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      Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks

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          Significance

          The frontoparietal control network (FPCN) contributes to executive control, the ability to deliberately guide action based on goals. While the FPCN is often viewed as a unitary domain general system, it is possible that the FPCN contains a fine-grained internal organization, with separate zones involved in different types of executive control. Here, we use graph theory and meta-analytic functional profiling to demonstrate that the FPCN is composed of two separate subsystems: FPCN A is connected to the default network and is involved in the regulation of introspective processes, whereas FPCN B is connected to the dorsal attention network and is involved in the regulation of perceptual attention. These findings offer a distinct perspective on the systems-level circuitry underlying cognitive control.

          Abstract

          The frontoparietal control network (FPCN) plays a central role in executive control. It has been predominantly viewed as a unitary domain general system. Here, we examined patterns of FPCN functional connectivity (FC) across multiple conditions of varying cognitive demands, to test for FPCN heterogeneity. We identified two distinct subsystems within the FPCN based on hierarchical clustering and machine learning classification analyses of within-FPCN FC patterns. These two FPCN subsystems exhibited distinct patterns of FC with the default network (DN) and the dorsal attention network (DAN). FPCN A exhibited stronger connectivity with the DN than the DAN, whereas FPCN B exhibited the opposite pattern. This twofold FPCN differentiation was observed across four independent datasets, across nine different conditions (rest and eight tasks), at the level of individual-participant data, as well as in meta-analytic coactivation patterns. Notably, the extent of FPCN differentiation varied across conditions, suggesting flexible adaptation to task demands. Finally, we used meta-analytic tools to identify several functional domains associated with the DN and DAN that differentially predict activation in the FPCN subsystems. These findings reveal a flexible and heterogeneous FPCN organization that may in part emerge from separable DN and DAN processing streams. We propose that FPCN A may be preferentially involved in the regulation of introspective processes, whereas FPCN B may be preferentially involved in the regulation of visuospatial perceptual attention.

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          Most cited references60

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          Situating the default-mode network along a principal gradient of macroscale cortical organization.

          Understanding how the structure of cognition arises from the topographical organization of the cortex is a primary goal in neuroscience. Previous work has described local functional gradients extending from perceptual and motor regions to cortical areas representing more abstract functions, but an overarching framework for the association between structure and function is still lacking. Here, we show that the principal gradient revealed by the decomposition of connectivity data in humans and the macaque monkey is anchored by, at one end, regions serving primary sensory/motor functions and at the other end, transmodal regions that, in humans, are known as the default-mode network (DMN). These DMN regions exhibit the greatest geodesic distance along the cortical surface-and are precisely equidistant-from primary sensory/motor morphological landmarks. The principal gradient also provides an organizing spatial framework for multiple large-scale networks and characterizes a spectrum from unimodal to heteromodal activity in a functional metaanalysis. Together, these observations provide a characterization of the topographical organization of cortex and indicate that the role of the DMN in cognition might arise from its position at one extreme of a hierarchy, allowing it to process transmodal information that is unrelated to immediate sensory input.
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            From sensation to cognition.

            M. Mesulam (1998)
            Sensory information undergoes extensive associative elaboration and attentional modulation as it becomes incorporated into the texture of cognition. This process occurs along a core synaptic hierarchy which includes the primary sensory, upstream unimodal, downstream unimodal, heteromodal, paralimbic and limbic zones of the cerebral cortex. Connections from one zone to another are reciprocal and allow higher synaptic levels to exert a feedback (top-down) influence upon earlier levels of processing. Each cortical area provides a nexus for the convergence of afferents and divergence of efferents. The resultant synaptic organization supports parallel as well as serial processing, and allows each sensory event to initiate multiple cognitive and behavioural outcomes. Upstream sectors of unimodal association areas encode basic features of sensation such as colour, motion, form and pitch. More complex contents of sensory experience such as objects, faces, word-forms, spatial locations and sound sequences become encoded within downstream sectors of unimodal areas by groups of coarsely tuned neurons. The highest synaptic levels of sensory-fugal processing are occupied by heteromodal, paralimbic and limbic cortices, collectively known as transmodal areas. The unique role of these areas is to bind multiple unimodal and other transmodal areas into distributed but integrated multimodal representations. Transmodal areas in the midtemporal cortex, Wernicke's area, the hippocampal-entorhinal complex and the posterior parietal cortex provide critical gateways for transforming perception into recognition, word-forms into meaning, scenes and events into experiences, and spatial locations into targets for exploration. All cognitive processes arise from analogous associative transformations of similar sets of sensory inputs. The differences in the resultant cognitive operation are determined by the anatomical and physiological properties of the transmodal node that acts as the critical gateway for the dominant transformation. Interconnected sets of transmodal nodes provide anatomical and computational epicentres for large-scale neurocognitive networks. In keeping with the principles of selectively distributed processing, each epicentre of a large-scale network displays a relative specialization for a specific behavioural component of its principal neurospychological domain. The destruction of transmodal epicentres causes global impairments such as multimodal anomia, neglect and amnesia, whereas their selective disconnection from relevant unimodal areas elicits modality-specific impairments such as prosopagnosia, pure word blindness and category-specific anomias. The human brain contains at least five anatomically distinct networks. The network for spatial awareness is based on transmodal epicentres in the posterior parietal cortex and the frontal eye fields; the language network on epicentres in Wernicke's and Broca's areas; the explicit memory/emotion network on epicentres in the hippocampal-entorhinal complex and the amygdala; the face-object recognition network on epicentres in the midtemporal and temporopolar cortices; and the working memory-executive function network on epicentres in the lateral prefrontal cortex and perhaps the posterior parietal cortex. Individual sensory modalities give rise to streams of processing directed to transmodal nodes belonging to each of these networks. The fidelity of sensory channels is actively protected through approximately four synaptic levels of sensory-fugal processing. The modality-specific cortices at these four synaptic levels encode the most veridical representations of experience. Attentional, motivational and emotional modulations, including those related to working memory, novelty-seeking and mental imagery, become increasingly more pronounced within downstream components of unimodal areas, where they help to create a highly edited subjective version of the world. (ABSTRACT TRUNCATED)
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              Multi-task connectivity reveals flexible hubs for adaptive task control

