Dorsal and ventral striatal functional connectivity shifts play a potential role in internet gaming disorder

Guang-Heng Dong,Min Wang,Haohao Dong,Marc N Potenza,Weiran Zhou,Xiaoxia Du,Jialin Zhang

doi:10.1038/s42003-021-02395-5

Abstract

Animal models suggest transitions from non-addictive to addictive behavioral engagement are associated with ventral-to-dorsal striatal shifts. However, few studies have examined such features in humans, especially in internet gaming disorder (IGD), a proposed behavioral addiction. We recruited 418 subjects (174 with IGD; 244 with recreational game use (RGU)). Resting-state fMRI data were collected and functional connectivity analyses were performed based on ventral and dorsal striatal seeds. Correlations and follow-up spectrum dynamic causal model (spDCM) analyses were performed to examine relationships between the ventral/dorsal striatum and middle frontal gyrus (MFG). Longitudinal data were also analysed to investigate changes over time. IGD relative to RGU subjects showed lower ventral-striatum-to-MFG (mostly involving supplementary motor area (SMA)) and higher dorsal-striatum-to-MFG functional connectivity. spDCM revealed that left dorsal-striatum-to-MFG connectivity was correlated with IGD severity. Longitudinal data within IGD and RGU groups found greater dorsal striatal connectivity with the MFG in IGD versus RGU subjects. These findings suggest similar ventral-to-dorsal striatal shifts may operate in IGD and traditional addictions.

Highlights

Animal models suggest transitions from non-addictive to addictive behavioral engagement are associated with ventral-to-dorsal striatal shifts
When examining the left dorsal and ventral striatal region of interests (ROIs), significant interactions were observed in relation to middle frontal gyrus (MFG) connectivity in internet gaming disorder (IGD) and recreational game use (RGU) subjects (F(1, 416) = 19.293, p < 0.001, η2 = 0.044)
Significant increases from ventral striatum (VS) to dorsal striatum (DS) were observed in both hemispheres in RGU and IGD separately (Fig. 1 and Table 1)

Summary

Introduction

Animal models suggest transitions from non-addictive to addictive behavioral engagement are associated with ventral-to-dorsal striatal shifts. Longitudinal data within IGD and RGU groups found greater dorsal striatal connectivity with the MFG in IGD versus RGU subjects. These findings suggest similar ventral-to-dorsal striatal shifts may operate in IGD and traditional addictions. The VS receives dopaminergic inputs primarily (but not exclusively) from the ventral tegmental area, and the DS receives dopaminergic afferents from the substantia nigra[8] This heterogeneous connection within the striatum has multiple contributions to addiction-related processes. Animal models and theories of substance and behavioural addictions have suggested that transitions from non-addictive to addictive engagement may involve shifts in involvement of ventral-todorsal striatal cortico-striato-thalamo-cortical circuits[1,2,9]. DS neuroadaptations have been implicated in transitions between incentive-based and habit-based control of behaviours, and greater involvement of the DS is often observed when substance/drug intake is more addictive or compulsive[3,13]

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