Smoking withdrawal is associated with increases in brain activation during decision making and reward anticipation: a preliminary study

Abstract

Rationale: Acute nicotine abstinence is associated with disruption of executive function and reward processes; however, the neurobiological basis of these effects has not been fully elucidated.

Methods: The effects of nicotine abstinence on brain function during reward-based probabilistic decision making were preliminarily investigated by scanning adult smokers (n = 13) following 24 h of smoking abstinence and in a smoking-satiated condition. During fMRI scanning, participants completed the wheel of fortune task (Ernst et al. in Neuropsychologia 42:1585-1597, 2004), a decision-making task with probabilistic monetary outcomes. Brain activation was modeled during selection of options, anticipation of outcomes, and outcome feedback.

Results: During choice selection, reaction times were slower, and there was greater neural activation in the postcentral gyrus, insula, and frontal and parietal cortices in the abstinent condition compared to the satiated condition. During reward anticipation, greater activation was observed in the frontal pole, insula, and paracingulate cortex in the abstinent condition compared to the satiated condition. Greater activation was also shown in the precentral gyrus and putamen in the satiated condition compared to the abstinent condition. During the outcome phase, rewards (compared to no rewards) resulted in significant activation in the paracingulate cortex in the satiated condition compared to the abstinent condition.

Conclusions: The results of this preliminary study suggest that smoking withdrawal results in greater recruitment of insular, frontal, and parietal cortical areas during probabilistic decision making.

Figure 1

Screen displays for the three phases of the wheel of fortune (WoF) task. (a) The selection phase consisted of three money trials, in which participants chose to bet on either the blue or magenta slice, or else a control trial. (b) In the anticipation phase, participants rated their confidence in winning the placed bet. (c) In the outcome phase, participants were informed whether or not they won and rated their emotional valence.

Figure 1

Screen displays for the three phases of the wheel of fortune (WoF) task. (a) The selection phase consisted of three money trials, in which participants chose to bet on either the blue or magenta slice, or else a control trial. (b) In the anticipation phase, participants rated their confidence in winning the placed bet. (c) In the outcome phase, participants were informed whether or not they won and rated their emotional valence.

Figure 1

Screen displays for the three phases of the wheel of fortune (WoF) task. (a) The selection phase consisted of three money trials, in which participants chose to bet on either the blue or magenta slice, or else a control trial. (b) In the anticipation phase, participants rated their confidence in winning the placed bet. (c) In the outcome phase, participants were informed whether or not they won and rated their emotional valence.

Figure 2

a Average reaction time for both safe and risky choices. Reaction time during the selection phase of the wheel of fortune (WoF) task was slower during the abstinent condition than during the satiated condition across the three money trials (p < 0.005). b Percentage of risky (magenta) selections across the three money trials. Risky selections were not affected by smoking condition (satiated versus abstinent).

Figure 2

a Average reaction time for both safe and risky choices. Reaction time during the selection phase of the wheel of fortune (WoF) task was slower during the abstinent condition than during the satiated condition across the three money trials (p < 0.005). b Percentage of risky (magenta) selections across the three money trials. Risky selections were not affected by smoking condition (satiated versus abstinent).

Figure 3

During the selection phase, activation was greater in the abstinent condition than the satiated condition in the right insular cortex (IC), the right precentral gyrus (PrG), the right postcentral gyrus (PcG), and the bilateral paracingulate cortex (PCC) (p < 0.01 uncorrected, extent threshold = 53 voxels; MNI brain template).

Figure 4

a During the anticipation phase, activation was greater in the abstinent condition than the satiated condition in the left insular cortex (IC), right paracingulate cortex (PCC), and the right frontal pole (FP). Figure 4b Activation was greater in the satiated condition than the abstinent condition in the right putamen (Pu) and the right precentral gyrus (PrG) (p < 0.01 uncorrected, extent threshold = 53 voxels; MNI brain template).

Figure 4

a During the anticipation phase, activation was greater in the abstinent condition than the satiated condition in the left insular cortex (IC), right paracingulate cortex (PCC), and the right frontal pole (FP). Figure 4b Activation was greater in the satiated condition than the abstinent condition in the right putamen (Pu) and the right precentral gyrus (PrG) (p < 0.01 uncorrected, extent threshold = 53 voxels; MNI brain template).

Figure 5

During the outcome phase, activation was greater during the satiated condition than during the abstinent condition in the left paracingulate cortex (PCC) (p < 0.01 uncorrected, extent threshold = 53 voxels; MNI brain template).