Stress and the commensal microbiota: importance in parturition and infant neurodevelopment

Abstract

The body is colonized by an enormous array of microbes that are collectively called the microbiota. During quiescent periods, microbial communities within the gut are relatively resistant to change. However, several factors that disrupt homeostasis can also significantly change gut microbial community structure. One factor that has been shown to change the composition of the gut microbiota is exposure to psychological stressors. Studies demonstrate that the commensal microbiota are involved in stressor-induced immunomodulation, but other biological effects are not yet known. This review discusses emerging evidence that the microbiota can impact the brain and behavior and indicates that stressor-induced alterations in the composition of gut microbial communities contribute to stressor-induced behavioral changes. This review will also discuss the evidence that such effects are most evident early in life, where both stress and the microbiota have been linked to birth outcomes, such as prematurity, and neurodevelopment. When considered together, a paradigm emerges in which stressor-induced alterations in commensal microbial populations significantly impact parturition and infant neurodevelopment.

Keywords: anxiety; depression; microbiota; neurodevelopment; neuroimmune; prematurity; psychological stress.

Figure 1

Bidirectional interactions exist between the central nervous system and the gut microbiota. During exposure to stressful stimuli, the physiological stress response can lead to alterations in gastrointestinal functioning, such as alterations to gastrointestinal motility and the secretion of factors like gastric acid and bile. The physiological stress response is also known to impact immune system activity. Both alterations to gastrointestinal functioning and immune system activity can significantly change the composition of the gut microbiota. These alterations to the microbiota can feedback and impact gastrointestinal functioning, immune system activity, as well as the physiological stress response and stressor-induced behavioral states.

Figure 2

Maternal stress can impact infant neurodevelopment through both microbiota-dependent and -independent pathways. The maternal physiological stress response can directly impact fetal development and may be involved with epigenetic changes in the offspring. In addition, the maternal physiological stress response may impact the commensal microbiota. Infants may become colonized with altered maternal microbes either in utero, through bacterial invasion of the amniotic cavity, or during/after birth when maternal microbes are passed to the infant. Either alterations in infant physiology (including epigenetic modifications) or colonization with dysbiotic microbial communities may lead to deficiencies in infant neurodevelopment.