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      Benefits of Implicit Regulation of Instructed Fear: Evidence From Neuroimaging and Functional Connectivity

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          Abstract

          Instructed fear, which denotes fearful emotions learned from others’ verbal instructions, is an important form of fear acquisition in humans. Maladaptive instructed fear produces detrimental effects on health, but little is known about performing an efficient regulation of instructed fear and its underlying neural substrates. To address this question, 26 subjects performed an instructed fear task where emotional experiences and functional neuroimages were recorded during watching, explicit regulation (calmness imagination), and implicit regulation (calmness priming) conditions. Results indicated that implicit regulation decreased activity in the left amygdala and left insula for instructed fear; however, these effects were absent in explicit regulation. The implementation of implicit regulation did not increase activity in the frontoparietal control regions, while explicit regulation increased dorsolateral prefrontal cortex activity. Furthermore, implicit regulation increased functional connectivity between the right amygdala and right fusiform gyrus, and decreased functional connectivity between the right medial temporal gyrus and left inferior frontal gyrus, which are key nodes of memory retrieval and cognitive control networks, respectively. These findings suggest a favourable effect of implicit regulation on instructed fear, which is subserved by less involvement of control-related brain mechanisms.

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          Most cited references78

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          A dual-networks architecture of top-down control.

          Complex systems ensure resilience through multiple controllers acting at rapid and slower timescales. The need for efficient information flow through complex systems encourages small-world network structures. On the basis of these principles, a group of regions associated with top-down control was examined. Functional magnetic resonance imaging showed that each region had a specific combination of control signals; resting-state functional connectivity grouped the regions into distinct 'fronto-parietal' and 'cingulo-opercular' components. The fronto-parietal component seems to initiate and adjust control; the cingulo-opercular component provides stable 'set-maintenance' over entire task epochs. Graph analysis showed dense local connections within components and weaker 'long-range' connections between components, suggesting a small-world architecture. The control systems of the brain seem to embody the principles of complex systems, encouraging resilient performance.
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            Evidence for a frontoparietal control system revealed by intrinsic functional connectivity.

            Two functionally distinct, and potentially competing, brain networks have been recently identified that can be broadly distinguished by their contrasting roles in attention to the external world versus internally directed mentation involving long-term memory. At the core of these two networks are the dorsal attention system and the hippocampal-cortical memory system, a component of the brain's default network. Here spontaneous blood-oxygenation-level-dependent (BOLD) signal correlations were used in three separate functional magnetic resonance imaging data sets (n = 105) to define a third system, the frontoparietal control system, which is spatially interposed between these two previously defined systems. The frontoparietal control system includes many regions identified as supporting cognitive control and decision-making processes including lateral prefrontal cortex, anterior cingulate cortex, and inferior parietal lobule. Detailed analysis of frontal and parietal cortex, including use of high-resolution data, revealed clear evidence for contiguous but distinct regions: in general, the regions associated with the frontoparietal control system are situated between components of the dorsal attention and hippocampal-cortical memory systems. The frontoparietal control system is therefore anatomically positioned to integrate information from these two opposing brain systems.
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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

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                13 March 2020
                2020
                : 14
                : 201
                Affiliations
                [1] 1The Laboratory for Affect Cognition and Regulation (ACRLab), Faculty of Psychology, Southwest University , Chongqing, China
                [2] 2Institute of Brain and Psychological Sciences, Sichuan Normal University , Chengdu, China
                Author notes

                Edited by: Chao Liu, Beijing Normal University, China

                Reviewed by: Dandan Zhang, Shenzhen University, China; XianXin Meng, Nanyang Normal College, China

                *Correspondence: Jiemin Yang, yangjiemin85@ 123456126.com

                These authors have contributed equally to this work

                This article was submitted to Decision Neuroscience, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2020.00201
                7082334
                f71828d3-3a98-4f26-9937-2be4d815b164
                Copyright © 2020 Zhang, Chen, Deng, Yang and Yuan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 November 2019
                : 24 February 2020
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 112, Pages: 13, Words: 0
                Categories
                Neuroscience
                Original Research

                Neurosciences
                implicit emotion regulation,instructed fear,fmri,functional connectivity,amygdala
                Neurosciences
                implicit emotion regulation, instructed fear, fmri, functional connectivity, amygdala

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