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      Executive functioning, ADHD symptoms and resting state functional connectivity in children with perinatal stroke

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          Abstract

          Perinatal stroke describes a group of focal, vascular brain injuries that occur early in development, often resulting in lifelong disability. Two types of perinatal stroke predominate, arterial ischemic stroke (AIS) and periventricular venous infarction (PVI). Though perinatal stroke is typically considered a motor disorder, other comorbidities commonly exist including attention-deficit hyperactivity disorder (ADHD) and deficits in executive function. Rates of ADHD symptoms are higher in children with perinatal stroke and deficits in executive function may also occur but underlying mechanisms are not known. We measured resting state functional connectivity in children with perinatal stroke using previously established dorsal attention, frontoparietal, and default mode network seeds. Associations with parental ratings of executive function and ADHD symptoms were examined. A total of 120 participants aged 6–19 years [AIS N = 31; PVI N = 30; Controls N = 59] were recruited. In comparison to typically developing peers, both the AIS and PVI groups showed lower intra- and inter-hemispheric functional connectivity values in the networks investigated. Group differences in between-network connectivity were also demonstrated, showing weaker anticorrelations between task-positive (frontoparietal and dorsal attention) and task-negative (default mode) networks in stroke groups compared to controls. Both within-network and between-network functional connectivity values were highly associated with parental reports of executive function and ADHD symptoms. These results suggest that differences in functional connectivity exist both within and between networks after perinatal stroke, the degree of which is associated with ADHD symptoms and executive function.

          Supplementary Information

          The online version contains supplementary material available at 10.1007/s11682-023-00827-w.

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          Most cited references77

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            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.
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              A default mode of brain function.

              A baseline or control state is fundamental to the understanding of most complex systems. Defining a baseline state in the human brain, arguably our most complex system, poses a particular challenge. Many suspect that left unconstrained, its activity will vary unpredictably. Despite this prediction we identify a baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF. The OEF is defined as the ratio of oxygen used by the brain to oxygen delivered by flowing blood and is remarkably uniform in the awake but resting state (e.g., lying quietly with eyes closed). Local deviations in the OEF represent the physiological basis of signals of changes in neuronal activity obtained with functional MRI during a wide variety of human behaviors. We used quantitative metabolic and circulatory measurements from positron-emission tomography to obtain the OEF regionally throughout the brain. Areas of activation were conspicuous by their absence. All significant deviations from the mean hemisphere OEF were increases, signifying deactivations, and resided almost exclusively in the visual system. Defining the baseline state of an area in this manner attaches meaning to a group of areas that consistently exhibit decreases from this baseline, during a wide variety of goal-directed behaviors monitored with positron-emission tomography and functional MRI. These decreases suggest the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
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                Author and article information

                Contributors
                helen.carlson@ahs.ca
                Journal
                Brain Imaging Behav
                Brain Imaging Behav
                Brain Imaging and Behavior
                Springer US (New York )
                1931-7557
                1931-7565
                1 December 2023
                1 December 2023
                2024
                : 18
                : 2
                : 263-278
                Affiliations
                [1 ]Calgary Pediatric Stroke Program, Alberta Children’s Hospital, ( https://ror.org/00sx29x36) 28 Oki Drive NW, Calgary, AB Canada
                [2 ]Alberta Children’s Hospital Research Institute, ( https://ror.org/00gmyvv50) 28 Oki Drive NW, Calgary, AB Canada
                [3 ]Department of Pediatrics, Cumming School of Medicine, University of Calgary, ( https://ror.org/03yjb2x39) Calgary, AB Canada
                [4 ]Hotchkiss Brain Institute, University of Calgary, ( https://ror.org/03yjb2x39) Calgary, AB Canada
                [5 ]Department of Clinical Neurosciences, University of Calgary, ( https://ror.org/03yjb2x39) Calgary, AB Canada
                [6 ]Neurosciences Program, Alberta Children’s Hospital, ( https://ror.org/00sx29x36) Calgary, AB Canada
                [7 ]Department of Psychology, University of Calgary, ( https://ror.org/03yjb2x39) Calgary, AB Canada
                [8 ]Department of Pediatrics, University of Alberta, ( https://ror.org/0160cpw27) Edmonton, AB Canada
                [9 ]Department of Pediatrics, University of Toronto, ( https://ror.org/03dbr7087) Toronto, ON Canada
                [10 ]Children’s Stroke Program, Division of Neurology, Hospital for Sick Children, ( https://ror.org/057q4rt57) Toronto, ON Canada
                [11 ]Department of Radiology, University of Calgary, ( https://ror.org/03yjb2x39) Calgary, AB Canada
                Author information
                http://orcid.org/0000-0002-5788-0542
                Article
                827
                10.1007/s11682-023-00827-w
                11156742
                38038867
                420877f1-8dbc-4c0f-ae9b-bae5f6794fb0
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 19 November 2023
                Categories
                Research
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                © Springer Science+Business Media, LLC, part of Springer Nature 2024

                Radiology & Imaging
                perinatal stroke,functional connectivity,adhd,executive function,cognition,default mode network

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