Longitudinal monitoring of maternal care and maternal neglect

Parental care is required to ensure the health and survival of offspring. Caretaking in mammals is challenging as infants are largely helpless and require near-continual oversight over prolonged periods. Mouse pups in particular cannot thermoregulate, and will succumb to hypothermia unless kept warm by an adult caretaker or an insulating nest. Parents must balance caretaking behaviors with other activities important for survival such as regulating their own temperature and foraging for food or water, which necessarily involve periods of pup neglect. To understand in high detail the consequential decision-making involved in care of infant pups, we built a new system for long-term 24/7 continuous monitoring of mouse homecage behaviors, including thermal imaging, video recording from above, side and directly under the nest, with environmental controls to standardize housing conditions across animals. We monitored single dams and their offspring, before, during and after parturition, from initial mating over four consecutive litters. We found that about half of the animals had high litter survival rates (‘high-pup-survival’ dams) but the other half had little to no pups survive (‘low-pup-survival’ dams). The relative amount of litter survival did not change or improve across litters in absence of intervention: Low-pup-survival dams continued to neglect pups and nest-building across litters, losing nearly all offspring within a day after birth. We could predict which animals would become low-pup-survival dams by inspecting the nests they built a few days before parturition. Low-pup-survival dams minimally engaged with nest building, and after birth, generally avoided pups and the nest. Nest quality deteriorated due to movement of the dam in and out of the nest, exacerbating temperature loss and mortality of the litter. In contrast, high-pup-survival dams spent a considerable amount of time rebuilding and adjusting the nest over the first postnatal day and beyond. Remarkably, if we co-housed low-pup-survival dams with a high-pup-survival dam and her litter, when the low-pup-survival dam was bred again and singly-housed, litter survival rates thereafter were consistently much higher along with increased attention toward pups and nest. Thus, even under well-controlled and ideal lab housing conditions, mouse maternal care can be remarkably variable, with continued nest rebuilding as the most important factor in ensuring high litter survival rates. Furthermore, despite some animals perseverating in maternal neglect and losing their pups, caretaking and nest-building can improve after interactions with experienced and successful parents.