Early Pup Removal Leads to Social Dysfunction and Dopamine Deficit in Late Postpartum Rats: Prevention by Social Support

Offspring interaction is among the most highly motivated behaviors in maternal mammals and is mediated by mesolimbic dopamine (DA) system activation. Disruption or loss of significant social relationships is among the strongest individual predictors of affective dysregulation and depression onset in humans. However, little is known regarding the effects of disrupted mother-infant attachment (pup removal) in rat dams. Here, we tested the effects of permanent pup removal in rat dams, which were assigned to one of three groups on postpartum day (PD) 1: pups; pups removed, single-housed; or pups removed, co-housed with another dam who also had pups removed; and underwent a behavioral test battery during PD 21-23. In vivo electrophysiological recordings of ventral tegmental area (VTA) DA neurons were performed on PD 22 and 23 in a subset of animals. Pup removal did not impact sucrose consumption or anxiety-like behavior, but increased passive forced swim test (FST) coping responses. Pup-removal effects on social behavior and VTA activity were sensitive to social buffering: only single-housed dams exhibited reduced social motivation and decreased numbers of active DA neurons. Dams that had pups removed and were co-housed did not exhibit changes in social behavior or VTA function. Moreover, no changes in social behavior, FST coping, or VTA activity were found in socially isolated adult virgin females, indicating that effects observed in dams are specific to pup loss. This study showed that deprivation of species-expected social relationships (pups) during the postpartum precipitates an enduring negative affect state (enhanced passive coping, blunted social motivation) and attenuated VTA DA function in the dam, and that a subset of these effects is partially ameliorated through social buffering.