Early postnatal environmental enrichment restores neurochemical and functional plasticities of the cerebral cortex and improves learning performance in hidden-prenatally-malnourished young-adult rats

Burgos, Héctor; Hernández, Alejandro; Constandil, Luís; Rı́os, Miguel A.; Flores, Osvaldo; Puentes, Gustavo Cortés; Hernández, Karina; Morgan, Carlos; Valladares, Luis; Castillo, Amparo; Cofré, Cristian; Milla, Luis A.; Sáez-Briones, Patricio; Barra, Rafael

doi:10.1016/j.bbr.2019.02.001

Cited by 11 publications

(4 citation statements)

References 51 publications

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“…Maternal malnutrition can alter the trajectory of fetal neurodevelopment to result in long-term changes in brain function and behavior [19][20][21][22] . To uncover mechanisms by which maternal protein undernutrition programs adverse behavioral outcomes in the offspring, we first examined the effects of maternal PR on E18.5 fetal brains by transcriptomic profiling.…”

Section: Maternal Protein Restriction Alters Functional Signatures In...mentioning

confidence: 99%

“…Brain abnormalities, such as cerebral atrophy, ventricular dilation, and myelin-related deficits, are seen in protein malnourished infants as young as 3 months of age and through 36 months of age 17,18 , highlighting an early critical period during which protein undernutrition impairs neurodevelopment. In animal models, restricting protein intake particularly during pregnancy yields persistent neurological and neurobehavioral impairments in the offspring, including abnormalities in neuronal proliferation and apoptosis 19 , neocortical activity 20 , hippocampal morphology 21 , learning and memory, and anxiety-like behaviors [19][20][21][22] . These results indicate that adverse neurological consequences of protein undernutrition can originate from gestational influences 23 .…”

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confidence: 99%

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The maternal microbiome modifies adverse effects of protein undernutrition on offspring neurobehavioral impairment in mice

Coley-O’Rourke,

Lum,

Pronovost

et al. 2024

Preprint

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Protein undernutrition is a global risk factor for impaired growth and neurobehavioral development in children. However, the critical periods, environmental interactions, and maternal versus neonatal influences on programming lasting behavioral abnormalities are poorly understood. In a mouse model of fetal growth restriction, limiting maternal protein intake particularly during pregnancy leads to cognitive and anxiety-like behavioral abnormalities in adult offspring, indicating a critical role for the gestational period. By cross-fostering newborn mice to dams previously exposed to either low protein or standard diet, we find that the adult behavioral impairments require diet-induced conditioning of both fetal development and maternal peripartum physiology, rather than either alone. This suggests that protein undernutrition during pregnancy directly disrupts fetal neurodevelopment and indirectly alters maternal state in ways that interact postnatally to precipitate behavioral deficits. Consistent with this, maternal protein restriction during pregnancy reduces the diversity of the maternal gut microbiome, modulates maternal serum metabolomic profiles, and yields widespread alterations in fetal brain transcriptomic and metabolomic profiles, including subsets of microbiome-dependent metabolites. Depletion of the maternal microbiome in protein-restricted dams further alters fetal brain gene expression and exacerbates neurocognitive behavior in adult offspring, suggesting that the maternal microbiome modifies the impact of gestational protein undernutrition on risk for neurobehavioral impairment in the offspring. To explore the potential for microbiome-targeted interventions, we find that maternal treatment with short chain fatty acids or a cocktail of 10 diet- and microbiome-dependent metabolites each yield differential effects on fetal development and/or postnatal behavior. Results from this study highlight impactful prenatal influences of maternal protein undernutrition on fetal neurodevelopment and adverse neurobehavioral trajectories in offspring, which are mitigated by microbiome-targeted interventions during pregnancy.

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Section: Maternal Protein Restriction Alters Functional Signatures In...mentioning

confidence: 99%

mentioning

confidence: 99%

The maternal microbiome modifies adverse effects of protein undernutrition on offspring neurobehavioral impairment in mice

Coley-O’Rourke,

Lum,

Pronovost

et al. 2024

Preprint

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“…Some studies have revealed that a protein-enriched diet increased BDNF concentrations in the serum of the elderly population 29 and BDNF production in the brains of young mice. 30 The activation of dopaminergic nerves promotes the expression of BDNF in the brain. [31][32][33] Food & Function Paper activated the cAMP-PKA-CREB signalling pathway through the DRD1, thereby promoting the synthesis of BDNF in neurons.…”

Section: Papermentioning

confidence: 99%

Duodenal infusion of soy protein hydrolysate activates cAMP signaling and hypothalamic neurotransmitter synthesis in pigs

Ding

et al. 2022

Food Funct.

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“…It has been revealed that an enriched environment (EE) is a non‐pharmacological intervention that can excite brain plasticity (Rojas et al, 2013), synaptogenesis (Kondo et al, 2012), neurogenesis (Rizzi et al, 2011), and protect CNS in both normal and brain‐damaged animals (Burgos et al, 2019; Miller et al, 2013). Housing in EEs can also up‐regulate BDNF expression that facilitates plasticity of the CNS and improves cognitive performances for instance learning and memory (Novkovic et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Beneficial effects of enriched environment on behavior, cognitive functions, and hippocampal brain‐derived neurotrophic factor level following postnatal serotonin depletion in male rats

Saadati

Ghaheri

Sadegzadeh

et al. 2022

Intl J of Devlp Neuroscience

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The neurotransmitter serotonin (5‐HT) is one of the most important modulators of neural circuitry and has a critical role in neural development and functions. Previous studies indicated that changes in serotonergic system signaling in early life critically impact mental health, behavior, the morphology of hippocampal neurons, and cognitive functions across the lifespan. The enriched environment (EE) has indicated beneficial effects on behavior and cognitive functions in the developmental period of life, but its impacts on cognitive impairments and behavioral changes following postnatal serotonin depletion are unknown. Therefore, the present study aimed to evaluate the influences of the EE housing (postnatal days [PNDs] 21–60) following postnatal serotonin depletion (by para‐chlorophenylalanine [PCPA], 100 mg/kg, s.c, in PNDs 10–20) on anxiety‐related behaviors, cognitive functions, and brain‐derived neurotrophic factor (BDNF) mRNA expression in the hippocampus of male rats. Memory and behavioral parameters were examined in early adulthood and after that, the hippocampi of rats were removed to determine the BDNF mRNA expression by PCR (PNDs 60–70). The findings of the present work indicated that adolescent EE exposure alleviated memory impairment, decreased BDNF levels, and anxiety disorders induced by experimental depletion of serotonin. Overall, these results indicate that serotonergic system dysregulation during the developmental periods can be alleviated by adolescent EE exposure.

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Early postnatal environmental enrichment restores neurochemical and functional plasticities of the cerebral cortex and improves learning performance in hidden-prenatally-malnourished young-adult rats

Cited by 11 publications

References 51 publications

The maternal microbiome modifies adverse effects of protein undernutrition on offspring neurobehavioral impairment in mice

The maternal microbiome modifies adverse effects of protein undernutrition on offspring neurobehavioral impairment in mice

Duodenal infusion of soy protein hydrolysate activates cAMP signaling and hypothalamic neurotransmitter synthesis in pigs

Beneficial effects of enriched environment on behavior, cognitive functions, and hippocampal brain‐derived neurotrophic factor level following postnatal serotonin depletion in male rats

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