The Brain, Gut and Consciousness: Microbiology of Our Mind
IN THIS ARTICLE
This paper presents a view that the brain is not the only actor responsible for emergence of our consciousness and that our consciousness is in fact a product of the brain-gut-microbiome axis. The paper first shows relevance of the contemporary research on the symbiotic bacteria for the study of our consciousness. Then, it discusses whether the brain itself is actually a necessary condition for the mere existence of consciousness. Finally, it concludes that our consciousness is our emergent property caused by the bidirectional communication between the brain and the gut microbiota.
We are never alone. And by this statement, I do not intend to argue for existence of some supernatural entities, aliens or God. We are never alone because we all share our bodies with trillions of symbiotic microorganisms that perform various physiological functions crucial for our health. In fact, they may be responsible for even more than that. Here, I present a view that the symbiotic microbiota is an important part of the complex system constituting our consciousness. By consciousness, I mean the type called phenomenal consciousness (Block 2002) which stands for the subjective experience of what is it like to be someone (see Nagel 1974).
If we look at the contemporary literature on consciousness (e.g. Dehaene 2014; Northoff 2014; Graziano 2015; Feinberg and Mallatt 2017), we can see that the current trend in philosophy of mind is to focus on the role of the brain. This seems quite reasonable since for so long we thought that it is just the brain that creates our mind. However, new biological discoveries in the last decade suggest that we were wrong and there are also other actors at play with a causal impact on our mental states1.
In this paper, I first introduce the concept of holobiont and explain what it signifies for the study of consciousness. Next, I focus on the role of the brain-gut-microbiome axis and its importance for the future research in philosophy of mind. Then, I discuss whether the brain is a necessary condition for the existence of consciousness at all, and finally I conclude that our consciousness is our emergent property caused by the brain-gut-microbiome axis.
We Are Holobionts
Before we proceed further with our search for consciousness, we must first reject the already outdated idea that we as biological entities are unitary individuals. What constitutes us as biological organisms is actually not just our body mass in the sense of organs, muscles, bones, etc., but also the microorganisms living in symbiosis with our bodies. In fact, our bodies contain on average 3.8x1013 bacteria (10-times more than the number of human nucleated cells) making approximately 0.2 kg of our body mass (Sender et al. 2016). However, what is more important here is not so much their number but rather the symbiotic relationship. As Suárez (2018: 91) correctly points out: ‘To prove that two entities living together are a biological individual, one needs to prove that there is a shared functionality. Inferring that two entities are a unique individual (or that they relate to each other mutualistically) from the fact that they share the same physical boundaries is insufficient.’
The current biological research shows that the symbiotic bacteria are responsible for various physiological processes in our bodies and thus fulfil the functional condition of being considered part of the individual (Gilbert et al. 2012). To describe this biological entity referring to the host and its microbiota, scientists use the term ‘holobiont’ (Rohwer et al. 2002: 8). As far as we know, the holobiont concept of an individual applies to the vast majority of organisms on Earth (Herron et al. 2013) which has led many biologists to conclude that all animals and plants are holobionts (e.g. Rosenberg and Zilber-Rosenberg 2018). The typical example of symbiosis presented in biological textbooks is the digestive process of cow. Cows are not capable of digesting grass themselves; it is the bacteria living in their stomachs doing the job (which is also the reason why humans cannot digest grass – we lack the right bacteria for that). In other words, in the same way as the host cannot live without certain organs, it often cannot exist without its microbiota2. Therefore, there is no reason to exclude the symbiotic bacteria from the definition of an individual.
Moreover, Ilana Zilber-Rosenberg and Eugene Rosenberg (2008; 2018) put forth the view of holobiont as a single unit of selection in evolution. They have come up with the hologenome theory which considers the host’s microbiota as part of the evolving holobiont (Zilber-Rosenberg and Rosenberg 2008: 723). Because of much shorter generation times of bacteria, the symbiotic microbiota can reflect changes in the environment faster and thus provide time for the host genome to evolve. Consequently, this gives the holobiont better chances to adapt to environmental changes and hence survive (ibid.: 730). The most questioned aspect of the theory is the transmission of microbiota between generations (see e.g. Godfrey-Smith 2015; Stencel 2016; Hurst 2017). Rosenberg and Zilber-Rosenberg (2018) argue that this transmission happens both vertically (e.g., transfer of maternal vaginal and fecal microbes at birth, or many others via breastfeeding) and horizontally (i.e., from the environment). Nevertheless, at the same time, they admit that this point of their theory is, considering the state of our current knowledge, the hardest to generalize3 (ibid.).
