Altered executive control network and default model network topology are linked to acute electronic cigarette use: A resting-state fNIRS study

Abstract

In recent years, electronic cigarettes (e-cigs) have gained popularity as stylish, safe, and effective smoking cessation aids, leading to widespread consumer acceptance. Although previous research has explored the acute effects of combustible cigarettes or nicotine replacement therapy on brain functional activities, studies on e-cigs have been limited. Using fNIRS, we conducted graph theory analysis on the resting-state functional connectivity of 61 male abstinent smokers both before and after vaping e-cigs. And we performed Pearson correlation analysis to investigate the relationship between alterations in network metrics and changes in craving. E-cig use resulted in increased degree centrality, nodal efficiency, and local efficiency within the executive control network (ECN), while causing a decrease in these properties within the default model network (DMN). These alterations were found to be correlated with reductions in craving, indicating a relationship between differing network topologies in the ECN and DMN and decreased craving. These findings suggest that the impact of e-cig usage on network topologies observed in male smokers resembles the effects observed with traditional cigarettes and other forms of nicotine delivery, providing valuable insights into their addictive potential and effectiveness as aids for smoking cessation.

Keywords: craving; default mode network; electronic cigarettes; executive control network; graph theory analysis.

FIGURE 1

(A) The experiment procedure of this study. Prior to the experiment, participants were instructed to refrain from smoking for 10–12 h, encompassing both combustible cigarettes and e‐cigs. Upon arrival at the laboratory, the exhaled carbon monoxide (CO) level of the abstinent smokers was assessed, with a requirement that it not exceed 10 ppm. Failure to meet this criterion would result in rescheduling of the experiment. Each session involved the completion of three fNIRS tasks: a resting‐state task, vaping e‐cigarettes, and another resting‐state task. The vaping procedure is depicted in the figure on the right. Participants were asked to take 10 consecutive puffs, with approximately a 30‐s interval between each puff. Subsequent to each puff, the current craving state was promptly evaluated using a brief questionnaire on smoking urge (“I have a desire for a cigarette right now”). (B) the configuration of optodes and channels in fNIRS study. Twelve pairs of sources (red dots) and detectors (blue dots) were placed on the forehead. Channels were formed between the nearby pair of source and detector, resulting in a total of 38 channels (white square with number) obtained through pairwise combinations. According to the channel positioning information, the channels were divided into three regions of interest, namely, the right ECN, left ECN, and DMN.

FIGURE 2

The functional network exhibited small‐world properties, and three ROIs showed altered brain functional characteristics, which were associated with the changes in craving before and after vaping. (A) the functional networks of abstinent smokers before and after using e‐cigs showed a higher clustering coefficient and a characteristic path length (Lp) approximately equal to that of matched random networks, resulting in a γ > 1 and λ ≈ 1. (B) Compared with the matched random networks, the functional networks exhibited higher local efficiency and nearly equal global efficiency. These findings suggest that the functional networks before and after using e‐cigs possess a small‐world topology. Additional detailed on these topological indices can be found in the supplementary materials. The results pertain to the small‐world parameters and network efficiencies of brain functional networks for smokers before and after vaping, with the networks constructed at a threshold level of cost = 0.2. (C) after vaping, the mean degree of the three ROIs significantly changed, with bilateral ECN showing an increase and the DMN showing a decrease. The increased mean degree of the right ECN was associated with decreased subjective craving, while alterations in the mean degree of the DMN were positively correlated with changes in raving. (D) at the global efficiency level, the use of e‐cigs resulted in similar changes in the three ROIs. Moreover, the increase in the global efficiency of the left ECN was related to a decrease in subjective cravings. (E) although vaping led to significant changes in the local efficiency of the ROIs, the magnitude of these changes was not significantly related to changes in craving. The error bars indicate standard deviations.