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Network failures: When incentives trigger impulsive responses.

Accepted version
Peer-reviewed

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Type

Article

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Authors

Morein-Zamir, Sharon 
Meng, Chun 
Dalley, Jeffrey W 

Abstract

Adequate control of impulsive urges to act is demanded in everyday life but is impaired in neuropsychiatric conditions such as stimulant use disorder. Despite intensive research it remains unclear whether failures in impulse control are caused by impaired suppression of behavior or by the over invigoration of behavior by stimuli associated with salient incentives such as drugs, food, and money. We investigated failures in impulse control using functional magnetic resonance imaging (fMRI) to map the neural correlates of premature (impulsive) responses during the anticipation phase of the Monetary Incentive Delay (MID) task in healthy controls (HC), stimulant-dependent individuals (SDIs), and their unaffected first-degree siblings (SIB). We combined task-based fMRI analyses with dynamic causal modeling to show that failures of impulse control were associated with interactions between cingulo-opercular and dorsal striatal networks regardless of group status and incentive type. We further report that group-specific incentive salience plays a critical role in modulating impulsivity in SDIs since drug-related incentives specifically increased premature responding and shifted task modulation away from the dorsal striatal network to the cingulo-opercular network. Our findings thus indicate that impulsive actions are elicited by salient personally-relevant incentive stimuli and those such slips of action recruit a distinct fronto-striatal network.

Description

Keywords

fMRI, impulsivity, monetary incentive delay, stimulant drug dependence, Adult, Anticipation, Psychological, Brain Mapping, Central Nervous System Stimulants, Female, Gyrus Cinguli, Humans, Impulsive Behavior, Magnetic Resonance Imaging, Male, Motivation, Neostriatum, Nerve Net, Personality, Prefrontal Cortex, Siblings, Substance-Related Disorders, Young Adult

Journal Title

Hum Brain Mapp

Conference Name

Journal ISSN

1065-9471
1097-0193

Volume Title

41

Publisher

Wiley

Rights

All rights reserved
Sponsorship
Medical Research Council (G0701497)
Cambridgeshire and Peterborough NHS Foundation Trust (CPFT) (unknown)
Cambridgeshire and Peterborough NHS Foundation Trust (CPFT) (unknown)
Wellcome Trust (105602/Z/14/Z)
This research was funded by a Medical Research Council (MRC) grant (G0701497), financially supported by the NIHR Cambridge Biomedical Research Centre, and conducted within the Behavioural and Clinical Neuroscience Institute (BCNI). CM is supported by the Wellcome Trust (105602/Z/14/Z) and the NIHR Cambridge Biomedical Research Centre. PZ was supported by the Pinsent Darwin studentship from the Department of Physiology, Development and Neuroscience, University of Cambridge.