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Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers

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Abstract

Rationale

Efficient function of neurocircuitry that supports working memory occurs within a narrow range of dopamine neurotransmission. Work in rodents has shown that exposure to nicotine during adolescence leads to nicotine withdrawal emergent alterations in cortical and subcortical dopamine neurotransmission.

Objectives

To test for evidence that the efficiency of neurocircuitry supporting working memory is altered during acute smoking abstinence in adolescent daily tobacco smokers.

Materials and methods

Fifty-five adolescent daily tobacco smokers were compared with 38 nonsmokers using functional magnetic resonance imaging while subjects performed a verbal working memory task. Smokers were studied during smoking and after 24 h of abstinence from tobacco use.

Results

Performance of a task with high working memory load in the context of smoking abstinence was associated with greater activation of components of the verbal working memory neurocircuit, including left ventrolateral prefrontal cortex and left inferior parietal lobe, among smokers relative to nonsmokers. During smoking abstinence, smokers failed to exhibit increases in functional connectivity between components of the working memory neurocircuit with increasing working memory load observed in nonsmoking adolescents and in prior studies of adults.

Conclusions

Smoking abstinence in adolescent smokers is associated with reductions in the efficiency of working memory neurocircuitry and alterations in the functional coordination between components of the working memory neurocircuit. These alterations may stem from effects of nicotine exposure on catecholaminergic systems during adolescent development.

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Acknowledgment

This research was supported by National Institutes of Health grants DA14655, DA017333, RR06022, and M01RR000125. BioImage Suite was developed with support from NIH RO1 EB006494. The authors thank Jonathan S. Feinstein, PhD for statistical consultation and the subjects and their families for their participation.

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Authors and Affiliations

  1. Department of Psychiatry, Yale University School of Medicine, 2 Church Street South, Suite 207, New Haven, CT, 06519, USA

    Leslie K. Jacobsen

  2. Department of Pediatrics, Yale University School of Medicine, 2 Church Street South, Suite 207, New Haven, CT, 06519, USA

    Leslie K. Jacobsen, Michael Westerveld & Kenneth R. Pugh

  3. Haskins Laboratories, New Haven, CT, USA

    Leslie K. Jacobsen, W. Einar Mencl & Kenneth R. Pugh

  4. Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT, USA

    R. Todd Constable

  5. Department of Neurosurgery, Yale University School of Medicine, New Haven, CT, USA

    R. Todd Constable & Michael Westerveld

  6. Department of Child Study, Yale University School of Medicine, New Haven, CT, USA

    Michael Westerveld

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  1. Leslie K. Jacobsen
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  2. W. Einar Mencl
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  3. R. Todd Constable
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  4. Michael Westerveld
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  5. Kenneth R. Pugh
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Corresponding author

Correspondence to Leslie K. Jacobsen.

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Supplementary Fig. S1

PLS analysis. On the left are shown factor loadings for the first component of the PLS analysis, which accounted for 83% of the variance, primarily reflected positive functional connectivity between the left inferior frontal gyrus and adjacent tissue, with similar loadings across groups and task conditions (factor loadings: smokers: 1-back = 0.39, 2-back = 0.40; nonsmokers: 1-back = 0.63, 2-back = 0.54). Connectivity maps for this component are shown on the right, where red/yellow indicates regions demonstrating positive functional connectivity with the seed region (encircled in green; Talairach coordinates: X = −56, Y = 7, Z = 24) that is consistent with the factor loadings. 1B binaural 1-back task, 2B binaural 2-back task, S smokers, NS nonsmokers (GIF 440 kb)

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Jacobsen, L.K., Mencl, W.E., Constable, R.T. et al. Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology 193, 557–566 (2007). https://doi.org/10.1007/s00213-007-0797-9

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  • DOI: https://doi.org/10.1007/s00213-007-0797-9

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