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Fractionating impulsivity: neuropsychiatric implications

Key Points

  • Although also being a characteristic of normal behaviour, excessive impulsivity is an important symptom of several neuropsychiatric and neurological disorders, including addiction, attention-deficit hyperactivity disorder and Parkinson disease.

  • However, impulsivity may comprise several apparently related forms that depend on distinct neuropsychological processes and neural systems. Of particular importance are interactions between frontostriatal systems and their neurochemical modulation, which are also providing new insights into the functions of these systems in behaviour.

  • The psychological and neural basis of impulsivity can be studied in a mutually profitable way in experimental animals and in humans. Striking parallels can be observed in the underlying neurobehavioural systems, allowing both macro- and micro-definition of functional circuits.

  • The dissection of impulsivity in this Review may represent a way in which complex behaviour relevant to psychiatric disorders can be broken down into its constituent parts, thus allowing for improved genetic understanding and more-precise treatments at the level of symptoms rather than according to categorical diagnoses of mental health disorders.

Abstract

The ability to make decisions and act quickly without hesitation can be advantageous in many settings. However, when persistently expressed, impulsive decisions and actions are considered risky, maladaptive and symptomatic of such diverse brain disorders as attention-deficit hyperactivity disorder, drug addiction and affective disorders. Over the past decade, rapid progress has been made in the identification of discrete neural networks that underlie different forms of impulsivity — from impaired response inhibition and risky decision making to a profound intolerance of delayed rewards. Herein, we review what is currently known about the neural and psychological mechanisms of impulsivity, and discuss the relevance and application of these new insights to various neuropsychiatric disorders.

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Figure 1: Translatable experimental paradigms to assess impulsivity in rodents and humans.
Figure 2: Distinct loci of 'stopping' and 'waiting' impulsivity in the dorsal and ventral striatum.
Figure 3: Topographical organization of the corticostriatal circuitry and associated impulsivity constructs in humans.

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Acknowledgements

The authors acknowledge support from the Wellcome Trust (grant 104631/Z/14/Z), UK Medical Research Council (grants G0701500, G0802729 and G9536855) and the European Commission (IMAGEN LSHM-CT-2007-037286). The Cambridge University Behavioural and Clinical Neuroscience Institute is supported by a joint award from the Wellcome Trust (093875/Z/10/Z) and Medical Research Council (G1000183). The authors also thank L. Morris and V. Voon for the frontostriatal connectivity illustrations in figure 3.

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Correspondence to Trevor W. Robbins.

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T.W.R. discloses consultancy with Cambridge Cognition, Lundbeck, Otsuka and Mundipharma, as well as a research grant with Lundbeck, royalties for CANTAB and editorial honoraria with Springer-Verlag and Elsevier. J.W.D. discloses research grant support from Boehringer Ingelheim and editorial honoraria from Wiley and Sage.

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Glossary

Differential reinforcement of low rates of responding (DRL) schedules

Schedules of reinforcement of instrumental behaviour in which the animal must wait for a given time after the last reinforcer before making an instrumental response.

Sensation seeking

A type of behaviour in which individuals apparently seek certain types of experience (such as mountaineering) despite the associated risks.

5-choice serial reaction time task

(5CSRTT). A behavioural test of sustained attention; animals must detect brief signals that predict food rewards. Importantly, animals are punished for responding prematurely.

Nafadotride

A relatively selective dopamine D3 receptor antagonist.

Dopamine transporter

(DAT). A transmembrane protein that pumps dopamine from the synapse into the neuron. Some drugs (for example, cocaine, methylphenidate and amphetamine) increase synaptic dopamine levels by blocking DAT.

Amphetamine

A psychomotor stimulant drug (a catecholaminergic indirect agonist) that increases activity and arousal. It is used as an effective, although perhaps paradoxical, treatment for attention-deficit hyperactivity disorder.

Autoreceptors

Receptors found in the presynaptic neuronal membrane, at both the neuronal bodies and the terminals. Their activity negatively regulates neurotransmitter release.

Antidromic

Referring to conduction of an action potential in the opposite direction; that is, away from the axon terminal to the cell body.

Striatal indirect pathway

A striatal output pathway in which striatal medium spiny neurons project via inhibitory neurons, first to the globus pallidus externa and thence to the subthalamic nucleus, which disinhibits the substantia nigra pars reticulata–globus pallidus interna.

Striatal direct pathway

A striatal output pathway in which inhibitory neurons directly project onto the cells of the substantia nigra pars reticulata–globus pallidus interna.

Hyperdirect pathway

Direct excitatory projections from several cortical areas, including the motor cortex, premotor cortex, supplementary motor area, anterior cingulate and dorsolateral prefrontal cortex, to the subthalamic nucleus, by-passing the striatum.

Beta system

A set of brain regions, including the nucleus accumbens and medial prefrontal cortex, that are postulated to process immediate rewards and hypothetically interact functionally with the so-called delta system.

Delta system

A set of brain regions, including the dorsolateral and ventrolateral prefrontal cortex and parietal cortex, that are thought to discount rewards over longer time periods and to determine behaviour by interactions with the so-called beta system.

Endophenotypes

A term from genetic epidemiology, implying, in psychiatry, an intermediate phenotype with a possible heritable basis, present not only in patients but also in their clinically non-affected first-degree relatives.

Goal-directed

Instrumental or purposeful, conscious and volitional, and in pursuit of defined outcomes.

Habitual

Elicited automatically by stimuli in the environment without reference to a goal or outcome.

Model-free learning algorithms

Algorithms for learning that reflect immediate reinforcement learning contingencies and therefore are associated with habitual behaviour.

Conduct disorder

A mental disorder of childhood or adolescence in which violent or disruptive anti-social behaviour is the main characteristic.

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Dalley, J., Robbins, T. Fractionating impulsivity: neuropsychiatric implications. Nat Rev Neurosci 18, 158–171 (2017). https://doi.org/10.1038/nrn.2017.8

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