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Pre-weaning dietary iron deficiency impairs spatial learning and memory in the cognitive holeboard task in piglets.

ABSTRACT: Iron deficiency is the most common nutritional deficiency in humans, affecting more than two billion people worldwide. Early-life iron deficiency can lead to irreversible deficits in learning and memory. The pig represents a promising model animal for studying such deficits, because of its similarities to humans during early development. We investigated the effects of pre-weaning dietary iron deficiency in piglets on growth, blood parameters, cognitive performance, and brain histology later in life. Four to six days after birth, 10 male sibling pairs of piglets were taken from 10 different sows. One piglet of each pair was given a 200 mg iron dextran injection and fed a control milk diet for 28 days (88 mg Fe/kg), whereas the other sibling was given a saline injection and fed an iron deficient (ID) milk diet (21 mg Fe/kg). Due to severely retarded growth of two of the ID piglets, only eight ID piglets were tested behaviorally. After dietary treatment, all piglets were fed a balanced commercial pig diet (190-240 mg Fe/kg). Starting at 7.5 weeks of age, piglets were tested in a spatial cognitive holeboard task. In this task, 4 of 16 holes contain a hidden food reward, allowing measurement of working (short-term) memory and reference (long-term) memory (RM) simultaneously. All piglets received 40-60 acquisition trials, followed by a 16-trial reversal phase. ID piglets showed permanently retarded growth and a strong decrease in blood iron parameters during dietary treatment. After treatment, ID piglets' blood iron values restored to normal levels. In the holeboard task, ID piglets showed impaired RM learning during acquisition and reversal. Iron staining at necropsy at 12 weeks of age showed that ID piglets had fewer iron-containing cells in hippocampal regions CA1 and dentate gyrus (DG). The number of iron-containing cells in CA3 correlated positively with the average RM score during acquisition across all animals. Our results support the hypothesis that early-life iron deficiency leads to lasting cognitive deficits. The piglet as a model animal, tested in the holeboard, can be useful in future research for assessing long-term cognitive effects of early-life diets or diet-induced deficiencies.

SUBMITTER: Antonides A

PROVIDER: S-EPMC4626557 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Pre-weaning dietary iron deficiency impairs spatial learning and memory in the cognitive holeboard task in piglets.

Antonides Alexandra A Schoonderwoerd Anne C AC Scholz Gabi G Berg Brian M BM Nordquist Rebecca E RE van der Staay Franz Josef FJ

Frontiers in behavioral neuroscience 20151030

Iron deficiency is the most common nutritional deficiency in humans, affecting more than two billion people worldwide. Early-life iron deficiency can lead to irreversible deficits in learning and memory. The pig represents a promising model animal for studying such deficits, because of its similarities to humans during early development. We investigated the effects of pre-weaning dietary iron deficiency in piglets on growth, blood parameters, cognitive performance, and brain histology later in l ...[more]

PMID: 26578919

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Project description:Early iron deficiency is associated with impaired (cognitive) development, the severity of which depends on the timing and duration of the under-supply of iron. To design effective treatment and prevention strategies for iron deficiency in humans, suited animal models are needed. In an earlier study (Antonides et al., 2015b) we separated 10 pairs of piglets from their mothers within a few days after birth and reared one sibling with artificial iron-deficient (ID) and the other with balanced control milk until weaning. ID piglets grew slower and showed poorer reference memory (RM) performance than their controls in a spatial holeboard task, even weeks after iron repletion. One putative intervening factor in that study was pre-weaning maternal deprivation. In an attempt to refine the piglet iron-deficiency model, we assessed whether piglets reared by sows, but withheld iron supplementation, can serve as animal model of iron deficiency. As sow milk is inherently ID, piglets normally receive a prophylactic iron injection. Ten pairs of piglets were housed with foster sows until weaning (4 weeks). One sibling per pair was randomly assigned to the control group (receiving iron dextran injections: 40 mg iron per kilogram body mass on days 3 and 10), the other to the ID group. From weaning, all pigs were fed a balanced commercial diet. Blood samples were taken in week 1, 3.5, 6, and 12. Pre-weaning blood iron values of ID piglets were lower than those of controls, but recovered to normal values after weaning. Hemoglobin of ID piglets did not reach anemic values. Hematocrit and hemoglobin of ID animals did not decrease, and serum iron even increased pre-weaning, suggesting that the piglets had access to an external source of iron, e.g., spilled feed or feces of the foster sows. Growth, and spatial memory assessed in the holeboard from 10 to 16 weeks of age, was unaffected in ID pigs. We conclude that sow-raised piglets are not a suitable model for iron-deficiency induced cognitive deficits in humans. Based on our previous and the present study, we conclude that growth and memory are only impaired in piglets that suffered from pre-weaning anemia.

