Are gut microbiota responsible for your child’s temperament and behavior?
The takeaway
Gut microbiota differs in children with different temperaments
Modulating the gut bacteria in mice induces behavioral changes
Different gut microbial communities in children are associated with cognitive performance
Probiotics can improve behavior and mood in mice and humans
Read on for more!
Over the last 3 weeks, we’ve discussed the connection between the gut and the brain, known as the gut-brain axis, and how the gut microbiome is related to autism spectrum disorder and attention deficit hyperactivity disorder. This week, we’ll discuss the relationship between gut microbiota, behavior, temperament and cognitive development. Although much of the research on these topics is fairly preliminary, it sheds light on just how intimate our interactions are with our gut microbiota.
A seminal study demonstrating a link between gut microbiota and behavior showed that germ-free mice display elevated stress response to forced immobilization [1]. Germ-free mice are also significantly socially impaired, and avoid both new and familiar mice [2]. These mice also have substantially higher levels of the stress hormone corticosterone and lower levels of brain-derived neurotrophic factor, which a protein that stimulates neurogenesis and synaptic growth [1]. Some of these traits can be partially reversed by colonization with specific microbiota, particularly the probiotic bacterium Bifidobacterium infantis, or with a complete microbiome [1, 2].
In this post I’ll discuss a few studies that further demonstrate the relationship between gut microbiota, temperament, behavior and cognitive development. As is the case in science, the results from one study do not mean anything definitive. Rather, they suggest a new way of thinking about things and call for additional work to confirm or challenge the findings and delve deeper into the details. So while the results discussed below are certainly intriguing and exciting, follow-up studies are needed to put these findings into a larger context.
Is there a relationship between gut microbiota and temperament?
One study assessed the relationship between gut microbiota and temperament of 77 children, ages 18-27 months [3]. The children’s mothers reported temperament based on a questionnaire and researchers determined the gut microbiota from fecal samples. They found that certain microbial communities and specific bacteria were associated with certain temperaments; this phenomenon was more pronounced and consistent in boys over girls [3].
Overall, the temperament ratings differed between boys and girls. Girls were rated higher in Effortful Control and boys in Surgency/Extraversion. Effortful Control describes better executive attention and emotional response regulation. Surgency/Extraversion relates to positive affect, high environmental engagement, and high energy. These temperaments were associated with differences in gut microbiome.
Boys and girls with Surgency/Extraversion had more diverse gut microbial communities. In boys, three sub-traits of Surgency/Extraversion were related to differences in specific microbiota. Sociability was associated with higher abundance of Ruminococcaceae and Parabacteroides, whereas High-Intensity Pleasure and Activity Level were associated with higher abundance of Dialister and Rikenellaceae.
In girls, Higher Effortful Control was associated with lower microbial community diversity. Additionally, differences in the bacterial family Rikenellaceae were observed in relationship to Fear.
Some of these bacteria have also been associated with depression and autism in humans, and stress behavior in mice. More research is needed to understand how these bacteria may be involved in behavioral traits.
The authors concluded that “In general, kids with more diverse microbiomes tended to be more curious, positive, social, extroverted, and impulsive, while lower overall bacterial diversity was linked with more fear, cuddliness, and self-restraint [3].”
Do changes in gut microbiota induce changes in behavior?
To assess whether changes in gut microbiota influence behavior, researchers treated mice with antibiotics for 1 week [4]. They determined that the antibiotics did induce changes in gut microbiota and increased the exploratory behavior in mice. Notably, two weeks after stopping the antibiotics, both the gut microbiota and behavior returned to normal. Overall, these results indicate that gut microbiota and behavior are intimately linked and adjust fairly quickly to changes.
The researchers then wondered if transferring gut could induce behavioral changes. To assess this, they used 2 different breeds of mice. Breed 1 is more timid and anxious and Breed 2 is more exploratory. Mice from both breeds were raised in germ-free environments, so they had no gut microbiota. Separately, researchers raised both breeds conventionally so that they would have natural gut microbiota.
Researchers collected fecal material, which contains gut microbiota, from these conventionally raised mice and transplanted it into the germ-free mice. The germ free mice adopted nearly 100% of the donor gut bacteria, although the proportions differed. Interestingly, within 3 weeks, the recipient mice also adopted the behavior of their donor mice. Now, mice from Breed 1 were more exploratory and mice from Breed 2 were less exploratory.
In both these experiments, researchers observed differences in the levels of the brain-derived neurotrophic factor (BDNF). BDNF increased in the hippocampus and decreased in the amygdala. Hippocampal BDNF is associated with memory and learning, and can have anti-anxiety and antidepressant effects [5]. In contrast, no changes in neurotransmitters, including dopamine, serotonin or noradrenalin, were observed [4].
This study shows that modulation of gut microbiota can impact behavioral traits such as exploration. Changes in gut microbiota can occur due to antibiotic use, dietary changes, probiotic use, stress, or even a fecal microbiota transplantation (FMT). FMT, in which the purified fecal material from a healthy donor is transferred to a patient, has gained much attention recently due to its unmatched success with curing chronic Clostridium dificile (commonly known as C. diff.) infections [6]. As I discussed previously, fecal microbiota transplantation has also been explored as an option to treat autism spectrum disorder [7]. We are learning that a disrupted gut microbiome influences a variety of health aspects, meaning there is great potential for treating these conditions using FMT.
