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

Abstract

IntroductionOver 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.MethodsForty-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.ResultsThroughout 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.ConclusionOur 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.

Influence of Dietary Polar Lipid Supplementation on Memory and Longitudinal Brain Development

“…The multicomponent driven equilibrium single pulse observation of T 1 and T 2 technique was used to measure myelin-associated water fraction (MWF). Imaging techniques are similar to those discussed previously [ 31 ] and are described in greater detail below.…”

“…Novel object recognition (NOR) is a behavioral paradigm used to assess recognition memory as a primary indicator of cognitive behavior of the pig, as described in detail previously [ 31 , 35 ]. Testing consisted of a habituation phase, a sample phase, and a test phase, with a delay period between the sample and test phases.…”

“…The BIC is a criterion for model selection where the lowest BIC is preferred because unexplained variation in the dependent variable, and the number of explanatory variables increase the value of BIC [ 42 ]. The Gompertz was chosen as the best model to use for absolute volumes, FA, and MWF data because it had the best Bayesian information criterion value, a criterion for model selection, across all brain regions using the highest ranked sum for those specific data, as discussed previously [ 31 ].…”

Effects of Post-natal Dietary Milk Fat Globule Membrane Polar Lipid Supplementation on Motor Skills, Anxiety, and Long-Term Memory in Adulthood

“…This suggests that the observed benefits following MFGM supplementation in artificially reared rodents could be specific to the experimental model. On the contrary, in young pigs, artificial rearing has been shown not to elicit detrimental effects on brain development and behavior ( 46 ). In a study assessing the effect of a supplementation with phospholipids and gangliosides during the neonatal period, better performance in a spatial T-Maze task was observed in supplemented piglets ( 47 ).…”

Epigenetic MRI: Noninvasive Imaging of DNA Methylation in the Brain

“…Pigs were maintained at PNCL through PND 32 per standard protocols as described elsewhere with the following modifications. All pigs were provided ad libitum access to water and a custom, nutritionally complete 50 milk replacer formula (TestDiet) via a semi-automated liquid delivery system that dispensed milk from 1000 to 0600 h the next day 51 . The milk replacer powder was formulated to contain 30.4% lactose, 30.3% stabilized lipids (i.e., dried fat; combination of lipid sources including sunflower oil, palm oil, and medium-chain triglycerides), and 25.4% purified amino acids; no intact protein was included in this formulation.…”