Prenatal, but not early postnatal, exposure to a Western diet improves spatial memory of pigs later in life and is paired with changes in maternal prepartum blood lipid levels

Abstract

Maternal obesity and perinatal high‐fat diets are known to affect cognitive development. We examined the effects of late prenatal and/or early postnatal exposure to a Western‐type diet, high in both fat and refined sugar, on the cognition of pigs (Sus scrofa) in the absence of obesity. Thirty‐six sows and their offspring were assigned to 1 of 4 treatments in a 2 × 2 factorial arrangement, with 8 wk prenatal and 8 wk postnatal exposure to a Western diet (enriched in fat, sucrose, and cholesterol) or control diets as factors. Compared to controls, piglets exposed to the prenatal Western diet showed enhanced working and reference memory during the acquisition and reversal phases of a spatial hole‐board task. Mothers fed the prenatal Western diet had higher prepartum blood cholesterol and free fatty acid levels. Postnatal exposure to the Western diet did not affect piglet cognitive performance, but it did increase postpartum maternal and postweaning piglet cholesterol levels. The Western diet had no effect on maternal or offspring insulin sensitivity or leptin levels. In conclusion, a prenatal Western diet improved memory function in pigs, which was paired with changes in prepartum maternal blood cholesterol levels. These findings highlight the key role of late fetal nutrition for long‐term programming of cognition.—Clouard, C., Kemp, B., Val‐Laillet, D., Gerrits, W. J. J., Bartels, A. C., Bolhuis, J. E. Prenatal, but not early postnatal, exposure to a Western diet improves spatial memory of pigs later in life and is paired with changes in maternal prepartum blood lipid levels. FASEB J. 30, 2466‐2475 (2016). http://www.fasebj.org

A maternal Western diet during gestation and lactation modifies offspring's microbiota activity, blood lipid levels, cognitive responses, and hippocampal neurogenesis in Yucatan pigs

“…Lipid profiles were significantly modified in WD sows, with a notably gradual increase in the plasma FFA and total cholesterol levels during gestation and until the end of lactation, suggesting that WD fetuses received more fat than SD fetuses via the placenta. This finding is consistent with the study from Clouard et al (16), who reported that the improved performance in a cognitive holeboard task of piglets born from sows fed a WD during gestation was also paired with changes in maternal blood lipid (FFA, cholesterol, HDL-C) levels before parturition. The fatty acid mix delivered to the fetus is largely determined by the fatty acid composition of the maternal blood (45) and pig placental trophoblast cells express numerous genes for micronutrient-and nutrient-transport proteins, including proteins for lipid transport (46).…”

“…Finally, it is important to state that the holeboard test has never been performed in piglets this young. Gieling et al (23) has already tested 9-wk-old piglets, whereas ours were only 4 wk old at the beginning of the tests, which probably explains their overall low success in comparison to the animals in published studies (16,(40)(41)(42).…”

“…Surprisingly, SD piglets did not even improve their reference memory over time, suggesting either lower adaptive capabilities or little motivation for the test compared to WD piglets. In line with the first explanation, Clouard et al (16) recently reported that, compared to offspring of sows on a control diet, offspring of sows fed a high‐fat/high‐sugar diet during the 8 last weeks of pregnancy showed enhanced working and reference memory, without signs of a higher motivation, during the acquisition and reversal phases of a similar spatial holeboard task. The second explanation ( i.e.…”

“…The lack of a clear detrimental effect of a maternal WD on cognitive performance in the offspring contradictory of result in most of the studies that assessed the impact of a WD on cognitive abilities (11, 24), except for the study from Clouard et al (16). For example, Tozuka et al (11) demonstrated in mice that maternal obesity induced by a high‐fat diet decreased hippocampal‐dependent learning performance in the offspring subjected to the Barnes maze test.…”

A Review of the Impact of Maternal Obesity on the Cognitive Function and Mental Health of the Offspring

“…Bilbo and Tsang [28] reported that young adult male and female rats born to dams fed a diet high in either saturated or trans fats performed significantly better on the Morris water maze task compared to control rats. Better spatial memory performance was also observed in three-month old offspring born to obese Peromyscus mouse dams [40], as well as in 11–15-week old piglets exposed to a high fat diet either during the prenatal or pre- and post-natal periods [41,42]. However, another study found that spatial memory performance in the Barnes maze was decreased in 4- and 10-week old male offspring of obese mothers compared to those born to lean mothers [43].…”