To summarize, holobionts are ‘composite organisms, whose physiology is a co-metabolism between the host and its microbiome, whose development is predicated upon signals derived from these commensal microorganisms, whose phenotype is predicated on microbial as well as host genes, and whose immune system recognizes these particular microbes as part of its “self”4,’ (Gilbert and Tauber 2016: 840). Some even maintain that entire ecosystems and ultimately the whole planet should be considered as a holobiont (e.g. Matyssek and Lüttge 2013). However, this is probably too far stretched since neither ecosystems, nor planets are biological organisms reproducing to the next generation.
Consciousness and the Brain-Gut-Microbiome Axis
Thus, we have to redefine the concept of an individual. So be it. But why is that important for the examination of our consciousness? Why should philosophers of mind care about the notion of holobiont? In other words, what are the implications of these new biological discoveries for philosophy of mind? To answer that, we must look at the role the symbiotic microbiota plays in our organism in detail.
First of all, it should be noted that the vast majority of the symbiotic bacteria dwells in our gut (Sender et al. 2016). The research of the last decade shows how important these microorganisms are for various processes we used to associate only with the central nervous system, namely with the brain. To give a better idea of the relevance of these new findings, they are so ground-breaking that some even call it a paradigm shift in neuroscience and psychiatry (Mayer et al. 2014). As a result, scientists have started to talk about the brain-gut-microbiome axis. Specifically, the brain-gut-microbiome axis refers to bidirectional communication between the central nervous system and the gut microbiota. This happens via several parallel interacting channels including the immune, endocrine and nervous systems (Martin et al. 2018: 133) with the major role played by the vagus nerve5 (Wang et al. 2002; Bravo et al. 2011).
When it comes to the impact of the gut microbiota on the brain, it begins as early as during the development of the brain itself. For instance, Hoban et al. (2016) found that that the microbiota is necessary for effective myelination of prefrontal cortex – the part of the brain dealing with emotions, memory or cognition. Moreover, the bacteria seem to contribute to synaptic growth and plasticity (Sampson and Mazmanian 2015: 567) and through the influence on the brain development also affect the progress of our motor control (Heijtz et al. 2013). On the other hand, brains of animals raised in sterile environments lack this structural integrity (Luczynski et al. 2016a). Besides that, Carlson et al. (2018) have demonstrated a link between the gut bacteria and cognition in human infants6.
Nevertheless, the role of the gut microbiota does not end in our childhood, but these microorganisms remain an inevitable part of the system responsible for various emotional and cognitive processes throughout our lives7 (Carabotti et al. 2015; Foster et al. 2017). For example, certain bacteria are known to improve object recognition and object discrimination (Savignac et al. 2015). In another study, Tillish et al. (2013) showed that consumption of probiotic8 cocktails alters the cognition of facial expressions of other people. Furthermore, the irritable bowel syndrome, a functional gastrointestinal disorder typically associated with the brain-gut-microbiome axis (Martin et al. 2018: 133), influences our cognition as well (Kennedy et al. 2014). In addition, some bacteria can even mediate pain perception (Kunze et al. 2009) and apart from that, the gut microbiota affects the process of learning and memory (Ogbonnaya et al. 2015). For instance, O’Hagan et al. (2017) demonstrated the effect of probiotics on both long-term and short-term memory of objects.
As remarked above, the gut microbiome shapes our emotional states, too (O’Mahony et al. 2014). Recent studies indicate the influence of microorganisms on the amygdala which controls responses to stressful stimuli (Stilling et al. 2015; Luczynski et al. 2016b). Moreover, some substances whose low levels are associated with the emergence of depression and anxiety are produced by the gut bacteria. This has been proven e.g. for the γ‐aminobutyric acid (Bravo et al. 2011; Barrett et al. 2012), oxytocin (Varian et al. 2017), or serotonin (Kim and Camilleri 2000; Reigstad et al. 2014; De Vadder et al. 2018). Actually, in the case of serotonin, 95 % of it is stored in the gut and just 5% belongs to the central nervous system (Kim and Camilleri 2000: 2698). Consequently, the gut bacteria affect social behaviour as well (Desbonnet et al. 2014; Varian et al. 2017; Sherwin et al. 2019), and in Smith and Wissel’s (2019: 2) words: ‘The microbiome’s ability to shape affect and emotion therefore indicates that the influence of bacteria may spill over into every aspect of what it means to be a conscious, living organism.’ However, as noted above, the communication is bidirectional and therefore our emotional states have at the same time an impact on the microbiome structure (Aguilera et al. 2013; Zijlmans et al. 2015). For instance, Galley et al. (2014) found in their study that just a single 2-hour exposure to a social stressor is enough to change the microbiota profile.
