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Associations among rearing environment and the infant gut microbiome with early-life neurodevelopment and cognitive
Katherine Daiy1, Kyle Wiley2, Jacob Allen3
1Department of Anthropology, Yale University, New Haven, CT, USA.
Insights
Early gut microbiome and social environment impact infant brain development. Nursery-reared infants showed lower emotional responsivity, linked to specific gut bacteria patterns and diversity.
Area of Science:
- Neuroscience
- Microbiology
- Developmental Psychology
Background:
- Early life experiences, including the gut microbiome and social environment, are critical for neurodevelopment.
- The interplay between the gut microbiome and social rearing conditions in shaping infant cognitive and behavioral outcomes remains incompletely understood.
Purpose of the Study:
- To investigate the association between the gut microbiome, social environments, and neurodevelopmental and cognitive outcomes in infant nonhuman primates.
- To identify specific gut microbial patterns and diversity metrics linked to infant temperament and cognitive functions.
Main Methods:
- Utilized a nonhuman primate model (Macaca mulatta) with distinct rearing conditions: mother-peer-reared (MPR) and nursery-reared (NR).
- Assessed neurodevelopment (emotional responsivity, visual orientation, motor maturity) using the Primate Neonatal Neurobehavioral Assessment (PNNA) and cognitive function (reward association, cognitive flexibility, impulsivity).
- Quantified fecal microbiome via 16S rRNA sequencing, analyzed microbial co-abundance factors, and employed multiple linear regressions and differential abundance analysis (MaAsLin2).
Main Results:
- A gut microbiome pattern characterized by high Prevotella and Lactobacillus abundance was negatively associated with infant emotional responsivity.
- Lower gut microbiome alpha diversity (Shannon diversity) was also negatively associated with emotional responsivity at 30 days of age.
- Nursery-rearing (NR) was independently associated with lower emotional responsivity compared to mother-peer-rearing (MPR).
Conclusions:
- The infant gut microbiome composition and diversity are associated with early neurodevelopmental outcomes, particularly emotional responsivity.
- Early-rearing environments significantly influence both the gut microbiome and neurobehavioral development.
- Findings suggest a complex interaction between the gut microbiome and social experiences in shaping infant temperament and cognitive development.
Abstract:
Early gut microbiome development may impact brain and behavioral development. Using a nonhuman primate model (Macaca mulatta), we investigated the association between social environments and the gut microbiome on infant neurodevelopment and cognitive function. Infant rhesus monkeys (n = 33) were either mother-peer-reared (MPR) or nursery-reared (NR). Neurodevelopmental outcomes, namely emotional responsivity, visual orientation, and motor maturity, were assessed with the Primate Neonatal Neurobehavioral Assessment (PNNA) at 14-30 days. Cognitive development was assessed through tasks evaluating infant reward association, cognitive flexibility, and impulsivity at 6-8 months. The fecal microbiome was quantified from rectal swabs via 16S rRNA sequencing. Factor analysis was used to identify "co-abundance factors" describing patterns of microbial composition. We used multiple linear regressions with AIC Model Selection and differential abundance analysis (MaAsLin2) to evaluate relationships between co-abundance factors, microbiome diversity, and neuro-/cognitive development outcomes. At 30 days of age, a gut microbiome co-abundance factor, or pattern, with high Prevotella and Lactobacillus (β = -0.88, p = 0.04, AIC Weight = 68%) and gut microbiome alpha diversity as measured by Shannon diversity (β = -1.33, p = 0.02, AIC Weight = 80%) were both negatively associated with infant emotional responsivity. At 30 days of age, being NR was also associated with lower emotional responsivity (Factor 1 model: β = -3.13, p < 0.01; Shannon diversity model: β = -3.77, p < 0.01). The infant gut microbiome, along with early-rearing environments, may shape domains of neuro-/cognitive development related to temperament.
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