stern, Forms of Vitality Exploring Dynamic Experience in Psychology, Arts, Psychotherapy, and Development (2010)]. Vitality forms express the agent’s attitudes toward others. In a series of fMRI studies, we found that the dorso-central insula (DCI) is the region that is selectively active during both vitality form observation and execution. In one previous experiment, however, the middle cingulate gyrus also exhibited activation. In the present study, in order to assess the role of the cingulate cortex in vitality form processing, we adopted a classical vitality form paradigm, but making the control condition devoid of vitality forms using jerky movements. Participants performed two different tasks: Observation of actions performed gently or rudely and execution of the same actions. The results showed that in addition to the insula, the middle cingulate cortex (MCC) was strongly activated during both action observation and execution. Using a voxel-based analysis, voxels showing a similar trend of the blood-oxygen-level-dependent (BOLD) signal in both action observation and execution were found in the DCI and in the MCC. Finally, using a multifiber tractography analysis, we showed that the active sites in MCC and DCI are reciprocally connected.

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          Most cited references26

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          How do you feel? Interoception: the sense of the physiological condition of the body.

          A. Craig (2002)
          As humans, we perceive feelings from our bodies that relate our state of well-being, our energy and stress levels, our mood and disposition. How do we have these feelings? What neural processes do they represent? Recent functional anatomical work has detailed an afferent neural system in primates and in humans that represents all aspects of the physiological condition of the physical body. This system constitutes a representation of 'the material me', and might provide a foundation for subjective feelings, emotion and self-awareness.
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            A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis.

            Whether we feel sympathy for another, listen to our heartbeat, experience pain or negotiate, the insular cortex is thought to integrate perceptions, emotions, thoughts, and plans into one subjective image of "our world". The insula has hence been ascribed an integrative role, linking information from diverse functional systems. Nevertheless, various anatomical and functional studies in humans and non-human primates also indicate a functional differentiation of this region. In order to investigate this functional differentiation as well as the mechanisms of the functional integration in the insula, we performed activation-likelihood-estimation (ALE) meta-analyses of 1,768 functional neuroimaging experiments. The analysis revealed four functionally distinct regions on the human insula, which map to the social-emotional, the sensorimotor, the olfacto-gustatory, and the cognitive network of the brain. Sensorimotor tasks activated the mid-posterior and social-emotional tasks the anterior-ventral insula. In the central insula activation by olfacto-gustatory stimuli was found, and cognitive tasks elicited activation in the anterior-dorsal region. A conjunction analysis across these domains revealed that aside from basic somatosensory and motor processes all tested functions overlapped on the anterior-dorsal insula. This overlap might constitute a correlate for a functional integration between different functional systems and thus reflect a link between them necessary to integrate different qualities into a coherent experience of the world and setting the context for thoughts and actions.
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              Towards the neurobiology of emotional body language.

              People's faces show fear in many different circumstances. However, when people are terrified, as well as showing emotion, they run for cover. When we see a bodily expression of emotion, we immediately know what specific action is associated with a particular emotion, leaving little need for interpretation of the signal, as is the case for facial expressions. Research on emotional body language is rapidly emerging as a new field in cognitive and affective neuroscience. This article reviews how whole-body signals are automatically perceived and understood, and their role in emotional communication and decision-making.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                29 October 2021
                2 November 2021
                29 October 2021
                : 118
                : 44
                : e2111358118
                Affiliations
                [1] aCognitive Architecture for Collaborative Technologies Unit, Italian Institute of Technology , Genova 16152, Italy;
                [2] bDepartment of Computer Science, University of Milan , Milan 20135, Italy;
                [3] cDepartment of Informatics, Bioengineering, Robotics, and Systems Engineering, University of Genoa , Genoa 16145, Italy;
                [4] dDepartment of Medicine and Surgery, University of Parma , Parma 43100, Italy;
                [5] eIstituto di Neuroscienze, Consiglio Nazionale delle Ricerche , Parma 43100, Italy
                Author notes
                1To whom correspondence may be addressed. Email: giacomo.rizzolatti@ 123456unipr.it .

                Contributed by G. Rizzolatti, September 13, 2021 (sent for review June 23, 2021; reviewed by David M. A. Mehler, Marco Tamietto, and Christian Wolf)

                Author contributions: G.D.C., A.S., and G.R. designed research; G.D.C. performed research; G.D.C., M.M., G.L., M.G., and A.S. analyzed data; and G.D.C., M.G., and G.R. wrote the paper.

                Author information
                https://orcid.org/0000-0001-9700-5171
                Article
                202111358
                10.1073/pnas.2111358118
                8612212
                34716272
                4b8a0c62-9606-43d9-8d5c-47a4a921ef8b
                Copyright © 2021 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 23 September 2021
                Page count
                Pages: 6
                Funding
                Funded by: EC | H2020 | H2020 Priority Excellent Science | H2020 European Research Council (ERC) 100010663
                Award ID: 804388 wHISPER
                Award Recipient : Alessandra Sciutti
                Funded by: Grant: Lombardia è Ricerca
                Award ID: 2017
                Award Recipient : Giacomo Rizzolatti
                Categories
                424
                431
                Biological Sciences
                Neuroscience
                Social Sciences
                Psychological and Cognitive Sciences

                vitality form network,cingulate,insula,mirror mechanism,social interaction

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