Cargando…

The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder

BACKGROUND: Establishing the motivational influences on human action is essential for understanding choice and decision making in health and disease. Here we used tests of value-based decision making, manipulating both predicted and experienced reward values to assess the motivational control of goa...

Descripción completa

Detalles Bibliográficos
Autores principales: Perkes, Iain E., Morris, Richard W., Griffiths, Kristi R., Quail, Stephanie, Waters, Felicity, O’Brien, Margot, Hazell, Philip L., Balleine, Bernard W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10593889/
https://www.ncbi.nlm.nih.gov/pubmed/37881550
http://dx.doi.org/10.1016/j.bpsgos.2022.11.004
_version_ 1785124529926832128
author Perkes, Iain E.
Morris, Richard W.
Griffiths, Kristi R.
Quail, Stephanie
Waters, Felicity
O’Brien, Margot
Hazell, Philip L.
Balleine, Bernard W.
author_facet Perkes, Iain E.
Morris, Richard W.
Griffiths, Kristi R.
Quail, Stephanie
Waters, Felicity
O’Brien, Margot
Hazell, Philip L.
Balleine, Bernard W.
author_sort Perkes, Iain E.
collection PubMed
description BACKGROUND: Establishing the motivational influences on human action is essential for understanding choice and decision making in health and disease. Here we used tests of value-based decision making, manipulating both predicted and experienced reward values to assess the motivational control of goal-directed action in healthy adolescents and those with obsessive-compulsive disorder (OCD). METHODS: After instrumental training on a two action–two outcome probabilistic task, adolescents (n = 21) underwent Pavlovian conditioning using distinct stimuli predicting either the instrumental outcomes, a third outcome, or nothing. We then assessed functional magnetic resonance imaging during choice tests in which we varied the predicted value, using specific and general Pavlovian-instrumental transfer, and the experienced value, using outcome devaluation. To establish functional significance, we tested a matched cohort of adolescents with OCD (n = 20). RESULTS: In healthy adolescents, both predicted and experienced values influenced the performance of goal-directed actions, mediated by distinct orbitofrontal-striatal circuits involving the lateral orbitofrontal cortex (OFC) and medial OFC, respectively. However, in adolescents with OCD, choice was insensitive to changes in either predicted or experienced values. These impairments were related to hypoactivity in the lateral OFC and hyperactivity in the medial OFC during specific Pavlovian-instrumental transfer and hypoactivity in the anterior prefrontal cortex, caudate nucleus, and their connectivity in the devaluation test. CONCLUSIONS: We found that predicted and experienced values exerted a potent influence on the performance of goal-directed actions in adolescents via distinct orbitofrontal- and prefrontal-striatal circuits. Furthermore, the influence of these motivational processes was severely blunted in OCD, as was the functional segregation of circuits involving medial and lateral OFC, producing dysregulated action control.
format Online
Article
Text
id pubmed-10593889
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Elsevier
record_format MEDLINE/PubMed
spelling pubmed-105938892023-10-25 The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder Perkes, Iain E. Morris, Richard W. Griffiths, Kristi R. Quail, Stephanie Waters, Felicity O’Brien, Margot Hazell, Philip L. Balleine, Bernard W. Biol Psychiatry Glob Open Sci Archival Report BACKGROUND: Establishing the motivational influences on human action is essential for understanding choice and decision making in health and disease. Here we used tests of value-based decision making, manipulating both predicted and experienced reward values to assess the motivational control of goal-directed action in healthy adolescents and those with obsessive-compulsive disorder (OCD). METHODS: After instrumental training on a two action–two outcome probabilistic task, adolescents (n = 21) underwent Pavlovian conditioning using distinct stimuli predicting either the instrumental outcomes, a third outcome, or nothing. We then assessed functional magnetic resonance imaging during choice tests in which we varied the predicted value, using specific and general Pavlovian-instrumental transfer, and the experienced value, using outcome devaluation. To establish functional significance, we tested a matched cohort of adolescents with OCD (n = 20). RESULTS: In healthy adolescents, both predicted and experienced values influenced the performance of goal-directed actions, mediated by distinct orbitofrontal-striatal circuits involving the lateral orbitofrontal cortex (OFC) and medial OFC, respectively. However, in adolescents with OCD, choice was insensitive to changes in either predicted or experienced values. These impairments were related to hypoactivity in the lateral OFC and hyperactivity in the medial OFC during specific Pavlovian-instrumental transfer and hypoactivity in the anterior prefrontal cortex, caudate nucleus, and their connectivity in the devaluation test. CONCLUSIONS: We found that predicted and experienced values exerted a potent influence on the performance of goal-directed actions in adolescents via distinct orbitofrontal- and prefrontal-striatal circuits. Furthermore, the influence of these motivational processes was severely blunted in OCD, as was the functional segregation of circuits involving medial and lateral OFC, producing dysregulated action control. Elsevier 2022-12-05 /pmc/articles/PMC10593889/ /pubmed/37881550 http://dx.doi.org/10.1016/j.bpsgos.2022.11.004 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Archival Report
Perkes, Iain E.
Morris, Richard W.
Griffiths, Kristi R.
Quail, Stephanie
Waters, Felicity
O’Brien, Margot
Hazell, Philip L.
Balleine, Bernard W.
The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title_full The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title_fullStr The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title_full_unstemmed The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title_short The Motivational Determinants of Human Action, Their Neural Bases and Functional Impact in Adolescents With Obsessive-Compulsive Disorder
title_sort motivational determinants of human action, their neural bases and functional impact in adolescents with obsessive-compulsive disorder
topic Archival Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10593889/
https://www.ncbi.nlm.nih.gov/pubmed/37881550
http://dx.doi.org/10.1016/j.bpsgos.2022.11.004
work_keys_str_mv AT perkesiaine themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT morrisrichardw themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT griffithskristir themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT quailstephanie themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT watersfelicity themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT obrienmargot themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT hazellphilipl themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT balleinebernardw themotivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT perkesiaine motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT morrisrichardw motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT griffithskristir motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT quailstephanie motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT watersfelicity motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT obrienmargot motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT hazellphilipl motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder
AT balleinebernardw motivationaldeterminantsofhumanactiontheirneuralbasesandfunctionalimpactinadolescentswithobsessivecompulsivedisorder