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The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood

BACKGROUND: The majority of reward learning neuroimaging studies have not focused on the motivational aspects of behavior, such as the inherent value placed on choice itself. The experience and affective value of personal control may have particular relevance for psychiatric disorders, including dep...

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Autores principales: Romaniuk, Liana, Sandu, Anca-Larisa, Waiter, Gordon D., McNeil, Christopher J., Xueyi, Shen, Harris, Matthew A., Macfarlane, Jennifer A., Lawrie, Stephen M., Deary, Ian J., Murray, Alison D., Delgado, Mauricio R., Steele, J. Douglas, McIntosh, Andrew M., Whalley, Heather C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier, Inc 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6374985/
https://www.ncbi.nlm.nih.gov/pubmed/30470583
http://dx.doi.org/10.1016/j.bpsc.2018.09.015
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author Romaniuk, Liana
Sandu, Anca-Larisa
Waiter, Gordon D.
McNeil, Christopher J.
Xueyi, Shen
Harris, Matthew A.
Macfarlane, Jennifer A.
Lawrie, Stephen M.
Deary, Ian J.
Murray, Alison D.
Delgado, Mauricio R.
Steele, J. Douglas
McIntosh, Andrew M.
Whalley, Heather C.
author_facet Romaniuk, Liana
Sandu, Anca-Larisa
Waiter, Gordon D.
McNeil, Christopher J.
Xueyi, Shen
Harris, Matthew A.
Macfarlane, Jennifer A.
Lawrie, Stephen M.
Deary, Ian J.
Murray, Alison D.
Delgado, Mauricio R.
Steele, J. Douglas
McIntosh, Andrew M.
Whalley, Heather C.
author_sort Romaniuk, Liana
collection PubMed
description BACKGROUND: The majority of reward learning neuroimaging studies have not focused on the motivational aspects of behavior, such as the inherent value placed on choice itself. The experience and affective value of personal control may have particular relevance for psychiatric disorders, including depression. METHODS: We adapted a functional magnetic resonance imaging reward task that probed the value placed on exerting control over one’s decisions, termed choice value, in 122 healthy participants. We examined activation associated with choice value; personally chosen versus passively received rewards; and reinforcement learning metrics, such as prediction error. Relationships were tested between measures of motivational orientation (categorized as autonomy, control, and impersonal) and subclinical depressive symptoms. RESULTS: Anticipating personal choice activated left insula, cingulate, right inferior frontal cortex, and ventral striatum (p(familywise error–corrected) < .05). Ventral striatal activations to choice were diminished in participants with subclinical depressive symptoms. Personally chosen rewards were associated with greater activation of the insula and inferior frontal gyrus, cingulate cortex, hippocampus, thalamus, and substantia nigra compared with rewards that were passively received. In participants who felt they had little control over their own behavior (impersonal orientation), prediction error signals in nucleus accumbens were stronger during passive trials. CONCLUSIONS: Previous findings regarding personal choice have been verified and advanced through the use of both reinforcement learning models and correlations with psychopathology. Personal choice has an impact on the extended reward network, potentially allowing these clinically important areas to be addressed in ways more relevant to personality styles, self-esteem, and symptoms such as motivational anhedonia.
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spelling pubmed-63749852019-02-26 The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood Romaniuk, Liana Sandu, Anca-Larisa Waiter, Gordon D. McNeil, Christopher J. Xueyi, Shen Harris, Matthew A. Macfarlane, Jennifer A. Lawrie, Stephen M. Deary, Ian J. Murray, Alison D. Delgado, Mauricio R. Steele, J. Douglas McIntosh, Andrew M. Whalley, Heather C. Biol Psychiatry Cogn Neurosci Neuroimaging Article BACKGROUND: The majority of reward learning neuroimaging studies have not focused on the motivational aspects of behavior, such as the inherent value placed on choice itself. The experience and affective value of personal control may have particular relevance for psychiatric disorders, including depression. METHODS: We adapted a functional magnetic resonance imaging reward task that probed the value placed on exerting control over one’s decisions, termed choice value, in 122 healthy participants. We examined activation associated with choice value; personally chosen versus passively received rewards; and reinforcement learning metrics, such as prediction error. Relationships were tested between measures of motivational orientation (categorized as autonomy, control, and impersonal) and subclinical depressive symptoms. RESULTS: Anticipating personal choice activated left insula, cingulate, right inferior frontal cortex, and ventral striatum (p(familywise error–corrected) < .05). Ventral striatal activations to choice were diminished in participants with subclinical depressive symptoms. Personally chosen rewards were associated with greater activation of the insula and inferior frontal gyrus, cingulate cortex, hippocampus, thalamus, and substantia nigra compared with rewards that were passively received. In participants who felt they had little control over their own behavior (impersonal orientation), prediction error signals in nucleus accumbens were stronger during passive trials. CONCLUSIONS: Previous findings regarding personal choice have been verified and advanced through the use of both reinforcement learning models and correlations with psychopathology. Personal choice has an impact on the extended reward network, potentially allowing these clinically important areas to be addressed in ways more relevant to personality styles, self-esteem, and symptoms such as motivational anhedonia. Elsevier, Inc 2019-02 /pmc/articles/PMC6374985/ /pubmed/30470583 http://dx.doi.org/10.1016/j.bpsc.2018.09.015 Text en © 2018 Society of Biological Psychiatry. Elsevier Inc. All rights reserved. http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Romaniuk, Liana
Sandu, Anca-Larisa
Waiter, Gordon D.
McNeil, Christopher J.
Xueyi, Shen
Harris, Matthew A.
Macfarlane, Jennifer A.
Lawrie, Stephen M.
Deary, Ian J.
Murray, Alison D.
Delgado, Mauricio R.
Steele, J. Douglas
McIntosh, Andrew M.
Whalley, Heather C.
The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title_full The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title_fullStr The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title_full_unstemmed The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title_short The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood
title_sort neurobiology of personal control during reward learning and its relationship to mood
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6374985/
https://www.ncbi.nlm.nih.gov/pubmed/30470583
http://dx.doi.org/10.1016/j.bpsc.2018.09.015
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