Electrical stimulation reduces smokers' craving by modulating the coupling between dorsal lateral prefrontal cortex and parahippocampal gyrus

Abstract

Applying electrical stimulation over the prefrontal cortex can help nicotine dependents reduce cigarette craving. However, the underlying mechanism remains ambiguous. This study investigates this issue with functional magnetic resonance imaging. Thirty-two male chronic smokers received real and sham stimulation over dorsal lateral prefrontal cortex (DLPFC) separated by 1 week. The neuroimaging data of the resting state, the smoking cue-reactivity task and the emotion task after stimulation were collected. The craving across the cue-reactivity task was diminished during real stimulation as compared with sham stimulation. The whole-brain analysis on the cue-reactivity task revealed a significant interaction between the stimulation condition (real vs sham) and the cue type (smoking vs neutral) in the left superior frontal gyrus and the left middle frontal gyrus. The functional connectivity between the left DLPFC and the right parahippocampal gyrus, as revealed by both psychophysical interaction analysis and the resting state functional connectivity, is altered by electrical stimulation. Moreover, the craving change across the real and sham condition is predicted by alteration of functional connectivity revealed by psychophysical interaction analysis. The local and long-distance coupling, altered by the electrical stimulation, might be the underlying neural mechanism of craving regulation.

Keywords: DLPFC; addiction; brain stimulation; craving; nicotine dependence; tDCS.

Fig. 1

Overview of the study procedure. The go/no-go task and MID task (Monetary Incentive Delay task) belonged to another study on the online effect of tDCS.

Fig. 2

(A) The smoking-neutral contrast map in the cue-reactivity task. l: left; r: right; MPFC, medial prefrontal cortex; PHG, para-hippocampal gyrus; FG: right fusiform gyrus; MTG: middle temporal gyrus; PCC, posterior cingulate cortex; SFG: superior frontal gyrus; MFG: middle frontal gyrus. The left, the posterior, and the inferior directions are negative. The contrast map was thresholded with cluster-wise P values <0.05. (B) tDCS × cue type interaction. (C) A detailed illustration of the tDCS × cue interaction in the left SFG and the left MFG.

Fig. 3

(A) The tDCS effect on PPI between lDLPFC and cue-related brain regions. (B) The tDCS effect on resting state functional connectivity between lDLPFC and cue-related brain regions.

Fig. 4

(A) Craving change (%) across cue-reactivity task in sham and real stimulation. The length of the error bar represents the standard error of the mean. (B) The changes of PPI between lDLPFC and rPHG across the two sessions (real–sham) correlated with the craving changes across the two sessions (real–sham).