Chronic tobacco smoking, impaired reward-based decision-making, and role of insular cortex: A comparison between early-onset smokers and late-onset smokers

Abstract

IntroductionThe literature suggests that tobacco smoking may have a neurotoxic effect on the developing adolescent brain. Particularly, it may impair the decision-making process of early-onset smokers (<16 years), by rendering them more prone to impulsive and risky choices toward rewards, and therefore more prone to smoking relapses, in comparison to late-onset smokers (≥16 years). However, no study has ever investigated reward-based decision-making and structural brain differences between early-onset smokers and late-onset smokers.MethodsComputerized measures of reward-based decision-making [Cambridge Gambling Task (CGT); 5-trials adjusting delay discounting task (ADT-5)] were administered to 11 early-onset smokers (mean age at regular smoking initiation = 13.2 years), 17 late-onset smokers (mean age at regular smoking initiation = 18.0 years), and 24 non-smoker controls. Voxel-based morphometry (VBM) was utilized to investigate the gray matter (GM) and white matter (WM) volume differences in fronto-cortical and striatal brain regions between early-onset smokers, late-onset smokers, and non-smokers.ResultsEarly-onset smokers displayed a riskier decision-making behavior in comparison to non-smokers as assessed by the CGT (p < 0.01, Cohen’s f = 0.48). However, no significant differences (p > 0.05) in reward-based decision-making were detected between early-onset smokers and late-onset smokers. VBM results revealed early-onset smokers to present lower GM volume in the bilateral anterior insular cortex (AI) in comparison to late-onset smokers and lower WM volume in the right AI in comparison to late-onset smokers.ConclusionImpairments in reward-based decision-making may not be affected by tobacco smoking initiation during early adolescence. Instead, lower GM and WM volume in the AI of early-onset smokers may underline a vulnerability to develop compulsive tobacco seeking and smoking behavior during adulthood.

Early-onset smoking theory of compulsivity development: a neurocognitive model for the development of compulsive tobacco smoking

“…No correlations were identified between tobacco use/exposure characteristics and GM/WM volume of early-onset smokers' anterior insular cortex. As reported in our previous study, this may indicate that such structural abnormalities were not due to differences in tobacco exposure between the two groups ( 31 ).…”

“…Recently, we conducted a VBM study hypothesizing that 11 adult smokers (mean age at recruitment = 25.2 years) who started regular tobacco use at 13.2 years of age (i.e., early-onset smokers) would present heightened impulsive and risky choices, in addition to reduced GM and WM volume in frontal brain regions modulating such behaviors in comparison with 17 adult smokers (mean age at recruitment= 30 years) who started regular smoking at 18 years of age (i.e., late-onset smokers) and 24 matched non-smoker controls ( 31 ). Our hypotheses were based on the previously cited TINACD theory ( 11 ).…”

“…From a neuroanatomical point of view, early-onset smokers displayed lower GM volume in the right ACC and lower WM volume in the left anterior corpus callosum, left anterior insular cortex, and bilateral thalamus in comparison with non-smokers ( 31 ). Remarkably, early-onset tobacco smokers displayed significantly lower GM volume in the bilateral anterior insular cortex and lower WM volume in the right anterior insular cortex in comparison with late-onset smokers ( 31 ) ( Figures 1 , 2 ).…”

“…According to the authors, this decrease in fiber density may represent the neuro-maturational processes of myelination and synaptic pruning that peak during adolescence. Nevertheless, as our VBM study ( 31 ) employed a cross-sectional design, it is not possible to infer causality, and the possibility that structural brain abnormalities in the anterior insular cortex of early-onset smokers were pre-existing cannot be excluded. Regardless of a possible neurotoxic effect of tobacco on the adolescent brain, it could be postulated that structural brain abnormalities in the anterior insular cortex of early-onset smokers may facilitate a compulsive smoking behavior and therefore heaviness of smoking during adulthood.…”

The Combined Effects of Nicotine and Cannabis on Cortical Thickness Estimates in Adolescents and Emerging Adults

“…Nicotine, a key component found in tobacco and electronic cigarettes, intricately engages with the developing brain primarily through its interaction with nicotinic acetylcholine receptors (nAChRs) crucial for regulating cognitive and neural functions, potentially resulting in changes at both structural and functional levels [ 56 , 57 , 58 ]. Prior research has shown that nicotine exposure during this adolescent and emerging adult developmental phase can influence neural plasticity and neurotransmitter systems, potentially leading to modifications in gray matter integrity, white matter development, and cortical thickness [ 27 , 29 , 59 , 60 , 61 ]. Our findings, showing thinner cortical estimates in regions such as the right precentral gyrus, left superior frontal gyrus, left pars opercularis, and left frontal pole among nicotine users, may reflect deleterious alterations in neuromaturation.…”