1
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Anterior insula regulates brain network transitions that gate conscious access

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          SUMMARY

          Conscious access to sensory information is likely gated at an intermediate site between primary sensory and transmodal association cortices, but the structure responsible remains unknown. We perform functional neuroimaging to determine the neural correlates of conscious access using a volitional mental imagery task, a report paradigm not confounded by motor behavior. Titrating propofol to loss of behavioral responsiveness in healthy volunteers creates dysfunction of the anterior insular cortex (AIC) in association with an impairment of dynamic transitions of default-mode and dorsal attention networks. Candidate subcortical regions mediating sensory gating or arousal (thalamus, basal forebrain) fail to show this association. The gating role of the AIC is consistent with findings in awake participants, whose conscious access is predicted by pre-stimulus AIC activity near perceptual threshold. These data support the hypothesis that AIC, situated at an intermediate position of the cortical hierarchy, regulates brain network transitions that gate conscious access.

          Graphical abstract

          In brief

          In a human neuroimaging study, Huang et al. manipulate the level and content of consciousness using independent experimental protocols to demonstrate that the anterior insula, situated between unimodal and transmodal cortical areas along the brain’s functional hierarchy, serves as a gate for conscious access of sensory information.

          Related collections

          Most cited references80

          • Record: found
          • Abstract: found
          • Article: not found

          The organization of the human cerebral cortex estimated by intrinsic functional connectivity.

          Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Dissociable intrinsic connectivity networks for salience processing and executive control.

            Variations in neural circuitry, inherited or acquired, may underlie important individual differences in thought, feeling, and action patterns. Here, we used task-free connectivity analyses to isolate and characterize two distinct networks typically coactivated during functional MRI tasks. We identified a "salience network," anchored by dorsal anterior cingulate (dACC) and orbital frontoinsular cortices with robust connectivity to subcortical and limbic structures, and an "executive-control network" that links dorsolateral frontal and parietal neocortices. These intrinsic connectivity networks showed dissociable correlations with functions measured outside the scanner. Prescan anxiety ratings correlated with intrinsic functional connectivity of the dACC node of the salience network, but with no region in the executive-control network, whereas executive task performance correlated with lateral parietal nodes of the executive-control network, but with no region in the salience network. Our findings suggest that task-free analysis of intrinsic connectivity networks may help elucidate the neural architectures that support fundamental aspects of human behavior.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Saliency, switching, attention and control: a network model of insula function.

              The insula is a brain structure implicated in disparate cognitive, affective, and regulatory functions, including interoceptive awareness, emotional responses, and empathic processes. While classically considered a limbic region, recent evidence from network analysis suggests a critical role for the insula, particularly the anterior division, in high-level cognitive control and attentional processes. The crucial insight and view we present here is of the anterior insula as an integral hub in mediating dynamic interactions between other large-scale brain networks involved in externally oriented attention and internally oriented or self-related cognition. The model we present postulates that the insula is sensitive to salient events, and that its core function is to mark such events for additional processing and initiate appropriate control signals. The anterior insula and the anterior cingulate cortex form a "salience network" that functions to segregate the most relevant among internal and extrapersonal stimuli in order to guide behavior. Within the framework of our network model, the disparate functions ascribed to the insula can be conceptualized by a few basic mechanisms: (1) bottom-up detection of salient events, (2) switching between other large-scale networks to facilitate access to attention and working memory resources when a salient event is detected, (3) interaction of the anterior and posterior insula to modulate autonomic reactivity to salient stimuli, and (4) strong functional coupling with the anterior cingulate cortex that facilitates rapid access to the motor system. In this manner, with the insula as its integral hub, the salience network assists target brain regions in the generation of appropriate behavioral responses to salient stimuli. We suggest that this framework provides a parsimonious account of insula function in neurotypical adults, and may provide novel insights into the neural basis of disorders of affective and social cognition.
                Bookmark

                Author and article information

                Journal
                101573691
                39703
                Cell Rep
                Cell Rep
                Cell reports
                2211-1247
                17 May 2021
                04 May 2021
                27 May 2021
                : 35
                : 5
                : 109081
                Affiliations
                [1 ]Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA
                [2 ]Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA
                [3 ]Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI 48109, USA
                [4 ]Lead contact
                Author notes

                AUTHOR CONTRIBUTIONS

                Z.H. designed and conducted both the pharmacological and psychological experiments, analyzed the data, interpreted data, and wrote the article. V.T., P.E.V., E.L.J., and P.P. performed the anesthetic procedures. A.M.M. coordinated the experiment. G.A.M. interpreted data and wrote the article. A.G.H. conceived the project, designed the pharmacological experiment, interpreted data, and wrote the article.

                [* ]Correspondence: huangzu@ 123456umich.edu (Z.H.), ahudetz@ 123456med.umich.edu (A.G.H.)
                Article
                NIHMS1700576
                10.1016/j.celrep.2021.109081
                8157795
                33951427
                e5082c42-19c7-45b9-b40a-4546ef2846cf

                This is an open access article under the CC BY-NC-ND license.

                History
                Categories
                Article

                Cell biology
                Cell biology

                Comments

                Comment on this article