Multimodal 7T Imaging reveals enhanced functional coupling between Salience and Frontoparietal networks mediating aberrant intertemporal choice but intact microstructural architecture and diffusion connectivity in young adult tobacco cigarette smokers.

Abstract

Abstract BACKGROUND: Deficits in intertemporal choice (ITC) are an important predictor of tobacco use and relapse rates. Cigarette smoking is associated with disrupted brain network dynamics in cognitive resting networks including the Salience (SN) and Fronto parietal (FPN). Unified multimodal methods [Resting state connectivity analysis, Diffusion Tensor Imaging (DTI), neurite orientation dispersion and density imaging (NODDI), and cortical thickness analysis] were employed to test the hypothesis that smokers have deficits in inter temporal choice and these deficits may be due to alterations in white matter (WM) microstructure and connectivity, functional connectivity and cortical thickness (CT). METHODS: Multimodal analyses of previously collected 7 Tesla MRI data via the Human Connectome Project were performed on 22 smokers (average number of daily cigarettes was 40 ± 4) and 22 age- and sex-matched nonsmoking controls. First, subjects scores on the delay discounting test were analyzed. Functional connectivity analysis was used to examine SN-FPN interactions between smokers and nonsmokers. The anatomy of these networks was then assessed using DTI and CT analyses while microstructural architecture of WM was analyzed using NODDI. RESULTS: Smokers scored significantly lower on all the items within delay discounting task (DD)] except for tasks: subjective value for $4K at 6 months and subjective value for $4K at 1-year tasks where we observed a trend. Seed-based connectivity analysis revealed significantly enhanced within network [p = 0.001 FDR corrected] and between network functional coupling of the salience and R-FP networks in smokers [p = 0.004 FDR corrected]. Functional coupling scores were inversely correlated with DD scores in nonsmokers. The total number of cigarettes smoked strongly correlated with FagerstrÖm Test for Nicotine Dependence scores. Whole brain diffusion analysis revealed no significant differences between smokers and nonsmokers in Fractional Anisotropy, and Mean diffusivities and in neurite orienting and density. There were also no significant differences in CT in the hubs of these networks. CONCLUSIONS: Our results demonstrate that tobacco cigarette smoking is associated with steeper devaluation of delayed rewards mirrored in enhanced functional connectivity, but anatomy is largely intact in young adults. Whether these reductions are pre-existing, transient or permanent is not known. The observed disrupted salience in resting state networks may be the reason for steeper discounting in smokers which may contribute to difficulties in quitting and/or facilitating relapse.