Because of this newly discovered link between the brain and gut, scientists now attribute (besides functional gastrointestinal disorders such as the already mentioned irritable bowel syndrome) various neurologic and psychiatric pathologies to the alterations in the gut microbiota. It has been intimated in the previous paragraph that the bacteria can cause anxiety and depression through its influence on the amygdala, which opens new possible ways of therapy in psychiatry (Kelly at al. 2016). Another widely discussed disorder related to the brain-gut-microbiome axis is autism spectrum disorder (ASD). For example, Hsiao et al. (2013) showed in their study a connection between the gut microbiota alterations and symptoms of ASD, and concluded that Bacteroides fragilis can help with the ASD treatment. Moreover, Sampson et al. (2016) demonstrated the relation between the gut bacteria and Parkinson’s disease. All in all, the list of disorders associated with the brain-gut-microbiome axis is still growing and it currently includes, among others, posttraumatic stress disorder, chronic fatigue syndrome, anorexia, alcoholism, schizophrenia, manic depression (Smith and Wissel 2019: 11), multiple sclerosis, and chronic pain (Martin et al. 2018: 133). In many cases, probiotics have been proven as an effective method of treatment of these disorders (Desbonnet et al. 2010; Bravo et al. 2011; Messaoudi et al. 2011; Arseneault-Bréard et al. 2012; Saulnier et al. 2013; Steenbergen et al. 2015).
Consciousness Without Brains
In the previous parts of this paper, we have seen that our mental states and consciousness do not depend solely on the brain but, as far as we know today, they are products of the system called the brain-gut-microbiome axis. Now, can we push this even further and argue that consciousness as such does not depend on the brain at all? In other words, can it be multiply realizable? Furthermore, if part of our consciousness is created by certain symbiotic microorganisms and if all animals (including humans) and plants are holobionts, can these symbiotic microorganisms have the same (or at least similar) effect on other species as they have on Homo sapiens? And are these microorganisms conscious as well? Just to make it clear, in the following paragraphs, I will focus only on the problem of consciousness of brain-less organisms since in the 21st century I find the Cartesian idea of humans as a unique species with consciousness so ridiculous that it would be a waste of time discussing that (see e.g. Griffin and Speck 2004; Barron and Klein 2016). The similar stance is nicely illustrated by William Hasker (2018: 64) when he commented Descartes’ idea that:
First, to be able to identify any examples of the possible multiple realizability of consciousness, we need to know what is the purpose of it. To put it differently, once we know what is the function of consciousness, we can explore whether there are any other structures than the central nervous system that serve the same purpose. And if there really are, we cannot reject the idea that consciousness can be multiply realizable.
Despite the fact that there are many competing theories about the function of consciousness (see e.g. Grossberg 1999; Merker 2005; Rosenthal 2008), the general consensus is that ‘being a conscious organism allows for the adaptive integration of many input and output signals in the service of behavioural flexibility, and the particular conscious content that is integrated functions to elicit a particular adaptive response’ (Seth 2009: 292). In short, consciousness helps us to deal with problems in a flexible way. Brian Earl (2014: 1) associates consciousness9 with ‘a flexible response mechanism(FRM) for decision-making, planning, and generally responding in nonautomatic ways.’ In his view (ibid.):
Hence, in general the goal of consciousness is to filter information so we are able to react more efficiently. This implies that there is a difference between an efficient and non-efficient way of dealing with problems and consciousness guides us towards the former. Therefore, being conscious means dealing with problems in an efficient non-automatic way. It cannot be automatic because under different conditions, different strategies are the best. Consciousness helps us to adjust to these different conditions faster and thus survive better. By the way, notice that the same function of quicker adjustment is fulfilled by the symbiotic microbiota according to the hologenome theory which only supports the claim that our consciousness is partly constituted by these microorganisms.
