Whose Mind Is This, Anyway?

"....we are not unitary individuals but superorganisms, built out of both human and nonhuman elements; it is their interaction that determines who we are."  (Kramer & Bressan, 2015)

One of the illusions most of us hold with great conviction is that we are separate and distinct from the rest of the world.  "I am here. You (and everything else) are there."  "I am this.  I am not that." This belief in separateness and in the essence of our self identity seems so clearly true that we tend not to question it.  However, once we begin to examine closely what is meant by "here" and "there," "I" and "you," "this" and "that," things start to get a bit fuzzy.

My somewhat deranged fascination with (a) microbes (aka "germs") and (b) excrement (aka "poop") has led me to discover that there is a lot of scientific evidence supporting the idea that our belief in separateness is simply not correct. I've written about some of this before (see Fabulous Synthetic Poop!, Microbes for Breakfast!, and How About A Fecal Transplant?).  Research has shown that each of us is host to more than 100 trillion microbes that live in, on, and around us. Some microbes have been with us since before birth, influencing our development in the womb, and others joined us as we traveled through the birth canal and when our mothers nursed us. The interdependency between their lives and ours is so complete that for the first year of life our immune systems are switched to low so that more microbes can colonize our bodies -- it seems that the evolutionary advantage of having beneficial strains of these critters become part of us is so strong that it outweighs the risk of early childhood infection from "bad" microbes or other pathogens. In fact, we are dependent on them to the point that we could not survive for long without them. They are essential in digesting food, mounting successful immune defenses against diseases, and synthesizing certain vitamins.

In adulthood there are 10 times more microbes in us than there are human cells. Together they are our "microbiome," a community of creatures that interact with each other and with us in complex ways throughout our lives.  The relative number of different strains of bacteria in our microbiomes is unique to each person -- a kind of microbial fingerprint. In fact, some recent preliminary research has shown that we leave microbial traces in our environments that are as identifiable as fingerprints even without touching anything (Meadow et al., 2015).  It seems each of us has a "cloud" of bacteria that surrounds us and which leaves our unique signature wherever we go. If we could make the cloud visible (a "microbiomic aura") it would be very difficult to discern where our microbes end and "we" begin.
 
"I" and "Me" most definitely do not refer to a single, unitary organism that exists separately from all other organisms.  As I suggested with the opening quote above, it is more appropriate to regard ourselves as "superorganisms" -- beings composed of many organisms whose lives are intimately and inextricably intertwined. This integration goes beyond just physical interactions, however.  There is now considerable evidence that even our thoughts, feelings, and behaviors are influenced by nonhuman elements within us -- our minds, in other words, may also be those of superorganisms.

The current state of our knowledge about humans as superorganisms was recently presented by Peter Kramer and Paola Bressan of the University of Padua in an excellent article published in the journal Perspectives on Psychological Science (Kramer & Bressan, 2015). Kramer and Bressan review the data on the microbiome and also research that has investigated other foreign components of our makeup, including viral DNA, cells from other human beings, and microbes that reside in the brain. Their conclusion is quite different from our usual self-view:

...our emotions, cognition, behavior, and mental health are influenced by a large number of entities that reside in our bodies while pursuing their own interests, which need not coincide with ours. Such selfish entities include microbes, viruses, foreign human cells, and imprinted genes regulated by viruslike  elements.......we are not unitary individuals in control of ourselves but rather ... collections of human and nonhuman elements that are to varying degrees integrated and, in an incessant struggle, jointly define who we are.

I'll focus on just two examples to illustrate the psychological influences of our nonhuman residents: gut microbes and brain microbes.  If you want to explore other sources of influence, see Kramer & Bressan's paper, or a less technical partial treatment from BBC.Com, "Is There Another Human Being Living Inside You?"

Effects of Gut Microbes on Behavior, Personality & Mood

Certain strains of microbes in our microbiome have been shown to alter a number of neurotransmitter chemicals, for example by manufacturing and releasing GABA and other neuroactive substances, including noradrenaline, acetylcholine,serotonin, and dopamine. These chemicals are involved in mood regulation (eg., euphoria, anxiety and depression), risk-taking behavior, memory formation, sociability, responsiveness to stress, and they likely play a role in certain mental disorders, such as schizophrenia and autism.

The link between specific patterns of gut microbes and behavior has been clearly shown in animal studies where normally timid strains of mice become adventurous and adventurous mice become timid when colonized with the microbiome of the other strain through fecal transplants. In other studies, mice raised with minimal gut microbes showed lower levels of anxiety under calm conditions, but stronger than normal reactions when stressed.  These effects could be eliminated if the germ free mice were given fecal implants from normal mice, but only up to a certain age: "Thus, early exposure to (healthy) gut flora is required for normal development of the stress response ...[and] neonatal infection with pathological bacteria may permanently alter such response, predisposing the individual to stress-related disorders later in life" (Kramer & Bressan, 2015).  Increasing certain microbe strains commonly found in yogurt reduced despair-like behaviors (eg., passivity, not attempting to escape stressful stimuli) in rats, and feeding mice a microbe-laced broth improved their memory and reduced anxiety and depression-like behaviors.

