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      Impact of exercise on older adults’ mood is moderated by sleep and mediated by altered brain connectivity

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          Abstract

          Older adults comprise the fastest growing global demographic and are at increased risk of poor mental health outcomes. Although aerobic exercise and sleep are critical to the preservation of emotional well-being, few studies have examined their combined mood-enhancing effects, or the potential neural mechanisms underlying these effects. Here, we used a randomized crossover design to test the impact of acute exercise on mood and the intrinsic functional connectivity (iFC) of the cingulo-opercular network in physically healthy older adults. Wrist actigraphy provided objective indices of sleep. Results revealed that 30 min of moderate-intensity aerobic exercise acutely enhanced positive affect (PA) and reduced iFC between the cingulo-opercular network and the hippocampus. Both effects were magnified among older adults with greater sleep disturbance. Exercise-induced changes in hippocampal iFC mediated relations between sleep disturbance and exercise-induced increases in PA. These findings provide evidence that aerobic exercise enhances mood, that it does so by altering connectivity between the anterior insula—a key hub in the cingulo-opercular network—and the hippocampus and that lower sleep quality is a stronger predictor of these effects among older adults. These observations underscore the benefits of moderate-intensity exercise—a safe and scalable behavioral intervention—and provide new clues about the neural circuitry underlying the interactive effects of sleep and exercise on mood.

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          The assessment and analysis of handedness: The Edinburgh inventory

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            FreeSurfer.

            FreeSurfer is a suite of tools for the analysis of neuroimaging data that provides an array of algorithms to quantify the functional, connectional and structural properties of the human brain. It has evolved from a package primarily aimed at generating surface representations of the cerebral cortex into one that automatically creates models of most macroscopically visible structures in the human brain given any reasonable T1-weighted input image. It is freely available, runs on a wide variety of hardware and software platforms, and is open source. Copyright © 2012 Elsevier Inc. All rights reserved.
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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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                Author and article information

                Contributors
                Journal
                Soc Cogn Affect Neurosci
                Soc Cogn Affect Neurosci
                scan
                Social Cognitive and Affective Neuroscience
                Oxford University Press (UK )
                1749-5016
                1749-5024
                November 2020
                17 November 2020
                17 November 2020
                : 15
                : 11
                : 1238-1251
                Affiliations
                departmentDepartment of Mental Health, Johns Hopkins Bloomberg School of Public Health , Baltimore, MD 21205, USA
                departmentDepartment of Kinesiology, University of Maryland School of Public Health , College Park, MD 20742, USA
                departmentDepartment of Kinesiology, University of Maryland School of Public Health , College Park, MD 20742, USA
                departmentNeuroscience and Cognitive Science Program, University of Maryland , College Park, MD 20742, USA
                departmentDepartment of Mental Health, Johns Hopkins Bloomberg School of Public Health , Baltimore, MD 21205, USA
                departmentNeuroscience and Cognitive Science Program, University of Maryland , College Park, MD 20742, USA
                departmentDepartment of Psychology, University of Maryland , College Park, MD, USA
                departmentDepartment of Mental Health, Johns Hopkins Bloomberg School of Public Health , Baltimore, MD 21205, USA
                departmentDepartment of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine , Baltimore, MD 21205, USA
                departmentCenter on Aging and Health, Johns Hopkins School of Medicine and Bloomberg School of Public Health , Baltimore, MD 21205, USA
                departmentDepartment of Kinesiology, University of Maryland School of Public Health , College Park, MD 20742, USA
                departmentNeuroscience and Cognitive Science Program, University of Maryland , College Park, MD 20742, USA
                Author notes
                Correspondence should be addressed to Alfonso J. Alfini, PhD, Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, 624 North Broadway, Hampton House, Room 806, Baltimore, MD 21205, USA. E-mail: aalfini1@ 123456jhu.edu
                Author information
                http://orcid.org/0000-0002-8743-8923
                Article
                nsaa149
                10.1093/scan/nsaa149
                7745152
                33201227
                1102b585-9eeb-427a-92e2-aa5f7598cb6f
                © The Author(s) 2020. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 03 July 2020
                : 25 September 2020
                : 27 October 2020
                : 12 October 2020
                Page count
                Pages: 14
                Funding
                Funded by: National Institute on Aging, DOI 10.13039/100000049;
                Award ID: AG027668
                Categories
                Original Manuscript
                AcademicSubjects/SCI01880

                Neurosciences
                sleep actigraphy,acute exercise,affect,cingulo-opercular network
                Neurosciences
                sleep actigraphy, acute exercise, affect, cingulo-opercular network

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