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From compulsivity to compulsion: the neural basis of compulsive disorders

Nature Reviews Neuroscience volume 25, pages 313–333 (2024)Cite this article

Abstract

Compulsive behaviour, an apparently irrational perseveration in often maladaptive acts, is a potential transdiagnostic symptom of several neuropsychiatric disorders, including obsessive-compulsive disorder and addiction, and may reflect the severe manifestation of a dimensional trait termed compulsivity. In this Review, we examine the psychological basis of compulsions and compulsivity and their underlying neural circuitry using evidence from human neuroimaging and animal models. Several main elements of this circuitry are identified, focused on fronto-striatal systems implicated in goal-directed behaviour and habits. These systems include the orbitofrontal, prefrontal, anterior cingulate and insular cortices and their connections with the basal ganglia as well as sensoriomotor and parietal cortices and cerebellum. We also consider the implications for future classification of impulsive–compulsive disorders and their treatment.

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Fig. 1: Behavioural models of perseverative and compulsive behaviour.
Fig. 2: Neural systems of compulsive behaviour: insights from cognitive neuroscience.
Fig. 3: Human neuroimaging and compulsion.
Fig. 4: Neural circuits of compulsive behaviour: insights from animal models.
Fig. 5: The anatomy of a compulsive action: a theoretical model of the psychological underpinnings of compulsive disorders.

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Acknowledgements

D.B. is supported by a UKRI grant (MR/W019647/1). P.B. is supported by a Sir Henry Postdoctoral Research Fellowship (Grant 204727/Z/16/Z). The authors thank B. Everitt for his insightful comments on the final draft of the manuscript.

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Authors and Affiliations

  1. Behavioural and Clinical Neuroscience Institute, Department of Psychology, University of Cambridge, Cambridge, UK

    Trevor W. Robbins, Paula Banca & David Belin

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  1. Trevor W. Robbins
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  2. Paula Banca
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The authors contributed equally to all aspects of the article.

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Correspondence to Trevor W. Robbins.

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T.W.R. declares consultancies with Cambridge Cognition and Supernus and a research grant from Shionogi. The other authors declare no competing interests.

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Nature Reviews Neuroscience thanks Casey Helpern, who co-reviewed with Wonkyung Choi; Christopher Pittenger; and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Arbitration

A resolution of conflict between alternative strategies.

Attractor network

A computational term referring to a network of neuronal nodes, often recurrently connected, whose dynamic relations over time settle into a stable pattern of activity.

Brodmann areas

Regions of the brain defined in terms of histological characteristics and denoted by numbers, such as BA 9.

Checking

Repeated monitoring of behaviour caused in part by uncertainty.

Chemogenetics

A method of manipulating neuronal activity in specific circuits using otherwise inert drugs that activate engineered receptors expressed in identified (genetically or otherwise) cells.

Cingulo-opercular networks

A neural system that includes the cingulate cortex, inferior prefrontal cortex and insula that is implicated in executive functions and thought to be a major mediator of urgency affecting action.

Cognitive-behavioural therapy

A general set of psychological treatments in which patients are instructed to adhere to certain cognitive strategies to combat their mental symptoms. In OCD, often combined with a special technique of ‘response prevention’.

Cognitive control

A set of executive operations that optimize behaviour mediated in part by frontal lobe circuitry; almost synonymous with executive control.

Compulsions

Strong feelings of wanting or having to do something repeatedly that are difficult to control.

Compulsivity

A trait that refers to a tendency towards repetitive behaviour.

Conditioned reinforcers

Conditioned stimuli (associated with a primary reward) that reinforce those actions by which they are produced.

Contingency degradation

An experimental manipulation that uncouples the predictive relationship or correlation between an instrumental action and its outcome or consequence. Persistent instrumental responding then indicates mediation by habitual (stimulus–response) tendencies.

Coping

A response, whether behavioural, cognitive or neuroendocrine, associated with reducing stress via negative reinforcement.

Craving

An overwhelming desire for a drug, frequently expressed by individuals with substance use disorder as ‘I want’.

Deep brain stimulation

A form of invasive neuromodulation by implanted electrodes increasingly used in some mental health disorders, including OCD and addiction, as well as its original application to Parkinson disease.

Dorsal striatum

That part of the basal ganglia of the brain that comprises the dorsal caudate nucleus and dorsal putamen in primates and their homologues in rodents.

Dorsolateral striatum

That region of the striatum in rodents generally assumed to be homologous with part of the primate putamen and, alongside the infralimbic cortex, central nucleus of the amygdala and pre/motor cortex, part of the so-called habit system.

