Valence-dependent synaptic plasticity drives approach and avoidance behavior in social context

Abstract Social interactions critically shape future decisions about engaging with or avoiding conspecifics. However, how the valence of previous social experiences translates into adaptive approach or avoidance behaviors remains unclear. Here, we identify a novel circuit from dopamine D1 receptor (D1R)-expressing neurons in the anterior insular cortex (AIC) to D1R-expressing neurons in the lateral nucleus accumbens (LNAc). We show that valence-specific firing frequencies—low-frequency for reward and high-frequency for aversion—induced distinct synaptic plasticity at these synapses. Imposing aversive-like firing patterns during rewarding interactions disrupts plasticity and subsequent social approach. Finally, we identify mGluR1 signaling as a critical molecular mechanism selectively required for positive-valence learning. Together, our findings elucidate the synaptic and molecular mechanisms by which social valence guides adaptive behavioral decisions, highlighting frequency-dependent plasticity within a single neural circuit as a dynamic regulator of social approach or avoidance.