              Extensive evidence suggests the human ability to adaptively implement a wide variety of tasks is preferentially due to the operation of a fronto-parietal brain network. We hypothesized that this network’s adaptability is made possible by ‘flexible hubs’ – brain regions that rapidly update their pattern of global functional connectivity according to task demands. We utilized recent advances in characterizing brain network organization and dynamics to identify mechanisms consistent with the flexible hub theory. We found that the fronto-parietal network’s brain-wide functional connectivity pattern shifted more than other networks’ across a variety of task states, and that these connectivity patterns could be used to identify the current task. Further, these patterns were consistent across practiced and novel tasks, suggesting reuse of flexible hub connectivity patterns facilitates adaptive (novel) task performance. Together, these findings support a central role for fronto-parietal flexible hubs in cognitive control and adaptive implementation of task demands generally.
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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
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                13 February 2018
                30 January 2018
                : 115
                : 7
                : E1598-E1607
                Affiliations
                [1] aDepartment of Psychology, University of British Columbia , Vancouver, BC V6T 1Z4, Canada;
                [2] bDepartment of Psychology, University of Texas at Austin , Austin, TX 78712;
                [3] cInstitute of Cognitive Science, University of Colorado at Boulder , Boulder, CO 80309-0345;
                [4] dLaboratory of Brain and Cognition, Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University , Montreal, QC H3A 2B4, Canada;
                [5] eHuman Neuroscience Institute, Department of Human Development, Cornell University , Ithaca, NY 14853-7601;
                [6] fCenter for Molecular and Behavioral Neuroscience, Rutgers University , Newark, NJ 08854;
                [7] gCentre for Brain Health, University of British Columbia , Vancouver, BC V6T 1Z4, Canada
                Author notes
                1To whom correspondence may be addressed. Email: mattdixon99@ 123456gmail.com or kchristoff@ 123456psych.ubc.ca .

                Edited by Earl K. Miller, Massachusetts Institute of Technology, Cambridge, MA, and accepted by Editorial Board Member Michael S. Gazzaniga January 8, 2018 (received for review September 6, 2017)

                Author contributions: M.L.D. and K.C. designed research; M.L.D. performed research; J.A.-H., R.N.S., and M.W.C. contributed new reagents/analytic tools; M.L.D., A.D.L.V., and C.M. analyzed data; J.A.-H., R.N.S., M.W.C., and K.C. provided guidance on analyses; and M.L.D. wrote the paper.

                Author information
                http://orcid.org/0000-0001-8033-8113
                http://orcid.org/0000-0003-1530-8916
                Article
                PMC5816169 PMC5816169 5816169 201715766
                10.1073/pnas.1715766115
                5816169
                29382744
                ddc8b67c-9818-4207-87aa-bee44e92fac7
                Copyright @ 2018

                Published under the PNAS license.

                History
                Page count
                Pages: 10
                Funding
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: RGPIN 327317-11
                Funded by: Gouvernement du Canada | Canadian Institutes of Health Research (CIHR) 501100000024
                Award ID: MOP-115197
                Categories
                PNAS Plus
                Biological Sciences
                Neuroscience
                PNAS Plus

                cognitive control,frontoparietal control network,default network,dorsal attention network,functional connectivity

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