Dysfunction of the paraventricular thalamus-prelimbic cortex circuit underlies maternal separation-induced deficits in contagious pain.

Contagious pain is considered one of the most common forms of emotional contagion observed in animal models. Nevertheless, little is known about the precise neural mechanisms governing the regulation of contagious pain in response to diverse environmental stressors. Here, we report that early life maternal separation (MS) precipitates impairments in the pain contagion between familiar partners. Specifically, we identify the indispensable role of glutamatergic projections from the paraventricular thalamus (PVT) to the prelimbic cortex (PrL) for the development of vicarious pain hypersensitivity. MS dampens activation of the PVT → PrL pathway during social interactions between observer and painful demonstrator. Augmenting the excitability or activity of the PVT → PrL circuit through chemogenetic interventions or tactile stimulation resembling social touch significantly ameliorates the MS-evoked contagious pain deficits. Collectively, our findings delineate a neural circuitry substrate underlying the loss of contagious pain stemming from MS and propose a potential therapeutic avenue for mitigating empathic impairments associated with early life adversity.