Project description:In commercial pig farming, an increasing number of low birth weight (LBW) piglets are born, due to selection for large litter sizes. While LBW piglets have a higher risk of pre-weaning mortality, a considerable number of these piglets survive to slaughter age. In humans, LBW is a risk factor for long-term cognitive impairments. In pigs, studies examining the post-weaning effects of LBW on cognition have reported contradictory results. Therefore, the current study aimed to assess the effects of LBW on cognitive development in pigs using an improved study design, by (1) testing a larger sample size than previous studies, (2) assessing acute and chronic stress responses to account for a potential altered stress response in LBW pigs, and (3) testing both female and male pigs to account for potential confounding effects of sex. Learning and memory of 20 LBW pigs and 20 normal birth weight (NBW) pigs, both groups consisting of 10 females and 10 males, were compared using a spatial holeboard task. In this task, pigs had to learn and remember the locations of hidden food rewards. After a pig had successfully acquired the task, it was presented with two successive reversal phases during which it was presented with a new configuration of reward locations. The holeboard allows for simultaneous assessment of working and reference memory, as well as measures of motivation, exploration, and behavioral flexibility. Mixed model ANOVAs revealed a transiently impaired reference memory performance of LBW pigs, implying they had more difficulty learning their reward configuration in the holeboard. Also, LBW piglets showed increased pre-weaning hair cortisol concentrations compared to their NBW siblings. No other effects of LBW were found. Sex had no direct or interaction effects on any measures of holeboard performance or stress. It is possible that the enriched housing conditions applied during our study had an ameliorating effect on our pigs' cognitive development. Overall, our results suggest LBW has a negative effect on post-weaning cognitive performance in pigs. This could have welfare consequences as cognitive skills are required for pigs to learn how to correctly respond to their environment.

Project description:The present study was conducted to evaluate the effect of dietary folic acid on the growth performance, intestinal morphology, and intestinal epithelial cells renewal in post-weaning piglets. Twenty-eight piglets (weaned at day 21, initial body weight of 6.73 ± 0.62 kg) were randomly allotted to 4 treatments with 7 pens per diet and 1 piglet per pen. The piglets were fed the same antibiotic-free and zinc oxide-free basal diets supplemented with folic acid at 0, 3, 9, and 18 mg/kg for 14 days. The results showed that dietary supplementation with folic acid increased villus height (VH) (P = 0.003; linear, P = 0.001), VH-to-crypt depth (VH:CD) ratio (P = 0.002; linear, P = 0.001), villus surface area (VSA) (P = 0.026; linear, P = 0.010). The analyzed parameters ADG, serum urea nitrogen (BUN) content, VH, VSA, and serum folate (SF) concentration responded linearly to the dietary folic acid concentration when the dietary folic acid concentration was below 4.42, 5.26, 4.79, 3.47, and 3.53 mg/kg respectively (R 2 = 0.995, 0.995, 0.999, 0.999, 0.872, P = 0.09, 0.07, 0.09, 0.09, 0.36, respectively), as assessed by a two-linear broken-line regression. Above these breakpoints, the response of ADG, VH, VSA, and SF plateaued in response to changes in dietary folic acid concentration. Moreover, dietary supplementation with folic acid significantly increased the lactase (P = 0.001; linear, P = 0.001) and sucrase activities (P = 0.021; linear, P = 0.010) in the jejunal mucosa of weaned piglets. The mRNA expression of solute carrier family 6 member 19 (SLC6a19), solute carrier family 1 member 1 (SLC7a1), tumor necrosis factor-α (TNF-α), the number of Ki67 positive cells, and cell shedding rate had a significant linear contrast (P = 0.023, 0.021, 0.038, 0.049, and 0.008, respectively) in dietary folic acid groups. In conclusion, our results indicate that folic acid supplementation can improve the growth performance and intestinal morphology of weaned piglets by maintaining the balance of epithelial cell renewal.

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Pre-weaning dietary iron deficiency impairs spatial learning and memory in the cognitive holeboard task in piglets.

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Pre-weaning dietary iron deficiency impairs spatial learning and memory in the cognitive holeboard task in piglets.

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