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Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits

Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits
Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits
Individual differences in impulsivity and compulsivity is thought to underlie vulnerability to a broad range of disorders and are closely tied to cortical-striatal-thalamic-cortical function. However, whether impulsivity and compulsivity in clinical disorders is continuous with the healthy population and explains cortical-striatal-thalamic-cortical dysfunction across different disorders remains unclear. Here, we characterized the relationship between cortical-striatal-thalamic-cortical effective connectivity, estimated using dynamic causal modelling of resting-state functional magnetic resonance imaging data, and dimensional phenotypes of impulsivity and compulsivity in two symptomatically distinct but phenotypically related disorders, obsessive-compulsive disorder and gambling disorder. 487 online participants provided data for modelling of dimensional phenotypes. These data were combined with 34 obsessive-compulsive disorder patients, 22 gambling disorder patients, and 39 healthy controls, who underwent functional magnetic resonance imaging. Three core dimensions were identified: disinhibition, impulsivity, and compulsivity. Patients’ scores on these dimensions were continuously distributed with the healthy participants, supporting a continuum model of psychopathology. Across all participants, higher disinhibition correlated with lower bottom-up connectivity in the dorsal circuit and greater bottom-up connectivity in the ventral circuit, and higher compulsivity correlated with lower bottom-up connectivity in the dorsal circuit. In patients, higher clinical severity was also linked to lower bottom-up connectivity in the dorsal circuit, but these findings were independent of phenotypic variation, demonstrating convergence towards behaviourally and clinically relevant changes in brain dynamics. Effective connectivity did not differ as a function of traditional diagnostic labels and only weak associations were observed for functional connectivity measures. Together, our results demonstrate that cortical-striatal-thalamic-cortical dysfunction across obsessive-compulsive disorder and gambling disorder may be better characterized by dimensional phenotypes than diagnostic comparisons, supporting investigation of quantitative liability phenotypes.
Compulsivity, DCM, Disinhibition, GD, Impulsivity, OCD
1053-8119
Parkes, Linden
45488113-b369-4d22-a78f-6802d297e8f3
Tiego, Jeggan
1172a044-daf1-4f04-af76-c3361d2da9c7
Aquino, K.
97abbd72-b916-4fba-b176-6b9a2ab0ee7d
Braganza, Leah
559e91c0-90d9-4f9c-8b7e-a53dd70b9cc3
Chamberlain, Samuel R.
8a0e09e6-f51f-4039-9287-88debe8d8b6f
Fontenelle, Leonardo F.
859206be-2b11-438a-9b18-d22579111a6b
Harrison, B. J.
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Lorenzetti, Valentina
2c3fbe9f-84e2-4d23-9095-1c58efbc4614
Paton, B.
78df291a-f356-4da5-b934-2a4147d2a82a
Razi, A.
f46533a2-9661-434c-82b7-a0b03d3d9370
Monash University and Alfred Hospital, Institute for Brain and Mental Health
Parkes, Linden
45488113-b369-4d22-a78f-6802d297e8f3
Tiego, Jeggan
1172a044-daf1-4f04-af76-c3361d2da9c7
Aquino, K.
97abbd72-b916-4fba-b176-6b9a2ab0ee7d
Braganza, Leah
559e91c0-90d9-4f9c-8b7e-a53dd70b9cc3
Chamberlain, Samuel R.
8a0e09e6-f51f-4039-9287-88debe8d8b6f
Fontenelle, Leonardo F.
859206be-2b11-438a-9b18-d22579111a6b
Harrison, B. J.
4a57d06f-c771-44ec-9d89-0b6863bd6734
Lorenzetti, Valentina
2c3fbe9f-84e2-4d23-9095-1c58efbc4614
Paton, B.
78df291a-f356-4da5-b934-2a4147d2a82a
Razi, A.
f46533a2-9661-434c-82b7-a0b03d3d9370

Chamberlain, Samuel R. , Monash University and Alfred Hospital, Institute for Brain and Mental Health (2019) Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits. NeuroImage, 202 (11), [116070]. (doi:10.1016/j.neuroimage.2019.116070).

Record type: Article

Abstract

Individual differences in impulsivity and compulsivity is thought to underlie vulnerability to a broad range of disorders and are closely tied to cortical-striatal-thalamic-cortical function. However, whether impulsivity and compulsivity in clinical disorders is continuous with the healthy population and explains cortical-striatal-thalamic-cortical dysfunction across different disorders remains unclear. Here, we characterized the relationship between cortical-striatal-thalamic-cortical effective connectivity, estimated using dynamic causal modelling of resting-state functional magnetic resonance imaging data, and dimensional phenotypes of impulsivity and compulsivity in two symptomatically distinct but phenotypically related disorders, obsessive-compulsive disorder and gambling disorder. 487 online participants provided data for modelling of dimensional phenotypes. These data were combined with 34 obsessive-compulsive disorder patients, 22 gambling disorder patients, and 39 healthy controls, who underwent functional magnetic resonance imaging. Three core dimensions were identified: disinhibition, impulsivity, and compulsivity. Patients’ scores on these dimensions were continuously distributed with the healthy participants, supporting a continuum model of psychopathology. Across all participants, higher disinhibition correlated with lower bottom-up connectivity in the dorsal circuit and greater bottom-up connectivity in the ventral circuit, and higher compulsivity correlated with lower bottom-up connectivity in the dorsal circuit. In patients, higher clinical severity was also linked to lower bottom-up connectivity in the dorsal circuit, but these findings were independent of phenotypic variation, demonstrating convergence towards behaviourally and clinically relevant changes in brain dynamics. Effective connectivity did not differ as a function of traditional diagnostic labels and only weak associations were observed for functional connectivity measures. Together, our results demonstrate that cortical-striatal-thalamic-cortical dysfunction across obsessive-compulsive disorder and gambling disorder may be better characterized by dimensional phenotypes than diagnostic comparisons, supporting investigation of quantitative liability phenotypes.

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More information

Accepted/In Press date: 2 August 2019
Published date: 15 November 2019
Additional Information: Publisher Copyright: © 2019 Elsevier Inc.
Keywords: Compulsivity, DCM, Disinhibition, GD, Impulsivity, OCD

Identifiers

Local EPrints ID: 492429
URI: http://eprints.soton.ac.uk/id/eprint/492429
ISSN: 1053-8119
PURE UUID: f67f48e5-80a5-4a9e-a5d5-f0bade6d8511
ORCID for Samuel R. Chamberlain: ORCID iD orcid.org/0000-0001-7014-8121

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Date deposited: 26 Jul 2024 16:38
Last modified: 27 Jul 2024 02:00

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Contributors

Author: Linden Parkes
Author: Jeggan Tiego
Author: K. Aquino
Author: Leah Braganza
Author: Samuel R. Chamberlain ORCID iD
Author: Leonardo F. Fontenelle
Author: B. J. Harrison
Author: Valentina Lorenzetti
Author: B. Paton
Author: A. Razi
Corporate Author: Monash University and Alfred Hospital, Institute for Brain and Mental Health

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