Ventral Tegmental Area Dopamine Neuron Dynamics During Postpartum Scarcity-Adversity Depend on Caregiving Quality and Pup Proximity

Maternal behaviors are evolutionarily conserved yet sensitive to environmental factors such as resource availability. Scarcity-adversity, modeled by providing dams with reduced bedding and nesting materials, reliably induces changes in sensitive and insensitive pup-directed maternal behaviors. Ventral tegmental area (VTA) dopamine (DA) neurons are activated by pup interactions and required for the expression of normal maternal behaviors. However, the effects of postpartum scarcity-adversity on dam VTA DA neuron activity during caregiving alterations remain unexplored. We conducted in vivo fiber photometry recordings of VTA DA neuron activity using Cre-dependent GCaMP7f in postpartum female TH-Cre rat dams in control or scarcity-adversity conditions. Dams were assigned to control or scarcity-adversity conditions on postpartum day (PD) 2 and underwent daily fiber photometry recordings during naturalistic maternal behavior observation sessions and a food pellet reward retrieval task through PD 5. Scarcity-adversity dams showed significantly elevated VTA DA neuron activity during insensitive caregiving, reflected by increased area under the curve, with no group differences during sensitive care. Additionally, scarcity-adversity dams exhibited a decrease in frequency of peaks when separated from their pups (i.e., out of nest), with no group differences during pup contact or nursing. Critically, alterations in VTA DA neuron activity in scarcity-adversity dams were not observed during food reward retrieval, suggesting that postpartum scarcity-adversity selectively disrupts VTA DA dynamics within the maternal caregiving context. These findings show that postpartum resource scarcity induces context-specific alterations in VTA DA neuron activity and provide a foundation for future investigation of projection-specific mechanisms underlying adversity-induced maternal behavior deficits. Significance Statement Postpartum adversity compromises maternal caregiving and increases risk for postpartum depression, but how it alters real-time maternal brain function during active caregiving is poorly understood. Using fiber photometry in TH-Cre dams exposed to resource scarcity, we demonstrate that adversity alters ventral tegmental area (VTA) dopamine (DA) neuron activity during ongoing maternal behavior in a context-dependent manner. Adversity elevated VTA DA neuron activity during insensitive caregiving and reduced VTA DA activity during pup separation, without affecting VTA DA responses to food. These findings reveal that postpartum scarcity-adversity shapes the motivational architecture of maternal caregiving through context-specific alterations in VTA DA neuron dynamics, providing a neurobiological framework for understanding how adverse postpartum environments impair maternal care quality without broadly affecting reward processing.