If you received a brain transplantation, you might expect to adopt the personality traits of your donor. But if you received a FMT, would you expect your behavior to change? Likely not, but this research suggests that the fecal donor’s personality traits or behavioral tendencies may be transferred along with their gut microbiota. As FMT becomes more widespread, it will be important to screen donors carefully and “choose your poop wisely” so to say.
What is the relationship between gut bacteria and cognition?
This next study examined the gut microbiota and cognitive development of 89 children [8]. The gut microbiota was determined at age 1, and cognitive development (gross motor, fine motor, visual reception, receptive language and expressive language) was assessed ages 1 and 2.
Based on the composition of the gut microbiota, 3 groups were formed. Group 1 had high abundance of Faecalibacterium, Group 2 had high abundance of Bacteroides and Group 3 was high in Ruminococcaceae. Group 1 had the highest microbial diversity, followed with Group 3 and then Group 2 with the lowest microbial diversity [8].
At age 1, there were no differences in cognitive development between these 3 groups; however, significant differences were observed at 2 years of age. In particular, receptive language and expressive language differed between the groups. Group 2 showed highest performance, followed with Group 3 and Group 1 showed the lowest [8].
The researchers found a negative correlation between microbial diversity and cognition; as in, Group 2 had the lowest diversity but was the highest performing and Group 1 had the highest diversity but was the lowest performing. Generally, higher diversity is associated with more mature microbiome. The gut microbiome typically matures after cessation of breastfeeding [9]. The children in Group 2 were more likely to be breastfed than children in the other groups, which may explain the lower diversity in their gut microbial community. Additionally, the fats in breast milk likely help brain development and the carbohydrates support the growth of beneficial gut bacteria and the production of short-chain fatty acids [10].
The researchers were somewhat surprised by the negative correlation between microbial diversity and cognition, because traditionally, low diversity is associated with more negative health outcomes. However, when looking at the big picture, the role of microbial is inconsistent. Low diversity is associated with including Type 1 diabetes [11] and asthma [12], but high alpha diversity has been observed in individuals with autism spectrum disorder [13] and adults with major depressive disorder [14].
Can probiotics modify behavior and mood?
Modification of gut microbiota through probiotics may also modulate host stress and behaviors as well. Mice given probiotics for ~30 days (Lactobacillus rhamnosus, L. helveticus, Bifidobacterium longum; B. breve) decreased anxiety-like behavior, and mice given B. infantis showed reduced depression-like behaviors in a variety of models [15].
Similarly, In a 4 week trial, humans given fermented milk containing the probiotic bacteria B. animalis, Streptococcus thermophilus, L. bulgaricus and Lactococcus lactis showed reduced activation of the emotional processing regions of the brain [16]. Probiotic consumption reduced self-reported feelings of sadness and aggressive thoughts. Consumption of L. helveticus and B. longum reduced self-reported anxiety and also decreased cortisol [17].
Interestingly, one study showed that consumption of probiotics in fermented dairy did not necessarily change the composition of the gut microbiome. Rather, the probiotics induced changes in the metabolic activity of the microbiota [18]. This suggests that just looking at the microbial profile, i.e., presence/absence of certain bacteria, of the gut may not tell the whole picture, but understanding which metabolites those microbes are producing can help us understand their role in our health.
References
Sudo, N., et al., Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol, 2004. 558(Pt 1): p. 263-75.
Desbonnet, L., et al., Microbiota is essential for social development in the mouse. Mol Psychiatry, 2014. 19(2): p. 146-8.
Christian, L.M., et al., Gut microbiome composition is associated with temperament during early childhood. Brain Behav Immun, 2015. 45: p. 118-27.
Bercik, P., et al., The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology, 2011. 141(2): p. 599-609, 609 e1-3.
Deltheil, T., et al., Behavioral and serotonergic consequences of decreasing or increasing hippocampus brain-derived neurotrophic factor protein levels in mice. Neuropharmacology, 2008. 55(6): p. 1006-14.
Rohlke, F. and N. Stollman, Fecal microbiota transplantation in relapsing Clostridium difficile infection. Therap Adv Gastroenterol, 2012. 5(6): p. 403-20.
Kang, S.S., et al., Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring. J Neuroinflammation, 2014. 11: p. 156.
Carlson, A.L., et al., Infant Gut Microbiome Associated With Cognitive Development. Biol Psychiatry, 2018. 83(2): p. 148-159.
Backhed, F., et al., Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe, 2015. 17(6): p. 852.
Jeurink, P.V., et al., Human milk: a source of more life than we imagine. Benef Microbes, 2013. 4(1): p. 17-30.
Kostic, A.D., et al., The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe, 2015. 17(2): p. 260-73.
Abrahamsson, T.R., et al., Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy, 2014. 44(6): p. 842-50.
Finegold, S.M., et al., Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe, 2010. 16(4): p. 444-53.
Jiang, H., et al., Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun, 2015. 48: p. 186-94.
Sampson, T.R. and S.K. Mazmanian, Control of brain development, function, and behavior by the microbiome. Cell Host Microbe, 2015. 17(5): p. 565-76.
Tillisch, K., et al., Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology, 2013. 144(7): p. 1394-401, 1401 e1-4.
Messaoudi, M., et al., Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr, 2011. 105(5): p. 755-64.
McNulty, N.P., et al., The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med, 2011. 3(106): p. 106ra106.
presence/absence of certain bacteria, of the gut may not tell the whole picture, but understanding which metabolites those microbes are producing can help us understand their role in our health.