In my opinion, every species that still exists on the Earth after 4 billion years since the birth of life is able to solve problems in more or less efficient ways, however not everyone may agree with this. On the other hand, due to the progress in natural sciences we know that even brain-less organisms are capable of flexible dealing with problems. One of the most famous examples is the single-celled organism called the slime mold. This organism is capable of memory, transferring learned behaviour, anticipating changes, making decisions, and dealing with problems in a flexible way (Nakagaki 2001; Reid et al. 2012; Jabr 2012; Vogel and Dussutour 2016). Scientists hypothesize that the answer to how the slime mold can react in an intelligent10 way is thanks to its plasmodial cytoskeleton which ‘may have similar functions to those of the mammalian neural network’ (Mayne et al. 2014: 9). Moreover, even plants are capable of similar intelligent actions such as remembering, communicating, learning, and flexible responding (Baldwin and Schultz 1983; Heil and Karban 2010; Thellier and Lüttge 2013; Gagliano et al. 2014). Besides that, plants do not ‘talk’ just to their own kin but they communicate with other species as well (Simard et al. 1997) using the so-called wood-wide web (Helgason et al. 1998). The suggested ‘brain’ of plants could be a sophisticated calcium-signalling network in their cells (Gagliano et al. 2014: 69-70).
Naturally, we can never know if these organisms really have phenomenal consciousness or not due to the problem of other minds (see Allen and Trestman 2017). On the other hand, if these creatures clearly possess the FRM and consciousness is responsible for providing the data to it, then it seems quite reasonable to posit that even brain-less organisms have subjective experience and hence consciousness. This implies that consciousness can actually be multiply realizable. Whether their consciousness is partly a product of their symbiotic microbiota, we do not know yet, but I see no problem with this assumption. Finally, answering ‘yes’ to the question if the symbiotic bacteria are themselves conscious looks like a straight road to panpsychism11. I will briefly discuss this issue in the next section.
Emergent Consciousness of Holobionts
According to the findings presented above, the mere existence of consciousness probably does not depend on the brain at all. To clarify this, I do not claim that we or any other organism that belongs to the species which has developed with the brain can be conscious without the brain. To say that would necessarily imply the existence of a soul, which I do not aim to defend here. I only argue that even species without the brain as we know it can possibly have consciousness.
Nevertheless, what about the second part of the axis – the microbiome? Does the existence of consciousness depend on the existence of the symbiotic bacteria? If the hologenome theory is correct, then all animals and plants share their bodies with bacteria and there is no natural way how to answer this question. On the other hand, there are, for instance, germ-free mice raised in laboratories. As mentioned previously, these animals suffer from neurodevelopmental deficits, have an underdeveloped immune system etc., yet they are clearly capable of mental states such as anxiety and depression similarly to normal individuals. Therefore, the symbiotic microbiota does not seem to be a necessary condition for the existence of some form of consciousness for any species that can somehow survive without its microbiome. However, there are no germ-free humans and the influence of microbiome on our consciousness has been already discussed. Consequently, if we want to study consciousness of healthy people, we must include the symbiotic microbiota into our research.
But can we not simplify the issue and think of the brain-gut-microbiome axis as a causal chain with the brain as the final segment of it? We could still admit that the gut microbiota has a causal impact on our consciousness, and yet the impact would be possible to observe in the brain which would be, among its other functions, the link between the microbiome and consciousness. In that case, the focus solely on the brain would be totally justifiable. At this point, I must repeat that the communication between the brain and the gut microbiota is bidirectional. Hence, there can logically be no final segment of a chain and the linear idea of the axis is wrong. We have to imagine the brain-gut-microbiome axis as a complex interacting system which is as a whole responsible for the emergence of our consciousness. Simply said, we cannot decide whether it was the chicken or the egg that came first. Therefore, both – the brain and the microbiome – are important for the study of the human type of consciousness.
Then, there is the question whether the microorganisms are themselves conscious. In fact, when even brain-less organisms can have consciousness, why should not bacteria too? No matter how interestingly this question may sound, I very much doubt its relevance for the study of our consciousness. As we know, we are holobionts and holobionts are complex systems (Zilber-Rosenberg and Rosenberg 2008: 731) which allows us to talk about holobionts as emergent individuals12 (Suárez and Triviño 2019). I maintain that the type of consciousness we have is an emergent property of this entity called holobiont. Specifically, I argue that, as far as we know, our consciousness is a product of the brain-gut-microbiome axis. To put it differently, our consciousness is a result of the particular relations13 between the brain and the gut microbiota. And because of that, we do not need to know whether there is also another type of consciousness at the lower level since we are interested only in the type of consciousness we have. In Kenneth Waters’ (2018: 98) words: ‘Answering the question “what is it to be a gene?” does not provide important metaphysical insights into the functioning or development of organisms.’ And the same applies to bacteria too.
