Increased functional coupling between the left fronto-parietal network and anterior insula predicts steeper delay discounting in smokers

Authors

  • David Clewett,

    Corresponding author
    1. Neuroscience Graduate Program, University of Southern California, Los Angeles, California
    • Correspondence to: David Clewett, Hedco Neuroscience Bldg, Rm 117, 3641 Watt Way, Los Angeles, CA 90089. E-mail: clewett@usc.edu or Shan Luo, Hedco Neuroscience Bldg, Rm 117, 3641 Watt Way, Los Angeles, CA 90089. E-mail: shanluo@usc.edu

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  • Shan Luo,

    Corresponding author
    1. National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China
    2. Department of Psychology, University of Southern California, Los Angeles, California
    3. Keck School of Medicine, Division of Endocrinology, University of Southern California, Los Angeles, California
    • Correspondence to: David Clewett, Hedco Neuroscience Bldg, Rm 117, 3641 Watt Way, Los Angeles, CA 90089. E-mail: clewett@usc.edu or Shan Luo, Hedco Neuroscience Bldg, Rm 117, 3641 Watt Way, Los Angeles, CA 90089. E-mail: shanluo@usc.edu

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  • Eustace Hsu,

    1. Department of Psychology, University of Southern California, Los Angeles, California
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  • George Ainslie,

    1. Coatesville Veterans Affairs Medical Center, Coatesville, Pennsylvania
    2. University of Cape Town, Rondebosch, South Africa
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  • Mara Mather,

    1. Neuroscience Graduate Program, University of Southern California, Los Angeles, California
    2. Department of Psychology, University of Southern California, Los Angeles, California
    3. Brain and Creativity Institute, University of Southern California, Los Angeles, California
    4. Davis School of Gerontology, University of Southern California, Los Angeles, California
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  • John Monterosso

    1. Neuroscience Graduate Program, University of Southern California, Los Angeles, California
    2. Department of Psychology, University of Southern California, Los Angeles, California
    3. Brain and Creativity Institute, University of Southern California, Los Angeles, California
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  • David Clewett and Shan Luo contributed equally to this article.

  • This work was supported by the National Institute of Health R01DA023176 (JM).

Abstract

In previous work, smokers showed steeper devaluation of delayed rewards than non-smokers. While the neural correlates of this link between nicotine dependence and delay of discounting are not established, altered activity in executive networks may relate to impaired delayed gratification. The goal of this study was to examine neural correlates of discounting and their relation to nicotine dependence. Thirty-nine smokers and 33 non-smokers completed a functional magnetic resonance imaging (fMRI) intertemporal choice task in which they made individualized Hard (similarly valued), easy (dissimilarly valued), and control monetary choices. FMRI data were analyzed using a group independent component analysis and dual regression. Smokers discounted more steeply than non-smokers, although this difference was only significant among severely dependent smokers. Intertemporal choices recruited distinct left- and right-lateralized fronto-parietal networks. A group-by-difficulty interaction indicated that smokers, relative to non-smokers, exhibited less difficulty-sensitivity in the right fronto-parietal network. In contrast, smokers showed greater functional connectivity between the left fronto-parietal network and the left fronto-insular cortex. Moreover, the degree of functional connectivity between the left fronto-parietal network and left fronto-insular cortex was significantly correlated with individual differences in discounting. Thus, greater functional coupling between the anterior insula and left fronto-parietal network is a candidate neural substrate linking smoking and impulsivity. Given the anterior insula's role in interfacing cognitive and interoceptive processing, this altered functional connectivity may relate to an addiction-related bias towards immediate rewards. Hum Brain Mapp 35:3774–3787, 2014. © 2014 Wiley Periodicals, Inc.

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