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Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review

Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review
Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review

Failures in cortical control of fronto-striatal neural circuits may underpin impulsive and compulsive acts. In this narrative review, we explore these behaviors from the perspective of neural processes and consider how these behaviors and neural processes contribute to mental disorders such as obsessive-compulsive disorder (OCD), obsessive-compulsive personality disorder, and impulse-control disorders such as trichotillomania and pathological gambling. We present findings from a broad range of data, comprising translational and human endophenotypes research and clinical treatment trials, focussing on the parallel, functionally segregated, cortico-striatal neural projections, from orbitofrontal cortex (OFC) to medial striatum (caudate nucleus), proposed to drive compulsive activity, and from the anterior cingulate/ventromedial prefrontal cortex to the ventral striatum (nucleus accumbens shell), proposed to drive impulsive activity, and the interaction between them. We suggest that impulsivity and compulsivity each seem to be multidimensional. Impulsive or compulsive behaviors are mediated by overlapping as well as distinct neural substrates. Trichotillomania may stand apart as a disorder of motor-impulse control, whereas pathological gambling involves abnormal ventral reward circuitry that identifies it more closely with substance addiction. OCD shows motor impulsivity and compulsivity, probably mediated through disruption of OFC-caudate circuitry, as well as other frontal, cingulate, and parietal connections. Serotonin and dopamine interact across these circuits to modulate aspects of both impulsive and compulsive responding and as yet unidentified brain-based systems may also have important functions. Targeted application of neurocognitive tasks, receptor-specific neurochemical probes, and brain systems neuroimaging techniques have potential for future research in this field.

Compulsive, Dopamine, Endophenotypes, Impulsive, Serotonin
0893-133X
591-604
Fineberg, Naomi A.
157dcac1-9fb2-4197-81f3-0167e1224f05
Potenza, Marc N.
4331dcd8-d078-437b-a202-85b02faf9d56
Chamberlain, Samuel R.
8a0e09e6-f51f-4039-9287-88debe8d8b6f
Berlin, Heather A.
9d41653b-a2e1-4023-9c44-4563483bae38
Menzies, Lara
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Bechara, Antoine
3f109c95-cb74-41a3-9a4d-d6bed8aa890c
Sahakian, Barbara J.
e689cd5c-b84f-4503-86ca-7526cf340121
Robbins, Trevor W.
20dd57dd-dbf3-4aaa-b7ba-bb4387ffcbc7
Bullmore, Edward T.
73492180-4e3f-4673-acf8-ad42ccc4e904
Hollander, Eric
9c199e18-f117-4e49-ab07-8eb26b6eac0c
Fineberg, Naomi A.
157dcac1-9fb2-4197-81f3-0167e1224f05
Potenza, Marc N.
4331dcd8-d078-437b-a202-85b02faf9d56
Chamberlain, Samuel R.
8a0e09e6-f51f-4039-9287-88debe8d8b6f
Berlin, Heather A.
9d41653b-a2e1-4023-9c44-4563483bae38
Menzies, Lara
06e7a774-9230-4e28-8862-df8d35f1b624
Bechara, Antoine
3f109c95-cb74-41a3-9a4d-d6bed8aa890c
Sahakian, Barbara J.
e689cd5c-b84f-4503-86ca-7526cf340121
Robbins, Trevor W.
20dd57dd-dbf3-4aaa-b7ba-bb4387ffcbc7
Bullmore, Edward T.
73492180-4e3f-4673-acf8-ad42ccc4e904
Hollander, Eric
9c199e18-f117-4e49-ab07-8eb26b6eac0c

Fineberg, Naomi A., Potenza, Marc N., Chamberlain, Samuel R., Berlin, Heather A., Menzies, Lara, Bechara, Antoine, Sahakian, Barbara J., Robbins, Trevor W., Bullmore, Edward T. and Hollander, Eric (2010) Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology, 35 (3), 591-604. (doi:10.1038/npp.2009.185).

Record type: Review

Abstract

Failures in cortical control of fronto-striatal neural circuits may underpin impulsive and compulsive acts. In this narrative review, we explore these behaviors from the perspective of neural processes and consider how these behaviors and neural processes contribute to mental disorders such as obsessive-compulsive disorder (OCD), obsessive-compulsive personality disorder, and impulse-control disorders such as trichotillomania and pathological gambling. We present findings from a broad range of data, comprising translational and human endophenotypes research and clinical treatment trials, focussing on the parallel, functionally segregated, cortico-striatal neural projections, from orbitofrontal cortex (OFC) to medial striatum (caudate nucleus), proposed to drive compulsive activity, and from the anterior cingulate/ventromedial prefrontal cortex to the ventral striatum (nucleus accumbens shell), proposed to drive impulsive activity, and the interaction between them. We suggest that impulsivity and compulsivity each seem to be multidimensional. Impulsive or compulsive behaviors are mediated by overlapping as well as distinct neural substrates. Trichotillomania may stand apart as a disorder of motor-impulse control, whereas pathological gambling involves abnormal ventral reward circuitry that identifies it more closely with substance addiction. OCD shows motor impulsivity and compulsivity, probably mediated through disruption of OFC-caudate circuitry, as well as other frontal, cingulate, and parietal connections. Serotonin and dopamine interact across these circuits to modulate aspects of both impulsive and compulsive responding and as yet unidentified brain-based systems may also have important functions. Targeted application of neurocognitive tasks, receptor-specific neurochemical probes, and brain systems neuroimaging techniques have potential for future research in this field.

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More information

Accepted/In Press date: 17 November 2009
e-pub ahead of print date: 25 November 2010
Keywords: Compulsive, Dopamine, Endophenotypes, Impulsive, Serotonin

Identifiers

Local EPrints ID: 492893
URI: http://eprints.soton.ac.uk/id/eprint/492893
ISSN: 0893-133X
PURE UUID: cddef9be-b196-4889-b281-21cdfa2c21c1
ORCID for Samuel R. Chamberlain: ORCID iD orcid.org/0000-0001-7014-8121

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Date deposited: 19 Aug 2024 16:49
Last modified: 20 Aug 2024 01:59

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Contributors

Author: Naomi A. Fineberg
Author: Marc N. Potenza
Author: Samuel R. Chamberlain ORCID iD
Author: Heather A. Berlin
Author: Lara Menzies
Author: Antoine Bechara
Author: Barbara J. Sahakian
Author: Trevor W. Robbins
Author: Edward T. Bullmore
Author: Eric Hollander

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