To sum up, generally speaking neither the brain nor the symbiotic microbiome is a necessary condition for the mere existence of consciousness. On the other hand, both the brain and the microbiome are necessary conditions for the study of the consciousness of healthy human individuals. In short, our consciousness is our emergent property caused by the brain-gut-microbiome axis. The symbiotic microbiota is necessary for the full development of our consciousness, but it does not need to be conscious itself. Hence, we do not have to be panpsychists to acknowledge the role of microbiome for the emergence of consciousness.
In this paper, I have discussed the importance of new biological discoveries for philosophy of mind. Specifically, I have shown how the brain-gut-microbiome axis forms a complex system creating our consciousness. Thus, our consciousness is realized through the material structure constituted by the bidirectional communication between the brain and the gut microbiota. I have demonstrated that none of the components of the brain-gut-microbiome axis is necessary for the mere existence of consciousness and hence consciousness is multiply realizable. On the other hand, I have argued that all the components of the axis are necessary for the type of consciousness healthy humans have. Consequently, philosophers must take into account the whole brain-gut-microbiome system in their studies and they cannot focus solely on the brain as they did in the past.
Naturally, as it is obvious from the brief outline of the influence of the gut microbiota on our consciousness presented here, the research in this area is still just at the beginning and it is likely that we will have to revise our conclusions someday again. Nevertheless, even now it is already clear that our mind is constituted by a far more complex system than we previously thought and we should remain open to new findings coming in the future.14
Aguilera, M., Vergara, P., & Martinez, V. (2013). Stress and antibiotics alter luminal and wall‐adhered microbiota and enhance the local expression of visceral sensory‐related systems in mice.Neurogastroenterology & Motility,25(8), e515-e529.
Allen, A. P., Dinan, T. G., Clarke, G., & Cryan, J. F. (2017). A psychology of the human brain–gut–microbiome axis.Social and personality psychology compass,11(4), e12309.
Allen, C., & Trestman, M. (2017). Animal Consciousness.The Stanford Encyclopedia of Philosophy(Winter 2017 Edition), Edward N. Zalta(ed.). Available at: https://plato.stanford.edu/entries/consciousness-animal/ (Accessed 1/12/2019)
Arseneault-Bréard, J., Rondeau, I., Gilbert, K., Girard, S. A., Tompkins, T. A., Godbout, R., & Rousseau, G. (2012). Combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model.British Journal of Nutrition,107(12), 1793-1799.
Baldwin, I. T., & Schultz, J. C. (1983). Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants.Science,221(4607), 277-279.
Barrett, E., Ross, R. P., O'toole, P. W., Fitzgerald, G. F., & Stanton, C. (2012). γ‐Aminobutyric acid production by culturable bacteria from the human intestine.Journal of applied microbiology,113(2), 411-417.
Barron, A. B., & Klein, C. (2016). What insects can tell us about the origins of consciousness.Proceedings of the National Academy of Sciences,113(18), 4900-4908.
Block, N. (2002). Concepts of Consciousness. In: David J. Chalmers (ed.). (2002).Philosophy of Mind: Contemporary Readings. New York: Oxford University Press, 206-218.
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., ... & Cryan, J. F. (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve.Proceedings of the National Academy of Sciences,108(38), 16050-16055.
Carabotti, M., Scirocco, A., Maselli, M. A., & Severi, C. (2015). The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.Annals of gastroenterology: quarterly publication of the Hellenic Society of Gastroenterology,28(2), 203-209.
Carlson, A. L., Xia, K., Azcarate-Peril, M. A., Goldman, B. D., Ahn, M., Styner, M. A., ... & Knickmeyer, R. C. (2018). Infant gut microbiome associated with cognitive development.Biological psychiatry,83(2), 148-159.
Chalmers, D. (2015). Panpsychism and panprotopsychism.In: Alter, T., & Nagasawa, Y. (Eds.). (2015).Consciousness in the Physical World: Perspectives on Russellian Monism. Oxford: Oxford University Press, 246-276.
De Vadder, F., Grasset, E., Holm, L. M., Karsenty, G., Macpherson, A. J., Olofsson, L. E., & Bäckhed, F. (2018). Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks.Proceedings of the National Academy of Sciences,115(25), 6458-6463.
Dehaene, S. (2014). Consciousness and the brain: Deciphering how the brain codes our thoughts. New York: Viking.
Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2014). Microbiota is essential for social development in the mouse.Molecular psychiatry,19(2), 146-148.
Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010). Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression.Neuroscience,170(4), 1179-1188.
Earl, B. (2014). The biological function of consciousness.Frontiers in psychology,5, 697.
Elder-Vass, D. (2010).The Causal power of social structures: Emergence, structure and agency. Cambridge: Cambridge University Press.
