Disruption of behavior and brain metabolism in artificially reared rats

Aguirre-Benítez, Elsa Liliana; Porras, Mercedes G.; Parra, Leticia; González-Ríos, Jacquelina; Garduño-Torres, Dafne F.; Albores-García, Damaris; Avendaño, Arturo; Ávila‐Rodríguez, Miguel A.; Melo, Angel I.; Jiménez‐Estrada, Ismael; Mendoza-Garrido, Ma. Eugenia; Toriz, Cesar G.; Díaz, Daniel; Ibarra-Coronado, Elizabeth; Mendoza-Ángeles, Karina; Hernández‐Falcón, Jesús

doi:10.1002/dneu.22548

Cited by 13 publications

(8 citation statements)

References 91 publications

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“…However, since non-supplemented animals successfully completed the cliff avoidance test on day 5, which is the cannulation day and first day of feeding, it is questionable whether differences in maturation age across groups for cliff avoidance are explained by diet. Additionally, artificially-reared pups might be more acclimatized to human handling, more adaptive to environments outside the dam cages, and may be less fearful in exploring the cliff avoidance test area 31 , 32 . Findings from the collective assessment of reflexes in this study highlight that effects of MFGM on reflex development are not comprehensive (not for all reflexes) and more research is needed to determine what the functional implications of the significant differences are for brain function.…”

Section: Discussionmentioning

confidence: 99%

Milk Fat Globule Membrane Supplementation in Formula-fed Rat Pups Improves Reflex Development and May Alter Brain Lipid Composition

Moukarzel

Dyer

Garcia

et al. 2018

Sci Rep

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Human milk contains nutritional, immunoprotective and developmental components that support optimal infant growth and development. The milk fat globule membrane (MFGM) is one unique component, comprised of a tri-layer of polar lipids, glycolipids, and proteins, that may be important for brain development. MFGM is not present in most infant formulas. We tested the effects of bovine MFGM supplementation on reflex development and on brain lipid and metabolite composition in rats using the “pup in a cup” model. From postnatal d5 to d18, rats received either formula supplemented with MFGM or a standard formula without MFGM; a group of mother-reared animals was used as reference/control condition. Body and brain weights did not differ between groups. MFGM supplementation reduced the gap in maturation age between mother-reared and standard formula-fed groups for the ear and eyelid twitch, negative geotaxis and cliff avoidance reflexes. Statistically significant differences in brain phospholipid and metabolite composition were found at d13 and/or d18 between mother-reared and standard formula-fed groups, including a higher phosphatidylcholine:phosphatidylethanolamine ratio, and higher phosphatidylserine, glycerol-3 phosphate, and glutamine in mother-reared compared to formula-fed pups. Adding MFGM to formula narrowed these differences. Our study demonstrates that addition of bovine MFGM to formula promotes reflex development and alters brain phospholipid and metabolite composition. Changes in brain lipid metabolism and their potential functional implications for neurodevelopment need to be further investigated in future studies.

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Section: Discussionmentioning

confidence: 99%

Milk Fat Globule Membrane Supplementation in Formula-fed Rat Pups Improves Reflex Development and May Alter Brain Lipid Composition

Moukarzel

Dyer

Garcia

et al. 2018

Sci Rep

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“…In another study, acceleration of some developmental reflexes has been observed in rats artificially reared with a milk replacer supplemented with MFGM, suggesting a beneficial effect of MFGM during post-natal neurodevelopment ( 17 ). To note, artificial rearing methods have been shown to be associated with negative impact on the maturation of physiological functions, including anxiety-like behavior ( 44 ) and changes in brain metabolism ( 45 ). This suggests that the observed benefits following MFGM supplementation in artificially reared rodents could be specific to the experimental model.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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Early life nutrition critically impacts post-natal brain maturation and cognitive development. Post-natal dietary deficits in specific nutrients, such as lipids, minerals or vitamins are associated with brain maturation and cognitive impairments. Specifically, polar lipids (PL), such as sphingolipids and phospholipids, are important cellular membrane building blocks and are critical for brain connectivity due to their role in neurite outgrowth, synaptic formation, and myelination. In this preclinical study, we assessed the effects of a chronic supplementation with a source of PL extracted from an alpha-lactalbumin enriched whey protein containing 10% lipids from early life (post-natal day (PND) 7) to adulthood (PND 72) on adult motor skills, anxiety, and long-term memory. The motor skills were assessed using open field and rotarod test. Anxiety was assessed using elevated plus maze (EPM). Long-term object and spatial memory were assessed using novel object recognition (NOR) and Morris water maze (MWM). Our results suggest that chronic PL supplementation improved measures of spatial long-term memory accuracy and cognitive flexibility in the MWM in adulthood, with no change in general mobility, anxiety and exploratory behavior. Our results indicate memory specific functional benefits of long-term dietary PL during post-natal brain development.

