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      Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients

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          Abstract

          Substance dependence is characterized by compulsive drug-taking despite negative consequences. Animal research suggests an underlying imbalance between goal-directed and habitual action control with chronic drug use. However, this imbalance, and its associated neurophysiological mechanisms, has not yet been experimentally investigated in human drug abusers. The aim of the present study therefore was to assess the balance between goal-directed and habit-based learning and its neural correlates in abstinent alcohol-dependent (AD) patients. A total of 31 AD patients and 19 age, gender and education matched healthy controls (HC) underwent functional magnetic resonance imaging (fMRI) during completion of an instrumental learning task designed to study the balance between goal-directed and habit learning. Task performance and task-related blood oxygen level-dependent activations in the brain were compared between AD patients and healthy matched controls. Findings were additionally associated with duration and severity of alcohol dependence. The results of this study provide evidence for an overreliance on stimulus-response habit learning in AD compared with HC, which was accompanied by decreased engagement of brain areas implicated in goal-directed action (ventromedial prefrontal cortex and anterior putamen) and increased recruitment of brain areas implicated in habit learning (posterior putamen) in AD patients. In conclusion, this is the first human study to provide experimental evidence for a disturbed balance between goal-directed and habitual control by use of an instrumental learning task, and to directly implicate cortical dysfunction to overreliance on inflexible habits in AD patients.

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          Most cited references45

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          The Inventory of Depressive Symptomatology (IDS): psychometric properties.

          The psychometric properties of the 28- and 30-item versions of the Inventory of Depressive Symptomatology, Clinician-Rated (IDS-C) and Self-Report (IDS-SR) are reported in a total of 434 (28-item) and 337 (30-item) adult out-patients with current major depressive disorder and 118 adult euthymic subjects (15 remitted depressed and 103 normal controls). Cronbach's alpha ranged from 0.92 to 0.94 for the total sample and from 0.76 to 0.82 for those with current depression. Item total correlations, as well as several tests of concurrent and discriminant validity are reported. Factor analysis revealed three dimensions (cognitive/mood, anxiety/arousal and vegetative) for each scale. Analysis of sensitivity to change in symptom severity in an open-label trial of fluoxetine (N = 58) showed that the IDS-C and IDS-SR were highly related to the 17-item Hamilton Rating Scale for Depression. Given the more complete item coverage, satisfactory psychometric properties, and high correlations with the above standard ratings, the 30-item IDS-C and IDS-SR can be used to evaluate depressive symptom severity. The availability of similar item content for clinician-rated and self-reported versions allows more direct evaluations of these two perspectives.
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            A unified statistical approach for determining significant signals in images of cerebral activation.

            We present a unified statistical theory for assessing the significance of apparent signal observed in noisy difference images. The results are usable in a wide range of applications, including fMRI, but are discussed with particular reference to PET images which represent changes in cerebral blood flow elicited by a specific cognitive or sensorimotor task. Our main result is an estimate of the P-value for local maxima of Gaussian, t, chi(2) and F fields over search regions of any shape or size in any number of dimensions. This unifies the P-values for large search areas in 2-D (Friston et al. [1991]: J Cereb Blood Flow Metab 11:690-699) large search regions in 3-D (Worsley et al. [1992]: J Cereb Blood Flow Metab 12:900-918) and the usual uncorrected P-value at a single pixel or voxel. Copyright (c) 1996 Wiley-Liss, Inc.
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              Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum.

              Clinical manifestations in diseases affecting the dopamine system include deficits in emotional, cognitive, and motor function. Although the parallel organization of specific corticostriatal pathways is well documented, mechanisms by which dopamine might integrate information across different cortical/basal ganglia circuits are less well understood. We analyzed a collection of retrograde and anterograde tracing studies to understand how the striatonigrostriatal (SNS) subcircuit directs information flow between ventromedial (limbic), central (associative), and dorsolateral (motor) striatal regions. When viewed as a whole, the ventromedial striatum projects to a wide range of the dopamine cells and receives a relatively small dopamine input. In contrast, the dorsolateral striatum (DLS) receives input from a broad expanse of dopamine cells and has a confined input to the substantia nigra (SN). The central striatum (CS) receives input from and projects to a relatively wide range of the SN. The SNS projection from each striatal region contains three substantia nigra components: a dorsal group of nigrostriatal projecting cells, a central region containing both nigrostriatal projecting cells and its reciprocal striatonigral terminal fields, and a ventral region that receives a specific striatonigral projection but does not contain its reciprocal nigrostriatal projection. Examination of results from multiple tracing experiments simultaneously demonstrates an interface between different striatal regions via the midbrain dopamine cells that forms an ascending spiral between regions. The shell influences the core, the core influences the central striatum, and the central striatum influences the dorsolateral striatum. This anatomical arrangement creates a hierarchy of information flow and provides an anatomical basis for the limbic/cognitive/motor interface via the ventral midbrain.
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                Author and article information

                Journal
                Transl Psychiatry
                Transl Psychiatry
                Translational Psychiatry
                Nature Publishing Group
                2158-3188
                December 2013
                17 December 2013
                1 December 2013
                : 3
                : 12
                : e337
                Affiliations
                [1 ]Department of Psychiatry, Neuroscience Campus Amsterdam, VU University Medical Center , Amsterdam, The Netherlands
                [2 ]Department of Psychiatry, Academic Medical Center, University of Amsterdam , Amsterdam, The Netherlands
                [3 ]Department of Clinical Psychology, University of Amsterdam , Amsterdam, The Netherlands
                [4 ]Cognitive Science Center Amsterdam, University of Amsterdam , Amsterdam, The Netherlands
                [5 ]Department of Experimental Psychology and Behavioural and Clinical Neuroscience Institute, University of Cambridge , Cambridge, UK
                [6 ]Department of Psychiatry, Leiden University Medical Center , Leiden, The Netherlands
                [7 ]Department of Psychiatry, University Medical Center of Groningen , Groningen, The Netherlands
                Author notes
                [* ]Max Planck Institute for Human Cognitive and Brain Sciences, Fellow-Group Cognitive and Affective Control of Behavioral Adaptation, Neurology, room C211 , Stephanstrasse 1A, 04103 Leipzig, Germany. E-mail: sjoerds.zs@ 123456gmail.com
                Article
                tp2013107
                10.1038/tp.2013.107
                4030326
                24346135
                7d53653a-00b7-47c6-8ce5-8b3f29627d2d
                Copyright © 2013 Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/

                History
                : 05 July 2013
                : 19 September 2013
                : 09 October 2013
                Categories
                Original Article

                Clinical Psychology & Psychiatry
                addiction,fmri,goal-directed behavior,habit formation,instrumental learning,striatum

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