Performance effects of nicotine during selective attention, divided attention, and simple stimulus detection: an fMRI study

Abstract

Attention-enhancing effects of nicotine appear to depend on the nature of the attentional function. Underlying neuroanatomical mechanisms, too, may vary depending on the function modulated. This functional magnetic resonance imaging study recorded blood oxygen level-dependent (BOLD) activity in minimally deprived smokers during tasks of simple stimulus detection, selective attention, or divided attention after single-blind application of a transdermal nicotine (21 mg) or placebo patch. Smokers' performance in the placebo condition was unimpaired as compared with matched nonsmokers. Nicotine reduced reaction time (RT) in the stimulus detection and selective attention but not divided attention condition. Across all task conditions, nicotine reduced activation in frontal, temporal, thalamic, and visual regions and enhanced deactivation in so-called "default" regions. Thalamic effects correlated with RT reduction selectively during stimulus detection. An interaction with task condition was observed in middle and superior frontal gyri, where nicotine reduced activation only during stimulus detection. A visuomotor control experiment provided evidence against nonspecific effects of nicotine. In conclusion, although prefrontal activity partly displayed differential modulation by nicotine, most BOLD effects were identical across tasks, despite differential performance effects, suggesting that common neuronal mechanisms can selectively benefit different attentional functions. Overall, the effects of nicotine may be explained by increased functional efficiency and downregulated task-independent "default" functions.

Figure 1.

Examples of the task stimuli. Participants were instructed to detect a difference in either the angles of the 2 wedges, in the sequence of color across the 3 rings, or in either aspect. In (A), there is a difference in the color dimension. In (B), there is a difference in the angle dimension. (C) Represents a stimulus presented during SDT, where responses did not depend on any stimulus aspects.

Figure 2.

Average (±standard error of the mean) DT (A) and RT (B) of 18 smokers performing the SDT, the angle discrimination (Sel-A), color discrimination (Sel-C), or combined angle and color discrimination task (divided attention, DIV) while wearing a nicotine or placebo patch. Significant differences between the nicotine and placebo session (**P < 0.01, ***P < 0.001, paired t-test) and between task conditions (###P < 0.001, paired t-test) are indicated.

Figure 3.

Brain regions displaying a main effect of nicotine across all 4 task conditions. Group activation maps are overlaid onto an individual anatomical scan in Talairach space. Slices are displayed in neurological view (left is on the viewer's left). In all regions, nicotine decreased the BOLD signal, causing either reductions in activation or significant deactivations. Regional BOLD activity is presented in the graph as averages ± standard error of the mean (n = 18). Significant differences from zero in 1-sample t-tests are indicated (*P < 0.05, **P < 0.01, ***P < 0.001). The difference between the nicotine and placebo session was always significant in paired t-tests (P < 0.003 in all regions). The numbering corresponds to ROIs in Table 1.

Figure 4.

Brain regions displaying an interaction of the effects of nicotine with task condition. Nicotine induced deactivation in right (R) MFG and SFG only in the SDT task. Significant differences between the nicotine and placebo session are indicated (*P < 0.05, **P < 0.01, paired t-test).