Network failures: When incentives trigger impulsive responses

Hum Brain Mapp. 2020 Jun 1;41(8):2216-2228. doi: 10.1002/hbm.24941. Epub 2020 Mar 9.

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.

Keywords: fMRI; impulsivity; monetary incentive delay; stimulant drug dependence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Anticipation, Psychological / physiology
  • Brain Mapping*
  • Central Nervous System Stimulants
  • Female
  • Gyrus Cinguli / diagnostic imaging
  • Gyrus Cinguli / physiology*
  • Humans
  • Impulsive Behavior / physiology*
  • Magnetic Resonance Imaging
  • Male
  • Motivation / physiology*
  • Neostriatum / diagnostic imaging
  • Neostriatum / physiology*
  • Nerve Net / diagnostic imaging
  • Nerve Net / physiology*
  • Personality / physiology*
  • Prefrontal Cortex / diagnostic imaging
  • Prefrontal Cortex / physiology*
  • Siblings
  • Substance-Related Disorders / diagnostic imaging
  • Substance-Related Disorders / physiopathology
  • Young Adult

Substances

  • Central Nervous System Stimulants