Studying the psychological influences of microbes in humans is more challenging because our experiences can be unwittingly influenced by expectations and prior beliefs  -- the so-called placebo effect, or just plain "wishful thinking."  Relying on self-reports of mood, for example, is not scientifically convincing, but several studies of the effects of altering microbial concentrations of certain gut microbes have also included more objective measures.  For instance, in one study healthy individuals ingested daily doses of lactobacilli, the same microbe found in yogurt and other "probiotic" products.  After one month there was a significant reduction of self-reported anxiety and depression, but more importantly there was also a measurable reduction in stress-related cortisol levels, showing the same effectiveness as benzodiazepines (eg. Valium). In another study these same bacteria modified healthy women’s brain activity in regions that control processing of emotion and sensation, dampening reactions to facial expressions of anger and fear ... these same regions are involved in anxiety disorders (Kramer & Bressan, 2015).

Microbes on My Brain

Most of us are hosts not only to gut microbes but also to strains of microbes that colonize our brains. Residing in the brain gives them the opportunity to directly manipulate neurotransmitters and to influence behavior. Particularly interesting, however, is evidence that they do not simply influence mental processes, they also manipulate the brain in ways that increase their own survival and genetic viability.

Unlike gut microbes, brain microbes are almost always parasites, in that they exploit us while simultaneously doing us harm. They are surprisingly (and disturbingly) common. We usually think of parasites as prevalent only in poorer, less developed countries, but in the case of certain brain microbes the rate of infection is uncorrelated with poverty or level of development. For instance, toxoplasma gondii infects about 22% of the U.S. population (CDC data), 50% of those in the U.K and continental Europe, and as high as 70-80% is some South American and African countries, but as low as 10% in parts of Asia (Hill & Dubey, 2002,  Kramer & Bressan, 2015). It is generally believed that toxoplasma evolved as an animal parasite and humans are an incidental host that has occurred in modern times because of close contact with certain animals.

Toxoplasma is a particularly good example of a microbe that manipulates the brain activity and behavior of its host. Toxoplasma eggs are usually found in the poop of animals that have eaten intermediary hosts of the microbe. Animals that ingest the poop become infected and the microbe is spread more widely.  A common example is when domestic cats eat infected mice or rats, then excrete poop with toxoplasma eggs. Rodents, not known to be picky about their food, eat the cat poop and complete the cycle. Humans who come into contact with infected cat feces (say through gardening or cleaning a litter box) can also become hosts by unwittingly ingesting eggs they have accidentally transferred to their food. Another source of infection for humans has been found to be commercially available food, particularly under-cooked meat or fish that has somehow been tainted with Toxoplasma eggs.

Now for the really interesting part. Rats and mice that are infected with Toxoplasma lose their fear of cats and even become sexually attracted to cat urine (see Berdoy, Webster, & Macdonald, 2000).  This, of course, is very bad for the rodents but very good for Toxoplasma because only in the intestines of cats or other intermediary hosts can the microbes produce eggs.  "Toxoplasma manipulates the brain of the rat so as to increase the probability that its otherwise uncertain transfer to the cat’s intestines actually takes place" (Kramer & Bressan, 2015).  The mechanism for this seems to be an increase of the neuroactive chemical dopamine, which in humans is known to be associated with recklessness and sensation-seeking behavior and greater susceptibility to schizophrenia.  This may also be a cause of higher workplace and traffic accidents among infected humans.  Aside from the neurological effects on behavior, Toxoplasma doesn't usually pose serious physical problems for its host unless the victim's immune system is weakened.  Humans with other health problems, young children, and elderly are at risk and in infants neurological damage can be quite severe.  For this reason pregnant women (who can be infected but asymptomatic) are often advised to avoid contact with cats in order to prevent passing Toxoplasma eggs to their offspring.

Conclusion

Besides Toxoplasma there are a number of other microbes that often colonize the brain, and there are several non-microbial life forms that also influence behavior and cognition. The bottom line for me is that "knowing thyself" requires assessing the contribution 100's of trillions of other organisms to our sense of who we are.  The old adage, "we are not alone," applies not only to things that are external to us but also to things that are deeply embedded within our bodies. Perhaps, as Kramer & Bressan put it: "It is time to change the very concept we have of ourselves and to realize that one human individual is neither just human nor just one individual. "
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Sources & Resources
Kramer, P., & Bressan, P. (2015). Perspectives on Psychological Science, Vol. 10(4) 464–481
You're Surrounded by a Cloud of Bacteria as Unique as a Fingerprint: Washington Post, 9/22/15
CDC - Toxoplasmosis - Epidemiology & Risk Factors 
CDC -Toxoplasma gondii Infection in the United States
Berdoy M., Webster, J. P. and Macdonald, D. W. (2000) Fatal attraction in rats infected with Toxoplasma gondi. Proc. R. Soc. Lond. B, 267, 1591-1594
Is There Another Human Being Living Inside You?:  BBC.com, 9/18/15