Evrensel, A., & Ceylan, M. E. (2015). The gut-brain axis: the missing link in depression.Clinical Psychopharmacology and Neuroscience,13(3), 239-244.
Feinberg, T. E., & Mallatt, J. M. (2017). The Ancient Origins of Consciousness: How the Brain Created Experience. Cambridge (Mass): The MIT Press.
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017). Stress & the gut-brain axis: regulation by the microbiome.Neurobiology of stress,7, 124-136.
Gagliano, M., Renton, M., Depczynski, M., & Mancuso, S. (2014). Experience teaches plants to learn faster and forget slower in environments where it matters.Oecologia,175(1), 63-72.
Galley, J. D., Nelson, M. C., Yu, Z., Dowd, S. E., Walter, J., Kumar, P. S., Lyte, M., & Bailey, M. T. (2014). Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota.BMC microbiology,14(1), 189.
Gilbert, S. F., & Tauber, A. I. (2016). Rethinking individuality: the dialectics of the holobiont.Biology & Philosophy,31(6), 839-853.
Gilbert, S. F., Sapp, J., & Tauber, A. I. (2012). A symbiotic view of life: we have never been individuals.The Quarterly review of biology,87(4), 325-341.
Godfrey-Smith, P. (2015). Reproduction, symbiosis, and the eukaryotic cell.Proceedings of the National Academy of Sciences,112(33), 10120-10125.
Graziano, M. S. A. (2015). Consciousness and the Social Brain. Oxford: Oxford University Press.
Griffin, D. R., & Speck, G. B. (2004). New evidence of animal consciousness.Animal cognition,7(1), 5-18.
Grossberg, S. (1999). The link between brain learning, attention, and consciousness.Consciousness and cognition,8(1), 1-44.
Hasker, W. (2018). The Case for Emergent Dualism.In: Loose, J., Menuge, A. J., & Moreland, J. P. (Eds.). (2018).The Blackwell companion to substance dualism. Hoboken: Wiley Blackwell, pp. 62-72.
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., ... & Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior.Proceedings of the National Academy of Sciences,108(7), 3047-3052.
Heil, M., & Karban, R. (2010). Explaining evolution of plant communication by airborne signals.Trends in ecology & evolution,25(3), 137-144.
Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H., & Young, J. P. W. (1998). Ploughing up the wood-wide web?.Nature,394(6692), 431.
Herron, M. D., Rashidi, A., Shelton, D. E., & Driscoll, W. W. (2013). Cellular differentiation and individuality in the ‘minor’multicellular taxa.Biological Reviews,88(4), 844-861.
Hoban, A. E., Stilling, R. M., Ryan, F. J., Shanahan, F., Dinan, T. G., Claesson, M. J., ... & Cryan, J. F. (2016). Regulation of prefrontal cortex myelination by the microbiota.Translational psychiatry,6(4), e774.
Hopkins, M. J., Sharp, R., & Macfarlane, G. T. (2002). Variation in human intestinal microbiota with age.Digestive and Liver Disease,34, S12-S18.
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., ... & Patterson, P. H. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders.Cell,155(7), 1451-1463.
Hurst, G. D. (2017). Extended genomes: symbiosis and evolution.Interface Focus,7(5), 20170001.
Jabr, F. (2012). How brainless slime molds redefine intelligence. Nature. Available at: https://www.nature.com/news/how-brainless-slime-molds-redefine-intelligence-1.11811 (Accessed 1/12/2019)
Kelly, J. R., Clarke, G., Cryan, J. F., & Dinan, T. G. (2016). Brain-gut-microbiota axis: challenges for translation in psychiatry.Annals of Epidemiology,26(5), 366-372.
Kennedy, P. J., Clarke, G., O‘Neill, A., Groeger, J. A., Quigley, E. M. M., Shanahan, F., ... & Dinan, T. G. (2014). Cognitive performance in irritable bowel syndrome: evidence of a stress-related impairment in visuospatial memory.Psychological medicine,44(7), 1553-1566.
Kim, D. Y., & Camilleri, M. (2000). Serotonin: a mediator of the brain–gut connection.The American journal of gastroenterology,95(10), 2698-2709.
Kim, J. (1996). Philosophy of Mind. Oxford: Westview Press.
Kunze, W. A., Mao, Y. K., Wang, B., Huizinga, J. D., Ma, X., Forsythe, P., & Bienenstock, J. (2009). Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium‐dependent potassium channel opening.Journal of cellular and molecular medicine,13(8b), 2261-2270.
