Prenatal stress enhances postnatal plasticity: The role of microbiota

Abstract

Separate fields of inquiry indicate (a) that prenatal stress is associated with heightened behavioral and physiological reactivity and (b) that these postnatal phenotypes are themselves associated with increased susceptibility to both positive and negative environmental influences. Collectively, this work supports Pluess and Belsky's (Psychopathology, 2011, 23, 29) claim that prenatal stress fosters, promotes or “programs” postnatal developmental plasticity. Herein, we review animal and human evidence consistent with this hypothesis before advancing the novel idea that infant intestinal microbiota may be one candidate mechanism for instantiating developmental plasticity as a result of prenatal stress. We then review research indicating that prenatal stress predicts differences in infant intestinal microbiota; that infant intestinal microbiota is associated with behavioral and physiological reactivity phenotypes; and, thus, that prenatal stress may influence infant intestinal microbiota in a way that results in heightened physiological and behavioral reactivity and, thereby, postnatal developmental plasticity. Finally, we offer ideas for testing this claim and consider implications for intervention and use of probiotics during early infancy.

Moving the dial on prenatal stress mechanisms of neurodevelopmental vulnerability to mental health problems: A personalized prevention proof of concept

“…In PHBP, we focus on emotion dysregulation as the optimal neurodevelopmental phenotype for assessing vulnerability to mental health problems as it is (a) measurable beginning at birth; (b) ubiquitous across most internalizing and externalizing disorders; (c) associated with corollary prefrontal disruptions; and (d) strongly linked to prenatal stress exposure from early in life (Beauchaine & Cicchetti, 2019; Davis et al., 2018; Finlay‐Jones et al., 2019; Hartman et al., 2019; Wakschlag, et al., 2019) (see Table S1 for multi‐level measurement specifics). In particular, we have emphasized atypical expressions of irritability as our central behavioral phenotype because it is a highly salient pattern identifiable in very young infants that is a transdiagnostic risk marker (Toohey & DiGiuseppe, 2017; Wakschlag, et al., 2019).…”

“…The fetal programming model holds that the fetus adapts to in utero exposures, impacting the development of later health and disease (Glover et al., 2018). The impact of maternal stress on fetal pathophysiology may include: stress physiology, alterations of placental biology and function, inflammation, and changes in microbiota (Hartman et al., 2019; O'Connor et al., 2019).…”

“…At the same time, advances in developmentally based methods (e.g., infant imaging, dimensional phenotypes), as well as emphasis on transdiagnostic common pathways (e.g., emotion dysregulation as infant risk phenotype) now enable detection of neurodevelopmental vulnerability to subsequent mental health problems beginning at birth. Capturing this vulnerability in proximity to exposure is critical when testing plasticity of causal pathways (Beauchaine & Cicchetti, 2019; Finlay‐Jones et al., 2019; Graham, Pfeifer, Fisher, Carpenter, & Fair, 2015; Graham, Pfeifer, Fisher, Lin, et al, 2015; Hartman et al., 2019; Wakschlag, et al., 2019). Joining a burgeoning call for action (Davis et al., 2018; Doyle & Cicchetti, 2018; Gelaye & Koenen, 2018; Glover, 2014; Goodman et al., 2018; Heim et al., 2018; Shonkoff, 2016), we aim to move the translational dial on prenatal stress research from robust observational evidence to a preventive approach, with promise for improving lifecourse health.…”

External environment and internal state in relation to life-history behavioural profiles of adolescents in nine countries

“…Animals likewise respond to internal cues by adopting the same biobehavioural strategies. Aspects of the internal or somatic state, such as body size, energy reserves, immune functioning, quality of cell-repair mechanisms, and microbiotic conditions, determine the optimal behaviour an animal should adopt to maximize its evolutionary fitness [26][27][28][29][30][31]. Animals in poor physical condition who face direct mortality-morbidity threats internally should calibrate their LH accordingly to prioritize immediate survival and reproduction over development and long-term fitness pay-offs, and they should adopt antagonistic-opportunistic social strategies to achieve shortterm reproductive goals.…”

Prenatal programming of environmental sensitivity

“…For example, alterations in the microbiome have been linked to psychological disorders including depression and anxiety [ 96 ]. Other work has highlighted variations in the composition of the intestinal microbiome as a potential marker of environmental sensitivity [ 97 ].…”