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The Journal of Neuroscience, March 28, 2007, 27(13):3477-3489; doi:10.1523/JNEUROSCI.5129-06.2007

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Behavioral/Systems/Cognitive
Nicotine Enhances Visuospatial Attention by Deactivating Areas of the Resting Brain Default Network

Britta Hahn,¹ Thomas J. Ross,¹ Yihong Yang,¹ Insook Kim,² Marilyn A. Huestis,² and Elliot A. Stein¹

¹Neuroimaging Research Branch and ²Chemistry and Drug Metabolism Section, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, Maryland 21224

Correspondence should be addressed to Britta Hahn, Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, 5500 Nathan Shock Drive, Baltimore, MD 21224. Email: bhahn{at}intra.nida.nih.gov

Nicotine-induced attentional enhancement is of potential therapeutic value. To investigate the precise attentional function(s) affected and their neuronal mechanisms, the current functional magnetic resonance imaging (fMRI) study used an attention task in which subjects responded to stimuli of high (INT_high) or low intensity presented randomly in one of four peripheral locations. Central cues of varying precision predicted the target location. In some trials, the cue was not followed by a target, allowing separate analysis of blood oxygenation level-dependent (BOLD) responses to cue. Minimally deprived smokers underwent fast event-related fMRI twice: once with a nicotine patch (21 mg) and once with a placebo patch. Matched nonsmokers were scanned twice without a patch. Behaviorally, nicotine reduced omission errors and reaction time (RT) of valid and invalid cue trials and intra-individual variability of RT and did so preferentially in trials with INT_high. The BOLD signal related to cue-only trials, regardless of cue precision, demonstrated nicotine-induced deactivation in anterior and posterior cingulate, angular gyrus, middle frontal gyrus, and cuneus. These regions overlapped with the so-called "default network," which activates during rest and deactivates with attention-demanding activities. Partial correlations controlling for nicotine plasma levels indicated associations of deactivation by nicotine in posterior cingulate and angular gyrus with performance improvements under INT_high. Performance and regional activity in the absence of nicotine never differed between smokers and nonsmokers, ruling out a simple reversal of a deprivation-induced state. These findings suggest that nicotine improved attentional performance by downregulating resting brain function in response to task-related cues. Together with the selectivity of effects for INT_high, this suggests a nicotine-induced potentiation of the alerting properties of external stimuli.

Key words: nicotine; attention; fMRI; default network; alerting; ASL

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Received Sept. 11, 2006; revised Feb. 21, 2007; accepted Feb. 22, 2007.

Correspondence should be addressed to Britta Hahn, Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, 5500 Nathan Shock Drive, Baltimore, MD 21224. Email: bhahn{at}intra.nida.nih.gov

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