Luczynski, P., McVey Neufeld, K. A., Oriach, C. S., Clarke, G., Dinan, T. G., & Cryan, J. F. (2016a). Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior.International Journal of Neuropsychopharmacology,19(8).
Luczynski, P., Whelan, S. O., O'Sullivan, C., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2016b). Adult microbiota‐deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus.European Journal of Neuroscience,44(9), 2654-2666.
Martin, C. R., Osadchiy, V., Kalani, A., & Mayer, E. A. (2018). The brain-gut-microbiome axis.Cellular and molecular gastroenterology and hepatology,6(2), 133-148.
Matyssek, R., & Lüttge, U. (2013). Gaia: the planet holobiont.Nova Acta Leopoldina NF,114(391), 325-344.
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014). Gut microbes and the brain: paradigm shift in neuroscience.Journal of Neuroscience,34(46), 15490-15496.
Mayne, R., Adamatzky, A., & Jones, J. (2015). On the role of the plasmodial cytoskeleton in facilitating intelligent behavior in slime mold Physarum polycephalum.Communicative & integrative biology,8(4), e1059007.
Merker, B. (2005). The liabilities of mobility: A selection pressure for the transition to consciousness in animal evolution.Consciousness and cognition,14(1), 89-114.
Messaoudi, M., Violle, N., Bisson, J. F., Desor, D., Javelot, H., & Rougeot, C. (2011). Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers.Gut microbes,2(4), 256-261.
Nagel, T. (1974). What is it like to be a bat?.The philosophical review,83:4, 435-450.
Nakagaki, T. (2001). Smart behavior of true slime mold in a labyrinth.Research in Microbiology,152(9), 767-770.
Northoff, G. (2014). Unlocking the Brain: Volume 2: Consciousness. New York: Oxford University Press.
O’Mahony, S. M., Felice, V. D., Nally, K., Savignac, H. M., Claesson, M. J., Scully, P., ... & Marchesi, J. R. (2014). Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats.Neuroscience,277, 885-901.
Ogbonnaya, E. S., Clarke, G., Shanahan, F., Dinan, T. G., Cryan, J. F., & O’Leary, O. F. (2015). Adult hippocampal neurogenesis is regulated by the microbiome.Biological psychiatry,78(4), e7-e9.
Parke, E. C., Calcott, B., & O’Malley, M. A. (2018). A cautionary note for claims about the microbiome’s impact on the “self.”PLoS biology,16(9), e2006654.
Pockett, S. (2004). Does consciousness cause behaviour?.Journal of Consciousness Studies,11(2), 23-40.
Reid, C. R., Latty, T., Dussutour, A., & Beekman, M. (2012). Slime mold uses an externalized spatial “memory” to navigate in complex environments.Proceedings of the National Academy of Sciences,109(43), 17490-17494.
Reigstad, C. S., Salmonson, C. E., Rainey III, J. F., Szurszewski, J. H., Linden, D. R., Sonnenburg, J. L., Farrugia, G., & Kashyap, P. C. (2014). Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells.The FASEB Journal,29(4), 1395-1403.
Rohwer, F., Seguritan, V., Azam, F., & Knowlton, N. (2002). Diversity and distribution of coral-associated bacteria.Marine Ecology Progress Series,243, 1-10.
Rosenberg, E., & Zilber-Rosenberg, I. (2018). The hologenome concept of evolution after 10 years.Microbiome,6:78.
Rosenthal, D. M. (2008). Consciousness and its function.Neuropsychologia,46(3), 829-840.
Sampson, T. R., & Mazmanian, S. K. (2015). Control of brain development, function, and behavior by the microbiome.Cell host & microbe,17(5), 565-576.
Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., ... & Chesselet, M. F. (2016). Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease.Cell,167(6), 1469-1480.
Saulnier, D. M., Ringel, Y., Heyman, M. B., Foster, J. A., Bercik, P., Shulman, R. J., ... & Guarner, F. (2013). The intestinal microbiome, probiotics and prebiotics in neurogastroenterology.Gut microbes,4(1), 17-27.
Savignac, H. M., Tramullas, M., Kiely, B., Dinan, T. G., & Cryan, J. F. (2015). Bifidobacteria modulate cognitive processes in an anxious mouse strain.Behavioural brain research,287, 59-72.
Sender, R., Fuchs, S., & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body.PLoS biology,14(8), e1002533.
Seth, A. K. (2009).Functions of Consciousness. Encyclopedia of Consciousness, 279–293.doi:10.1016/b978-012373873-8.00033-5
Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G., & Cryan, J. F. (2019). Microbiota and the social brain.Science,366(6465).
