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Chronic smoking, but not acute nicotine administration, modulates neural correlates of working memory

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Abstract

Rationale

Beyond the amelioration of deprivation-induced impairments, and in contrast to effects on attentional processes, the cognitive-enhancing properties of nicotine on working memory (WM) operations remain unclear.

Objectives

In an effort to elucidate potential enhancing effects, we explored the impact of transdermal nicotine on neural functioning in minimally deprived smokers and, in addition, assessed differences between smokers and non-smokers using a mixed block/event-related fMRI design that attempted to isolate specific central executive operations (attentional switch events) within general WM function (task blocks).

Methods

In task blocks, participants performed a continuous counting paradigm that required the simultaneous maintenance of, and frequent switching of attentional focus between, two running tallies in WM on some trials. Cigarette smokers (n = 30) were scanned twice, once each with a nicotine and placebo patch, while non-smokers (n = 27) were scanned twice with no patch.

Results

Across both groups, task blocks were associated with bilateral activation, notably in medial and lateral prefrontal cortex (PFC), anterior insula, and parietal regions, whereas individual attentional switch trials were associated with activation in a similar, but predominantly left-lateralized network. Within the smoker group, although nicotine increased heart rate, altered performance and mood, and reduced tobacco cravings, no acute drug (state-like) effect on brain activity was detected for either the task or switch effects. However, relative to non-smokers, smokers showed greater tonic activation in medial superior frontal cortex, right anterior insula, and bilateral anterior PFC throughout task blocks (trait-like effect).

Conclusions

These data suggest smokers require recruitment of additional WM and supervisory control operations during task performance.

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Notes

  1. While nicotine-induced alterations in behavioral performance were observed, these gross measures collected at the end of the counting blocks are unlikely to be useful indices of the trial-to-trial dynamics associated with attentional switching, but rather may reflect non-specific effects on motoric responding or psychomotor speed.

  2. That is, last cigarette smoked ∼3 h and transdermal patch applied ∼2–2.5 h pre-scan. See also supplementary information regarding additional overlap with the Hahn et al. (2007) study.

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Acknowledgments

This work was supported by the National Institute on Drug Abuse—Intramural Research Program. We thank all NIDA-IRP staff members who assisted in data collection, the NIH Fellow’s Editorial Board for suggestions on this manuscript, and Hugh Garavan.

Conflict of interest

The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Neuroimaging Research Branch, National Institute on Drug Abuse-Intramural Research Program, NIH/DHHS, 251 Bayview Blvd, Suite 200, Baltimore, MD, 21224, USA

    Matthew T. Sutherland, Thomas J. Ross & Elliot A. Stein

  2. Chemistry and Drug Metabolism Section, National Institute on Drug Abuse-Intramural Research Program, NIH/DHHS, 251 Bayview Blvd, Suite 200, Baltimore, 21224, MD, USA

    Diaá M. Shakleya & Marilyn A. Huestis

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  1. Matthew T. Sutherland
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  2. Thomas J. Ross
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  3. Diaá M. Shakleya
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Correspondence to Matthew T. Sutherland.

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This work was supported by the National Institute on Drug Abuse—Intramural Research Program.

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Sutherland, M.T., Ross, T.J., Shakleya, D.M. et al. Chronic smoking, but not acute nicotine administration, modulates neural correlates of working memory. Psychopharmacology 213, 29–42 (2011). https://doi.org/10.1007/s00213-010-2013-6

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