The Effects of Human Milk Oligosaccharide Supplementation During Critical Periods of Development on the Mesolimbic Dopamine System

Tuplin, Erin W. Noye; Chleilat, Faye; Alukic, Erna; Reimer, Raylene A.

doi:10.1016/j.neuroscience.2021.02.006

Cited by 10 publications

(5 citation statements)

References 54 publications

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“…One study tested the effects of combined SL and FL supplementation on the mesolimbic dopamine system in rats. The results showed that the HMOS supplementation exerted sex-dependent effects; 3 -SL + 2 -FL fortification decreased dopamine transporter expression in the ventral tegmental area and increased leptin expression in the nucleus accumbens in females only [62]. This study not only highlighted the impact of HMOS supplementation on the dopamine system but suggested for the first time that variations in response to the HMOS supplementation may be sex-dependent [62].…”

Section: Rodent Modelsmentioning

confidence: 68%

“…Fucosylated HMOS, especially 2 -FL, are usually the most abundant HMOS in secretor mothers [98]. Many studies included in this review supported the role of 2 -FL and fucosylated HMOS in learning and memory formation processes [53,[59][60][61][62]66,67]. This may be explained by the neuroprotective effects of 2 -FL in animal models [99,100], although the exact mechanism for this effect is unclear.…”

Section: Fucosylated Mos and Cognitionmentioning

confidence: 68%

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Review on the Impact of Milk Oligosaccharides on the Brain and Neurocognitive Development in Early Life

Fan,

McMath,

Donovan

2023

Nutrients

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Milk Oligosaccharides (MOS), a group of complex carbohydrates found in human and bovine milk, have emerged as potential modulators of optimal brain development for early life. This review provides a comprehensive investigation of the impact of milk oligosaccharides on brain and neurocognitive development of early life by synthesizing current literature from preclinical models and human observational studies. The literature search was conducted in the PubMed search engine, and the inclusion eligibility was evaluated by three reviewers. Overall, we identified 26 articles for analysis. While the literature supports the crucial roles of fucosylated and sialylated milk oligosaccharides in learning, memory, executive functioning, and brain structural development, limitations were identified. In preclinical models, the supplementation of only the most abundant MOS might overlook the complexity of naturally occurring MOS compositions. Similarly, accurately quantifying MOS intake in human studies is challenging due to potential confounding effects such as formula feeding. Mechanistically, MOS is thought to impact neurodevelopment through modulation of the microbiota and enhancement of neuronal signaling. However, further advancement in our understanding necessitates clinical randomized-controlled trials to elucidate the specific mechanisms and long-term implications of milk oligosaccharides exposure. Understanding the interplay between milk oligosaccharides and cognition may contribute to early nutrition strategies for optimal cognitive outcomes in children.

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Section: Rodent Modelsmentioning

confidence: 68%

Section: Fucosylated Mos and Cognitionmentioning

confidence: 68%

Review on the Impact of Milk Oligosaccharides on the Brain and Neurocognitive Development in Early Life

Fan,

McMath,

Donovan

2023

Nutrients

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“…Sex differences in gut microbiota-manipulated animals during DA system critical development periods have been reported recently by Noye Tuplin et al ( 2021), where they supplemented 21-days old rats with maternal milk oligosaccharides, which are known to regulate infant's gut microbiota during lactation period and are considered as prebiotics. They found that oligosaccharide-supplemented females displayed lower levels of DAT mRNA in VTA, and lower D 2 mRNA expression in NAcc (Noye Tuplin et al, 2021), suggesting that gut microbiota manipulation during the mesolimbic development period alters the resulting adult dopaminergic system differentially according to sex. Taken together, these results suggest that gut microbiota composition regulates protein expression within the dopaminergic reward system during critical developmental periods, and that sex is an important factor to determine how these regulations occur.…”

Section: Discussionmentioning

confidence: 99%

“…Early-life exposure to broad-range non-absorbable antibiotics has been previously shown to decrease diversity and richness of gut microbiota in adult rodents ( Clarke et al, 2014 ; O'Mahony et al, 2014 ), suggesting that perinatal exposure to antibiotics alters gut microbiota composition in adulthood. Additionally, these findings showed that reducing the diversity and richness of gut microbiota during key stages of development, results in different metabolic and neuronal alterations ( Clarke et al, 2014 ; O'Mahony et al, 2014 ; Mueller et al, 2015 ; Codagnone et al, 2018 ; Noye Tuplin et al, 2021 ), which could also be affecting the neurodevelopment and function of the NAcc and, possibly, of the whole dopaminergic reward system impacting drug response.…”

Section: Discussionmentioning

confidence: 99%

Early-Life Exposure to Non-Absorbable Broad-Spectrum Antibiotics Affects the Dopamine Mesocorticolimbic Pathway of Adult Rats in a Sex-Dependent Manner

González-Arancibia

Collio²,

Silva-Olivares³

et al. 2022

Front. Pharmacol.