Simard, S. W., Perry, D. A., Jones, M. D., Myrold, D. D., Durall, D. M., & Molina, R. (1997). Net transfer of carbon between ectomycorrhizal tree species in the field.Nature,388(6642), 579.
Smith, L. K., & Wissel, E. F. (2019). Microbes and the Mind: How Bacteria Shape Affect, Neurological Processes, Cognition, Social Relationships, Development, and Pathology.Perspectives on Psychological Science,14(3), 1-22. Available at: https://doi.org/10.1177/1745691618809379 (Accessed 26/11/2019)
Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S. (2015). A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood.Brain, behavior, and immunity,48, 258-264.
Stencel, A. (2016). The relativity of Darwinian populations and the ecology of endosymbiosis.Biology & philosophy,31(5), 619-637.
Stilling, R. M., Ryan, F. J., Hoban, A. E., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F. (2015). Microbes & neurodevelopment–Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala.Brain, behavior, and immunity,50, 209-220.
Suárez, J. (2018). The importance of symbiosis in philosophy of biology: an analysis of the current debate on biological individuality and its historical roots.Symbiosis,76(2), 77-96.
Suárez, J., & Triviño, V. (2019). A metaphysical approach to holobiont individuality: Holobionts as emergent individuals.
Thellier, M., & Lüttge, U. (2013). Plant memory: a tentative model.Plant Biology,15(1), 1-12.
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., & Mayer, E. A. (2013). Consumption of fermented milk product with probiotic modulates brain activity.Gastroenterology,144(7), 1394-1401.
Varian, B. J., Poutahidis, T., DiBenedictis, B. T., Levkovich, T., Ibrahim, Y., Didyk, E., ... & Kolandaivelu, K. (2017). Microbial lysate upregulates host oxytocin.Brain, behavior, and immunity,61, 36-49.
Vogel, D., & Dussutour, A. (2016). Direct transfer of learned behaviour via cell fusion in non-neural organisms.Proceedings of the Royal Society B: Biological Sciences,283(1845), 20162382.
Wang, X., Wang, B. R., Zhang, X. J., Xu, Z., Ding, Y. Q., & Ju, G. (2002). Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats.World journal of gastroenterology,8(3), 540-545.
Waters, C. K. (2018). Ask not “what is an individual?.” In: Bueno, O., Chen, R. L., & Fagan, M. B. (Eds.). (2018).Individuation, Process, and Scientific Practices. Oxford: Oxford University Press, 91-113.
Zijlmans, M. A., Korpela, K., Riksen-Walraven, J. M., de Vos, W. M., & de Weerth, C. (2015). Maternal prenatal stress is associated with the infant intestinal microbiota.Psychoneuroendocrinology,53, 233-245.
Zilber-Rosenberg, I., & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution.FEMS microbiology reviews,32(5), 723-735.
1.) To be fair, it is not just philosophy of mind who overslept. Other disciplines, such as psychology (with notable exceptions of e.g. Allen et al. , or Smith and Wissel ), have not reflected these findings either. Actually, the concepts of holobiont or the brain-gut-microbiome axis still remain topics mainly for biologists and are little known outside the field.
2.) The issue of germ-free animals will be discussed later.
3.) For instance, Suárez and Triviño (2019) suggest to substitute the idea of transgenerational transmission by transgenerational trait-recurrence.
4.) For the discussion of this last point see Parke et al. (2018).
5.) The vagus nerve has a significant influence on emotional, cognitive and behavioural outcomes (Smith and Wissel 2019: 11-12).
6.) As the authors stress, this study proves the possibility of translating animal data into the clinic (Carlson et al. 2018: 148) which is a huge step since most of the data of the brain-gut-microbiome research come from animal experiments.
7.) Although the microbial profile usually changes across the life span (Hopkins et al. 2002).
8.) Probiotics are live microorganisms often found in milk products and dietary supplements. On the other hand, prebiotics support the growth and survival of the gut microbiota (Evrensel and Ceylan 2015: 242).
9.) He is dealing with the notion of phenomenal consciousness (Earl 2014: 1), which is the same as in this paper.
10.) I use the word ‘intelligence’ to describe a non-automatic efficient way of solving problems.
11.) For the idea of panpsychism see e.g. Chalmers (2015).
12.) For the notion of emergence see e.g. Kim (1996).
13.) For the relational emergence theory see Elder-Vass (2010).
14.) I am very grateful to Rebeca Santano Garcia for introducing me the brain-gut-microbiota problem several years ago.