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      Task-relevant brain networks identified with simultaneous PET/MR imaging of metabolism and connectivity

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          Abstract

          Except for task-specific functional MRI, the vast majority of imaging studies assessed human brain function at resting conditions. However, tracking task-specific neuronal activity yields important insight how the brain responds to stimulation. We specifically investigated changes in glucose metabolism, functional connectivity and white matter microstructure during task performance using several recent methodological advancements. Opening the eyes and right finger tapping had elicited an increased glucose metabolism in primary visual and motor cortices, respectively. Furthermore, a decreased metabolism was observed in the regions of the default mode network, which allowed absolute quantification of commonly described deactivations during cognitive tasks. These brain regions showed widespread task-specific changes in functional connectivity, which stretched beyond their primary resting-state networks and presumably reflected the level of recruitment of certain brain regions for each task. Finally, the corresponding white matter fiber pathways exhibited changes in axial and radial diffusivity during the tasks, which were regionally distinctive for certain tract groups. These results highlight that even simple task performance leads to substantial changes of entire brain networks. Exploiting the complementary nature of the different imaging modalities may reveal novel insights how the brain processes external stimuli and which networks are involved in certain tasks.

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          The online version of this article (10.1007/s00429-017-1558-0) contains supplementary material, which is available to authorized users.

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          Most cited references41

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          Two systems of resting state connectivity between the insula and cingulate cortex.

          The insula and cingulate cortices are implicated in emotional, homeostatic/allostatic, sensorimotor, and cognitive functions. Non-human primates have specific anatomical connections between sub-divisions of the insula and cingulate. Specifically, the anterior insula projects to the pregenual anterior cingulate cortex (pACC) and the anterior and posterior mid-cingulate cortex (aMCC and pMCC); the mid-posterior insula only projects to the posterior MCC (pMCC). In humans, functional neuroimaging studies implicate the anterior insula and pre/subgenual ACC in emotional processes, the mid-posterior insula with awareness and interoception, and the MCC with environmental monitoring, response selection, and skeletomotor body orientation. Here, we tested the hypothesis that distinct resting state functional connectivity could be identified between (1) the anterior insula and pACC/aMCC; and (2) the entire insula (anterior, middle, and posterior insula) and the pMCC. Functional connectivity was assessed from resting state fMRI scans in 19 healthy volunteers using seed regions of interest in the anterior, middle, and posterior insula. Highly correlated, low-frequency oscillations (< 0.05 Hz) were identified between specific insula and cingulate subdivisions. The anterior insula was shown to be functionally connected with the pACC/aMCC and the pMCC, while the mid/posterior insula was only connected with the pMCC. These data provide evidence for a resting state anterior insula-pACC/aMCC cingulate system that may integrate interoceptive information with emotional salience to form a subjective representation of the body; and another system that includes the entire insula and MCC, likely involved in environmental monitoring, response selection, and skeletomotor body orientation. 2008 Wiley-Liss, Inc.
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            Decoupling of the brain's default mode network during deep sleep.

            The recent discovery of a circuit of brain regions that is highly active in the absence of overt behavior has led to a quest for revealing the possible function of this so-called default-mode network (DMN). A very recent study, finding similarities in awake humans and anesthetized primates, has suggested that DMN activity might not simply reflect ongoing conscious mentation but rather a more general form of network dynamics typical of complex systems. Here, by performing functional MRI in humans, it is shown that a natural, sleep-induced reduction of consciousness is reflected in altered correlation between DMN network components, most notably a reduced involvement of frontal cortex. This suggests that DMN may play an important role in the sustenance of conscious awareness.
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              Significance of the insula for the evolution of human awareness of feelings from the body.

              An ascending sensory pathway that underlies feelings from the body, such as cooling or toothache, terminates in the posterior insula. Considerable evidence suggests that this activity is rerepresented and integrated first in the mid-insula and then in the anterior insula. Activation in the anterior insula correlates directly with subjective feelings from the body and, strikingly, with all emotional feelings. These findings appear to signify a posterior-to-anterior sequence of increasingly homeostatically efficient representations that integrate all salient neural activity, culminating in network nodes in the right and left anterior insulae that may be organized asymmetrically in an opponent fashion. The anterior insula has appropriate characteristics to support the proposal that it engenders a cinemascopic model of human awareness and subjectivity. This review presents the author's views regarding the principles of organization of this system and discusses a possible sequence for its evolution, as well as particular issues of historical interest. © 2011 New York Academy of Sciences.
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                Author and article information

                Contributors
                rupert.lanzenberger@meduniwien.ac.at
                Journal
                Brain Struct Funct
                Brain Struct Funct
                Brain Structure & Function
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1863-2653
                1863-2661
                13 November 2017
                13 November 2017
                2018
                : 223
                : 3
                : 1369-1378
                Affiliations
                [1 ]ISNI 0000 0000 9259 8492, GRID grid.22937.3d, Department of Psychiatry and Psychotherapy, , Medical University of Vienna, ; Waehringer Guertel 18-20, 1090 Vienna, Austria
                [2 ]ISNI 0000 0000 9259 8492, GRID grid.22937.3d, Division of Nuclear Medicine, Department of Biomedical Imaging and Image-guided Therapy, , Medical University of Vienna, ; Vienna, Austria
                [3 ]Center for Biomarker Research in Medicine (CBmed), Graz, Austria
                [4 ]Ludwig Bolzmann Institute Applied Diagnostics, Vienna, Austria
                Author information
                http://orcid.org/0000-0003-4641-9539
                Article
                1558
                10.1007/s00429-017-1558-0
                5869947
                29134288
                6392e2e1-73c7-4c83-8690-414beaca6ed3
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 12 April 2017
                : 30 October 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002428, Austrian Science Fund;
                Award ID: FWF KLI 610
                Award ID: FWF KLI 516
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001822, Austrian Academy of Sciences;
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                Neurology
                continuous task performance,functional connectivity,glucose metabolism,white matter microstructure,functional pet, fpet

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