Greater externalizing personality traits predict less error-related insula and anterior cingulate cortex activity in acutely abstinent cigarette smokers

Allison J. Carroll, Matthew T. Sutherland*, Betty Jo Salmeron, Thomas J. Ross, Elliot A. Stein

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

Abstract

Attenuated activity in performance-monitoring brain regions following erroneous actions may contribute to the repetition of maladaptive behaviors such as continued drug use. Externalizing is a broad personality construct characterized by deficient impulse control, vulnerability to addiction and reduced neurobiological indices of error processing. The insula and dorsal anterior cingulate cortex (dACC) are regions critically linked with error processing as well as the perpetuation of cigarette smoking. As such, we examined the interrelations between externalizing tendencies, erroneous task performance, and error-related insula and dACC activity in overnight-deprived smokers (n-=-24) and non-smokers (n-=-20). Participants completed a self-report measure assessing externalizing tendencies (Externalizing Spectrum Inventory) and a speeded Flanker task during functional magnetic resonance imaging scanning. We observed that higher externalizing tendencies correlated with the occurrence of more performance errors among smokers but not non-smokers. Suggesting a neurobiological contribution to such suboptimal performance among smokers, higher externalizing also predicted less recruitment of the right insula and dACC following error commission. Critically, this error-related activity fully mediated the relationship between externalizing traits and error rates. That is, higher externalizing scores predicted less error-related right insula and dACC activity and, in turn, less error-related activity predicted more errors. Relating such regional activity with a clinically relevant construct, less error-related right insula and dACC responses correlated with higher tobacco craving during abstinence. Given that inadequate error-related neuronal responses may contribute to continued drug use despite negative consequences, these results suggest that externalizing tendencies and/or compromised error processing among subsets of smokers may be relevant factors for smoking cessation success. As compromised error processing is linked to certain personality traits and drug abuse, we examined in cigarette smokers the interrelations between erroneous task performance, externalizing personality characteristics, and error-related brain activity. We observed during smoking abstinence that higher externalizing scores predicted less error-related activity in the insula and anterior cingulate cortex and, in turn, that less error-related activity predicted more commission errors. These results suggest that externalizing traits and/or compromised error processing may be relevant factors for smoking cessation success.

Original languageEnglish (US)
Pages (from-to)377-389
Number of pages13
JournalAddiction Biology
Volume20
Issue number2
DOIs
StatePublished - Mar 1 2015

Keywords

  • Anterior cingulate cortex
  • errors
  • functional magnetic resonance imaging (fMRI) impulsivity
  • insula
  • nicotine abstinence

ASJC Scopus subject areas

  • Medicine (miscellaneous)
  • Pharmacology
  • Psychiatry and Mental health

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