Dorsomedial striatum

That region of the striatum in rodents generally assumed to be homologous with part of the primate caudate nucleus and, alongside the prelimbic cortex and the basolateral amygdala, part of the so-called goal-directed system.

Excitotoxic lesions

Cell-body-specific lesions of brain regions, produced by glutamatergic agonist drugs that spare nerve fibres of passage (connections).

Executive function

A set of cognitive operations, including working memory, attention, inhibitory control, cognitive flexibility and monitoring, that optimize behaviour. Largely synonymous with cognitive control.

Fronto-parietal networks

A neural system, especially including the lateral prefrontal cortex and its connections with the parietal cortex, thought to be a major component of the executive control system.

Glutamate-to-GABA balance

Hypothetical relationship between excitatory (glutamate) and local inhibitory (GABA) neurons in the cerebral cortex.

Goal devaluation

An experimental manipulation that reduces the value of a goal or an outcome produced by instrumental behaviour (such as reducing food value by satiation or poisoning). Persistent instrumental responding assessed under extinction conditions then indicates performance mediation by habitual (stimulus–response) tendencies.

Goal-directed behaviour

A sequence of purposeful, motivated instrumental actions whose initiation is predicated on a clear conscious representation of a goal.

Grey matter volume

The volume of nerve cells established by voxel-based morphometric methods in neuroimaging.

Habits

Instrumental responses generally elicited by internal or external environmental stimuli in the absence of any previous conscious representation of the primary goal.

Homologue

Neuroanatomical structure of common developmental and evolutionary history over species.

Impulsivity

A trait that refers to a tendency to premature, risky behaviour.

Incentive habit

A habit in which a response has acquired inherent motivational value (and hence can be a goal on its own) through its development under the pavlovian incentive influence of conditioned reinforcers (either exteroceptive or interoceptive) that enable the incentive value of pavlovian cues to transfer to the setting-bound (stimulus–response) response itself.

Incentive motivation

Invigoration of instrumental responding either by conditioned stimuli (pavlovian–instrumental transfer) or by incremental changes in value of the primary goal.

Negative urgency

An aversive motivational state associated with urges to respond.

Obsessions

Persistent intrusive lines of thought, often aversive.

Optogenetic

A method of manipulating neuronal activity in specific circuits using the photostimulation of a light-sensitive channel ectopically expressed in genetically or otherwise identified cells.

Ordering

Imposing organization on a scene or objects.

Positron emission tomography

Neuroimaging technique using radioactive tracers to detect specific chemicals (often receptors) and metabolic or chemical changes in brain.

Repetitive transcranial magnetic stimulation

A form of non-invasive neuromodulation using magnetic stimulation applied to the scalp.

Resting state functional connectivity

A particular form of functional MRI using inactive participants performing no task. Correlations of resultant fluctuations of the oxygenated haemoglobin response are made across functionally coherent brain regions to produce a proxy measure of connectivity. Hypoconnectivity, diminished blood-oxygen-level-dependent responses; hyperconnectivity, enhanced blood-oxygen-level-dependent responses.

Schedule-induced polydipsia

Excessive drinking caused by intermittent, but predictable, delivery of small food rewards, generally in food-deprived rodents.

Serotonin selective reuptake inhibitor

A class of drugs used for the treatment of depression and OCD that selectively inhibit serotonin reuptake and bind directly to the BDNF trkB receptor.

Striosomal

Refers to one of the two complementary neurochemically defined compartments within the striatum visualized by staining for immunocytochemical markers (that receives limbic inputs).

Symptom provocation

Attempt to generate the symptoms of a patient by specific environmental challenge or by presenting a stimulus associated with those symptoms (for example, by visual imagery or touch).

Trait

A behavioural disposition, generally assumed to be of genetic origin.

Trichotillomania

The continual pulling out of one’s own hair, often resulting in baldness.

Urge

An urgent feeling (often called an impulse) that a behaviour must be performed imminently.

Ventral striatum

That part of the basal ganglia of the brain comprising the nucleus accumbens (including both its core and shell sub-regions), the olfactory tubercle and sometimes (in primates) the ventral caudate and ventral putamen. The region is often defined in terms of its anatomical projections from the limbic system, associated with emotional behaviour.

Voxel-based morphometry

A neuroimaging method that investigates focal differences in brain anatomy.

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Robbins, T.W., Banca, P. & Belin, D. From compulsivity to compulsion: the neural basis of compulsive disorders. Nat. Rev. Neurosci. 25, 313–333 (2024). https://doi.org/10.1038/s41583-024-00807-z

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