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      Executive Impairment in Alcohol Use Disorder Reflects Structural Changes in Large-Scale Brain Networks: A Joint Independent Component Analysis on Gray-Matter and White-Matter Features

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          Abstract

          Alcohol Use Disorder (AUD) entails chronic effects on brain structure. Neurodegeneration due to alcohol toxicity is a neural signature of executive impairment typically observed in AUD, previously related to both gray-matter volume/density and white-matter abnormalities. Recent studies highlighted the role of meso-cortico-limbic structures supporting the salience and executive networks, in which the extent of neurostructural damage is significantly related to patients’ executive performance. Here we aim to integrate multimodal information on gray-matter and white-matter features with a multivariate data-driven approach (joint Independent Component Analysis, jICA), and to assess the relationship between the extent of damage in the resulting neurostructural superordinate components and executive profile in AUD. Twenty-two AUD patients and 18 matched healthy controls (HC) underwent a Magnetic Resonance Imaging (MRI) protocol, alongside clinical and neuropsychological examinations. We ran jICA on five neurostructural features, including gray-matter density and different diffusion tensor imaging metrics. We extracted 12 Independent Components (ICs) and compared the resulting mixing coefficients in patients vs. HC. Finally, we correlated significant ICs with executive and clinical variables. One out of 12 ICs (IC11) discriminated patients from healthy controls and correlated positively both with executive performance in all subjects, and with lifetime duration of alcohol abuse in patients. In line with previous related evidence, this component involved widespread gray-matter and white-matter patterns including key nodes and fiber tracts of salience, default-mode and central executive networks. These findings highlighted the role of multivariate data integration as a valuable approach revealing superordinate hallmarks of neural changes related to cognition in neurological and psychiatric populations.

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          Most cited references41

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          The somatic marker hypothesis: A neural theory of economic decision

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            Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain.

            During rest, multiple cortical brain regions are functionally linked forming resting-state networks. This high level of functional connectivity within resting-state networks suggests the existence of direct neuroanatomical connections between these functionally linked brain regions to facilitate the ongoing interregional neuronal communication. White matter tracts are the structural highways of our brain, enabling information to travel quickly from one brain region to another region. In this study, we examined both the functional and structural connections of the human brain in a group of 26 healthy subjects, combining 3 Tesla resting-state functional magnetic resonance imaging time-series with diffusion tensor imaging scans. Nine consistently found functionally linked resting-state networks were retrieved from the resting-state data. The diffusion tensor imaging scans were used to reconstruct the white matter pathways between the functionally linked brain areas of these resting-state networks. Our results show that well-known anatomical white matter tracts interconnect at least eight of the nine commonly found resting-state networks, including the default mode network, the core network, primary motor and visual network, and two lateralized parietal-frontal networks. Our results suggest that the functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain.
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              Addiction and the brain antireward system.

              A neurobiological model of the brain emotional systems has been proposed to explain the persistent changes in motivation that are associated with vulnerability to relapse in addiction, and this model may generalize to other psychopathology associated with dysregulated motivational systems. In this framework, addiction is conceptualized as a cycle of decreased function of brain reward systems and recruitment of antireward systems that progressively worsen, resulting in the compulsive use of drugs. Counteradaptive processes, such as opponent process, that are part of the normal homeostatic limitation of reward function fail to return within the normal homeostatic range and are hypothesized to repeatedly drive the allostatic state. Excessive drug taking thus results in not only the short-term amelioration of the reward deficit but also suppression of the antireward system. However, in the long term, there is worsening of the underlying neurochemical dysregulations that ultimately form an allostatic state (decreased dopamine and opioid peptide function, increased corticotropin-releasing factor activity). This allostatic state is hypothesized to be reflected in a chronic deviation of reward set point that is fueled not only by dysregulation of reward circuits per se but also by recruitment of brain and hormonal stress responses. Vulnerability to addiction may involve genetic comorbidity and developmental factors at the molecular, cellular, or neurocircuitry levels that sensitize the brain antireward systems.
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                Author and article information

                Contributors
                Journal
                Front Psychol
                Front Psychol
                Front. Psychol.
                Frontiers in Psychology
                Frontiers Media S.A.
                1664-1078
                26 November 2019
                2019
                : 10
                : 2479
                Affiliations
                [1] 1NEtS Center, Scuola Universitaria Superiore Istituto Universitario di Studi Superiori Pavia , Pavia, Italy
                [2] 2Cognitive Neuroscience Laboratory, Istituti Clinici Scientifici Maugeri IRCCS , Pavia, Italy
                [3] 3Psychology Unit, Istituti Clinici Scientifici Maugeri IRCCS , Pavia, Italy
                [4] 4University of Milano-Bicocca , Milan, Italy
                [5] 5Radiology Unit, Istituti Clinici Scientifici Maugeri IRCCS , Pavia, Italy
                Author notes

                Edited by: Pietro Cipresso, Italian Auxological Institute (IRCCS), Italy

                Reviewed by: Bernd Lachmann, University of Ulm, Germany; Gustavo Gonzalez-Cuevas, Idaho State University, United States

                *Correspondence: Chiara Crespi, chiara.crespi@ 123456iusspavia.it

                These authors have contributed equally to this work

                This article was submitted to Quantitative Psychology and Measurement, a section of the journal Frontiers in Psychology

                Article
                10.3389/fpsyg.2019.02479
                6988803
                32038340
                74a58d9f-792d-47af-a7e6-789cb033e315
                Copyright © 2019 Crespi, Galandra, Manera, Basso, Poggi and Canessa.

                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
                : 16 August 2019
                : 21 October 2019
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 62, Pages: 10, Words: 6944
                Categories
                Psychology
                Brief Research Report

                Clinical Psychology & Psychiatry
                alcohol use disorder,alcohol chronic consumption,voxel-based morphometry,diffusion tensor mri,joint independent component analysis,large-scale brain network,rehabilitative applications

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