Developmental Changes in Habenular and Striatal Social Reinforcement Responsivity Across Adolescence Linked With Substance Use

ABSTRACT

Background

Habenula (HB) function is implicated in substance use disorders and is involved in inhibiting dopamine release in the ventral striatum (VS). While blunted VS reward-responsivity is implicated in risk for later substance use, links between HB reinforcement processing and progression of use has not been examined among adolescents. In the present study, we longitudinally assess HB and VS responsivity to social rewards and punishments, across adolescence, and examine associations with substance use.

Methods

Within a longitudinal design, 170 adolescents (53.5% female) completed 1-3 fMRI scans across 6^th-9^th grade and reported yearly substance use across 6^th-11^th grade. We examined VS and HB responsivity to social reinforcement during a social incentive delay task in which adolescents received social rewards (smiling faces) and punishments (scowling faces).

Results

We observed increased VS responsivity to social rewards (vs. reward omissions) and increased VS, but decreased HB, responsivity to social punishment avoidance vs. receipt. However, contrary to hypotheses, the HB displayed increased responsivity to social rewards (vs. reward omissions). Further, adolescents reporting regular substance use displayed longitudinally declining HB responsivity to social rewards (vs. reward omissions), whereas adolescents reporting no substance use displayed longitudinally increasing HB responsivity. In contrast, whereas VS responsivity to punishment avoidance vs. receipt increased longitudinally among regular substance users, it stayed relatively stable among non-users.

Conclusions

These results suggest differential HB and VS social reinforcement processing trajectories across adolescence are associated with substance use.