“The Social Network” – How the Gut Microbiome Governs Our Social Behaviour

Mario Corrado, Hons. BSc Microbiology and Immunology
Contributor

---

Image Courtesy of Sarah C.P. Williams, Howard Hughes Medical Institute

            ​It is Aristotle that once famously remarked how “man is by nature a social animal”. Of course, we need only reflect on our past experiences for a short while to understand the truth in Aristotle’s words. Our very existence as a species depended on our ancestor’s abilities to interact and help one another. Seeing as how social skills often (but not universally) serve as a prerequisite for a fulfilled life, social psychologists and neuroscientists alike have dedicated large resources to deciphering the mechanisms behind our social nature. A major breakthrough came at the turn of the 20th century, when Henry Dale discovered “Oxytocin”, a chemical that has earned the reputation of the “love hormone” for its role in encouraging social bonding, prosocial behaviours, “maternal instincts”, fear reduction and in antagonizing the effects of depression (learn more here: 1). But oxytocin alone cannot explain the entirety of our social behaviour.
 
We’re missing something.
 
            In natural sciences, one will often hear the phrase “paradigm shift” to describe a series of scientific findings that radically alters our basic understanding of a scientific phenomenon (the most notable example, for instance, is Charles Darwin’s Evolutionary Theory, which rigorously challenged the way in which we perceived our very origin as a species). With a wealth of studies demonstrating new ways in which our intestinal bacteria dictates our health and behaviour (a great review can be found here: 2), the gut microbiome is primed to give way to the next great paradigm shift – particularly in relation to the extent to which the gut-brain axis influences our mood and behaviour.
 
            If you are familiar with my previous blog post Life on The Spectrum – An Abnormal Microbiome and…Autism?, you may recall the three characteristic behavioural autism-like symptoms: limited social interactions, a tendency for repetitive behaviour and reduced overall communication (3). Autism patients are also known to possess an altered gut microbiome composition (4). Up until recently, this observation was merely an association; an altered gut microbiome in autistic patients was associated with disruption in social development, but was never shown to be a cause of social disruption. However, recent evidence emerging from the lab of Dr. JF Cryan at University College Cork in Ireland (5) suggests that an altered gut microbiome does indeed impede normal social development.
 
            To support his claim, Cryan’s team studied the social behaviour of mice using a “three-chambered sociability test” (6). This test includes a three-chambered box with openings between the chambers. In brief, this setup assesses social behavior in the form of general sociability as well as interest in social novelty. Cryan’s group performed two experiments:

• General sociability: Here, a subject mouse is placed in the middle chamber. In one chamber, we can find a second mouse, while the other chamber remains empty. We can then track our subject mouse by measuring how much time it spends in each chamber to assess its social inclination. Mice, like humans, are a highly social species and thus have a natural propensity to seek out the benefits afforded by stable social situations. Cryan’s team noted that while a normal mouse with an intact microbiome was likely to spend a considerable amount of time with the other mouse, a germ-free mouse (a mouse void of a gut microbiome) spent a significant amount of time alone. Interestingly, it was observed that if the gut microbiome of the germ-free mouse was repopulated, then the opposite trend was observed: germ-free mice with a repopulated microbiome spent a significant amount of time with the other mouse. This experiment is remarkable, suggesting that the presence of an intact gut microbiome increases the mouse’s propensity to engage in social activity.
  
  
• Social novelty: Here, a subject mouse is placed in the middle chamber. In one chamber, we can find a second mouse with whom the subject mouse is familiar with. An unfamiliar third mouse is then placed in the third chamber. We can then track the amount of time the subject mouse spends with the “familiar” and “unfamiliar” mice. Cryan found that while normal mice have a tendency to spend time with the unfamiliar mouse, this propensity for social novelty is lost in germ-free subject mouse, which practice an attitude of social avoidance. Unlike in the first experiment, re-introducing the gut microbiome into the germ-free mouse did not increase time spent with the unfamiliar mouse.

 
          The results of this study have potentially large implications in the realm of autism. In addition to symptoms of reduced social motivation, children with autism exhibit poor communication skills as well as repetitive behaviours. Since it is well understood that many autism patients have a dysregulated gut microbiome, is it a far-stretched hypothesis that the impaired social behaviour observed among autistic patients is at least a partial result of an abnormal microbiome? If so, could we substantially decrease autism-like symptoms and increase social development by focusing our treatments and efforts on re-balancing the gut microbiome?
 
          And how about introverts? Approximately 50% of the population identify themselves as introverted (7). Do they house a microbiome that differs from those of extroverts?  Cryan’s results spur a whole new set of questions concerning our social behaviour as a species.
 
          A final question that may come to mind is why gut bacteria are dictating our social behaviour. We have a fairly clear idea as to how – via the gut-brain axis. But why have humans and microbes co-evolved in such a way? Although we cannot know for certain, it is worth noting that microbes have lived on Earth for far longer than humans have. In that time, microbes have yearned for one ultimate evolutionary goal: to reproduce and spread throughout the planet. Is it possible, then, that bacteria, in a parasitic way, are purposefully encouraging our social drive? By encouraging us to interact with other humans, bacteria can jump to our neighbors, who then go their own way. Just like that, bacteria figured out a way long ago to use mammals as vehicles to spread across the globe… Although this idea is difficult to prove, what a remarkable mechanism that would be – microbes stimulate our social development for their benefit, to promote their spread.
 
          And if that’s true, what other behaviours are being manipulated by microscopic organisms? If our gut microbiome is controlling our social development, who’s to say they don’t play a role in other cognitive functions? Are we really in control of our own thoughts and actions, or are we merely the puppets in a microbe-dominated world?
 
References
1.         Ishak, W. W., M. Kahloon, and H. Fakhry. 2011. Oxytocin role in enhancing well-being: a literature review. J. Affect. Disord. 130: 1-9.
2.         Shreiner, A. B., J. Y. Kao, and V. B. Young. 2015. The gut microbiome in health and in disease. Current opinion in gastroenterology 31: 69-75.
3.         Prevention, C. f. D. C. a. 2012. Autism Spectrum Disorder — Data & Statistics.
4.         Kang, D. W., J. B. Adams, A. C. Gregory, T. Borody, L. Chittick, A. Fasano, A. Khoruts, E. Geis, J. Maldonado, S. McDonough-Means, E. L. Pollard, S. Roux, M. J. Sadowsky, K. S. Lipson, M. B. Sullivan, J. G. Caporaso, and R. Krajmalnik-Brown. 2017. Microbiota Transfer Therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5: 10.
5.         Desbonnet, L., G. Clarke, F. Shanahan, T. G. Dinan, and J. F. Cryan. 2014. Microbiota is essential for social development in the mouse. Mol. Psychiatry 19: 146-148.
6.         Yang, M., J. L. Silverman, and J. N. Crawley. 2011. Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci. Chapter 8: Unit 8.26.
7.         Myers, I. B., McCaulley, M. H., Quenk, N. L., & Hammer, A. L. (1998). MBTI Manual: A guide to the development and use of the Myers-Briggs Type Indicator (3rd ed.). Palo Alto, CA: Consulting Psychologists Press.