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“…During the breeding process the MR pups and their foster dams were housed in clear Plexiglas cages (30 × 15 × 14 cm), with Purina Rat Chow and water available ad libitum, and left undisturbed except during bedding and cage change. For the AR group, the pups were selected randomly for artificial reared subject to a surgery, which consists in the implantation of a cannula through the cheek where milk is supplied [28, 30]. The surgery was performed according to previous works [27, 31].…”

Section: Methodsmentioning

confidence: 99%

“…In the artificial rearing procedure (AR), the pup is deprived of the mother-pup interaction and the breast milk, and it is fed with a rat formula milk throughout the lactation period [26]. This procedure has been used to analyse the effects of maternal deprivation over social behaviour in rats [27, 28]. However, no studies have been performed analysing the endocrine system, specifically the GH in AR animals, especially because GH serum concentration is considered to be regulated by maternal-pup interaction and by the energy metabolism requirements during the different stages before weaning.…”

Section: Introductionmentioning

confidence: 99%

Physiological changes of growth hormone during lactation in pup rats artificially reared

et al. 2019

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During the lactation period, rat pups are fed by the dam, and the patterns of mother-pup interaction change during this period. Additionally, there are changes in feeding; first, mother´s milk is the only food needed for sustenance, and later, it is combined with solid food and water. GH serum concentrations depend on both maternal-pup interaction and energy metabolism. In the artificial rearing (AR) procedure, pups are deprived of mother-pup interaction, and the feeding pattern is controlled. This rearing paradigm has been used in rats to analyze the effects of maternal deprivation on social behavior. In the present study, we analyzed the variation in GH, acylated ghrelin and IGF-1 serum concentrations throughout the lactation period in AR pups. At pnd7, the maternal rearing (MR) pups responded to a 4 h fast with a drop in GH serum concentration, which is a well-known response to maternal deprivation. GH serum levels in the AR pups did not change, suggesting an adaptation phenomenon. A dopamine inhibitory effect of GH secretion was observed in pnd7 cultured somatotropes, suggesting dopamine regulation of GH secretion at this age. Acylated ghrelin serum levels in the AR pups showed an inverted pattern compared to that in the MR pups, which was related to the artificial feeding pattern. IGF-1 serum levels were lower in the AR pups than in MR pups, which was associated with hepatic GH resistance and with low Igf1 mRNA expression at pnd7. Interestingly, at pnd14, both pup groups showed high hepatic Igf1 mRNA expression but low IGF-1 serum levels, and this was inverted at pnd21. However, serum glucose levels were lower in the AR pups at pnd14 but reached the same levels as the MR pups at pnd21. Moreover, hepatomegaly and higher hepatic GH-receptor levels were observed in the AR pups at pnd21, which was in agreement with an absence of a solid food meal. During AR, the pups lost the maternal interaction-stimulated GH secretion, which correlated with lower IGF-1 serum levels during the first week of postnatal development. Later, the AR pups exhibited hepatic responses, in order to satisfy the metabolic demand for the normal weaning, with low carbohydrates levels in their meal.

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Disruption of behavior and brain metabolism in artificially reared rats

Cited by 13 publications

References 91 publications

Milk Fat Globule Membrane Supplementation in Formula-fed Rat Pups Improves Reflex Development and May Alter Brain Lipid Composition

Milk Fat Globule Membrane Supplementation in Formula-fed Rat Pups Improves Reflex Development and May Alter Brain Lipid Composition

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

Physiological changes of growth hormone during lactation in pup rats artificially reared

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