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Gut microbiota with a stable, rich, and diverse composition is associated with adequate postnatal brain development. Colonization of the infant’s gut begins at birth when parturition exposes the newborn to a set of maternal bacteria, increasing richness and diversity until one to two first years of age when a microbiota composition is stable until old age. Conversely, alterations in gut microbiota by diet, stress, infection, and antibiotic exposure have been associated with several pathologies, including metabolic and neuropsychiatric diseases such as obesity, anxiety, depression, and drug addiction, among others. However, the consequences of early-life exposure to antibiotics (ELEA) on the dopamine (DA) mesocorticolimbic circuit are poorly studied. In this context, we administered oral non-absorbable broad-spectrum antibiotics to pregnant Sprague-Dawley dams during the perinatal period (from embryonic day 18 until postnatal day 7) and investigated their adult offspring (postnatal day 60) to assess methylphenidate-induced conditioned place preference (CPP) and locomotor activity, DA release, DA and 3,4-dihydroxyphenylacetic acid (DOPAC) content in ventral tegmental area (VTA), and expression of key proteins within the mesocorticolimbic system. Our results show that ELEA affect the rats conduct by increasing drug-seeking behavior and locomotor activity induced by methylphenidate of males and females, respectively, while reducing dopamine striatal release and VTA content of DOPAC in females. In addition, antibiotics increased protein levels of DA type 1 receptor in prefrontal cortex and VTA of female rats, and tyrosine hydroxylase in VTA of adult male and female rats. Altogether, these results suggest that ELEA alters the development of the microbiota-gut-brain axis affecting the reward system and the response to abuse drugs in adulthood.

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“…By contrast, STAT3-deficient mice have reduced mesolimbic dopamine function, requiring more stimulation to achieve a similar food-related reward [250]. Administration of prebiotics promotes an increased leptin expression in the nucleus accumbens with reduced DAT expression in the VTA [251]. Bariatric surgery decreases leptin, an effect associated with microbiota metabolites and improvements in microbial composition [252].…”

Section: Bariatric Surgery Gut Microbiota Dopamine and Gut Hormonesmentioning

confidence: 99%

Influence of Bariatric Surgery on Gut Microbiota Composition and Its Implication on Brain and Peripheral Targets

Hamamah,

Hajnal,

Covasa

2024

Nutrients

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Obesity remains a significant global health challenge, with bariatric surgery remaining as one of the most effective treatments for severe obesity and its related comorbidities. This review highlights the multifaceted impact of bariatric surgery beyond mere physical restriction or nutrient malabsorption, underscoring the importance of the gut microbiome and neurohormonal signals in mediating the profound effects on weight loss and behavior modification. The various bariatric surgery procedures, such as Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG), act through distinct mechanisms to alter the gut microbiome, subsequently impacting metabolic health, energy balance, and food reward behaviors. Emerging evidence has shown that bariatric surgery induces profound changes in the composition of the gut microbiome, notably altering the Firmicutes/Bacteroidetes ratio and enhancing populations of beneficial bacteria such as Akkermansia. These microbiota shifts have far-reaching effects beyond gut health, influencing dopamine-mediated reward pathways in the brain and modulating the secretion and action of key gut hormones including ghrelin, leptin, GLP-1, PYY, and CCK. The resultant changes in dopamine signaling and hormone levels contribute to reduced hedonic eating, enhanced satiety, and improved metabolic outcomes. Further, post-bariatric surgical effects on satiation targets are in part mediated by metabolic byproducts of gut microbiota like short-chain fatty acids (SCFAs) and bile acids, which play a pivotal role in modulating metabolism and energy expenditure and reducing obesity-associated inflammation, as well as influencing food reward pathways, potentially contributing to the regulation of body weight and reduction in hedonic eating behaviors. Overall, a better understanding of these mechanisms opens the door to developing non-surgical interventions that replicate the beneficial effects of bariatric surgery on the gut microbiome, dopamine signaling, and gut hormone regulation, offering new avenues for obesity treatment.

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The Effects of Human Milk Oligosaccharide Supplementation During Critical Periods of Development on the Mesolimbic Dopamine System

Cited by 10 publications

References 54 publications

Review on the Impact of Milk Oligosaccharides on the Brain and Neurocognitive Development in Early Life

Review on the Impact of Milk Oligosaccharides on the Brain and Neurocognitive Development in Early Life

Early-Life Exposure to Non-Absorbable Broad-Spectrum Antibiotics Affects the Dopamine Mesocorticolimbic Pathway of Adult Rats in a Sex-Dependent Manner

Influence of Bariatric Surgery on Gut Microbiota Composition and Its Implication on Brain and Peripheral Targets

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