Influence of Rearing Environment on Longitudinal Brain Development, Object Recognition Memory, and Exploratory Behaviors in the Domestic Pig (Sus scrofa)

INTRODUCTION: Over the last 40 years, the domestic pig has emerged as a prominent preclinical model as this species shares similarities with humans with regard to immunity, gastrointestinal physiology, and neurodevelopment. Artificial rearing of pigs provides a number of advantages over conventional rearing (i.e., true maternal care), including careful control of nutrient intake and environment conditions. Yet there remains a gap in knowledge when comparing brain development between sow-reared and artificially reared domestic pigs. Thus, our research sought to model brain development and assess recognition memory in a longitudinal manner by directly comparing rearing environments. METHODS: Forty-four intact (i.e., not castrated) male pigs were artificially reared or sow-reared from postnatal day 2 until postnatal week 4. After postnatal week 4, all pigs were housed in a group setting within the same environment until postnatal week 24. Magnetic resonance imaging was conducted on pigs at 8 longitudinal time-points to model developmental trajectories of brain macrostructural and microstructural outcomes. Additionally, pigs behavior were tested using the novel object recognition task at postnatal weeks 4 and 8. RESULTS: Throughout the 24-week study, no differences between rearing groups were noted in weekly body weights, average growth and feed intake patterns, or feed efficiency. Whole brain, gray matter, white matter, and cerebrospinal fluid growth patterns also did not differ between pigs assigned to different early-life rearing environments. Moreover, minimal differences in regional absolute volumes and fractional anisotropy developmental trajectories were identified, though artificially reared pigs exhibited higher initial rates of myelination in multiple brain regions compared with sow-reared pigs. Furthermore, behavioral assessment at both PNW 4 and 8 suggested little influence of rearing environment on recognition memory, however, an age-dependent increase in object recognition memory was observed in the sow-reared group. CONCLUSION: Our findings suggest that early-life rearing environment influences the rate of development in some brain regions but has little influence on overall brain growth and object recognition memory and exploratory behaviors in the domestic pig. Artificial rearing may promote maturation in certain brain areas but does not appear to elicit long-term effects in outcomes including brain structure or object recognition memory.