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EDITORIAL article

Front. Neurosci., 15 April 2024
Sec. Gut-Brain Axis
This article is part of the Research Topic The Organs of Sensibility: Multimodal Sensing Within the Microbiota-Gut-Brain Axis and How it Drives Physiology, Behavior and Perception View all 5 articles

Editorial: The organs of sensibility: multimodal sensing within the microbiota-gut-brain axis and how it drives physiology, behavior and perception

\r\nRim Hassouna
Rim Hassouna1*Lukas Van Oudenhove,,,,Lukas Van Oudenhove2,3,4,5,6Boris Le NevBoris Le Nevé1Ann-Sophie Barwich,Ann-Sophie Barwich7,8
  • 1Danone Nutricia Research, Danone Global Research & Innovation Center, Gif-sur-Yvette, France
  • 2Translational Research Center for Gastrointestinal Disorders, Katholieke Universiteit Leuven, Leuven, Belgium
  • 3Laboratory for Brain-Gut Axis Studies, Translational Research Center for Gastrointestinal Disorders, Katholieke Universiteit Leuven, Leuven, Belgium
  • 4Leuven Brain Institute, Katholieke Universiteit Leuven, Leuven, Belgium
  • 5Consultation-Liaison Psychiatry, University Psychiatric Centre Katholieke Universiteit Leuven Campus Gasthuisberg, Leuven, Belgium
  • 6Cognitive and Affective Neuroscience Laboratory, Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH, United States
  • 7Cognitive Science Program, Indiana University, Bloomington, IN, United States
  • 8Department of History and Philosophy of Science and Medicine, Indiana University, Bloomington, IN, United States

An exhilarating pace has been set in the exploration of the microbiota-gut-brain axis (hereafter referred to with the acronym MGBA). A growing body of research has laid bare the profound impact of our gut on the brain's workings, neural dynamics, and our behaviors (Valles-Colomer et al., 2019; Radjabzadeh et al., 2022). However the converse is equally true. Our emotional states and perceptions also impact gastrointestinal functions, highlighting a complex, bidirectional relationship that deepens our insight into mind-body connections (Cryan et al., 2019; Brushett et al., 2023).

Still, we are confronted with a critical gap in our understanding of the cellular and molecular mechanisms driving the gut-brain communication axis, especially when it comes to humans. A significant roadblock in our quest for understanding is the scarcity of non-invasive tools tailored for clinical research. This shortage means we are mostly leaning on data from animal models and translational studies, with significant results remaining scarce (Kelly et al., 2017; Margolis et al., 2021).

Navigating this two-way street reveals a maze of interacting components, adding layers of complexity and challenge. It is becoming obvious that cracking the code of the MGBA's varied communication mechanisms demands a deeper grasp of how the gut senses its surroundings. Interoceptive signals play a key role in a host of functions like energy balance, nutrient detection, hunger and satiety cues, gut stability, and the interaction between host and microbiota. Just as crucial is understanding how emotions, stress, and the broader external environment influence the digestive system.

Our goal was to focus on the various ways signals are detected, not just in the brain but also in the gut. This Research Topic includes an original study, a theoretical piece, a review, and a perspective, each offering different insights and fresh outlooks on these issues. These pieces cover three key areas: the immune system, mental states, and the digestive system.

The immune system plays a pivotal role in the dialogue within the MGBA. How the immune system affects visceral pain is the focus of Pawlik et al.'s investigation. Specifically, they explore how pro-inflammatory cytokines circulating in the blood of healthy people affect individual differences in sensing internal visceral signals. Mental states affecting the MGBA is the central focus of the following two pieces. Han et al. give us a comprehensive overview of how the MGBA connects to emotion-related disorders, with an eye on depression. They make the case for deeper exploration into the MGBA's workings to improve our investigation and treatment of gut-brain disorders. Within the same line of research and looking at MGBA through the prism of short-chain fatty acids, Mansuy-Aubert et al. illuminate how these fatty acids could revolutionize human health in ways that affect metabolic and psychological wellness.

Finally, how should we frame our understanding of the gut within the gut-brain axis? Boem et al. expand on the notion that to fully understand cognition and perception, we must view the digestive system as a multifaceted organ/ecosystem, integrating the enteric nervous system, endocrine system, immune system, microbiota, as well as gut tissue and mucosal structures.

Taken together, this accumulation of knowledge showcases the possibility of new investigative pathways–pathways leading to enhanced well-being, sharper diagnostic processes, and targeted treatments for the intricate disorders profoundly linked to the workings of the MGBA. With a blend of hope and anticipation, we hope these perspectives will meet your interest.

Author contributions

RH: Writing – original draft, Writing – review & editing. LV: Writing – original draft, Writing – review & editing. BL: Writing – original draft, Writing – review & editing. A-SB: Writing – original draft, Writing – review & editing.

Funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.

Conflict of interest

RH and BL were employed by company Danone Global Research & Innovation Center.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Brushett, S., Gacesa, R., Vich Vila, A., Brandao Gois, M. F., Andreu-Sanchez, S., Swarte, J. C., et al. (2023). Gut feelings: the relations between depression, anxiety, psychotropic drugs and the gut microbiome. Gut Microbes 15, 2281360. doi: 10.1080/19490976.2023.2281360

PubMed Abstract | Crossref Full Text | Google Scholar

Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., et al. (2019). The microbiota-gut-brain axis. Physiol. Rev. 99, 1877–2013. doi: 10.1152/physrev.00018.2018

Crossref Full Text | Google Scholar

Kelly, J. R., Allen, A. P., Temko, A., Hutch, W., Kennedy, P. J., Farid, N., et al. (2017). Lost in translation? The potential psychobiotic Lactobacillus rhamnosus (JB-1) fails to modulate stress or cognitive performance in healthy male subjects. Brain Behav. Immun. 61, 50–59. doi: 10.1016/j.bbi.2016.11.018

PubMed Abstract | Crossref Full Text | Google Scholar

Margolis, K. G., Cryan, J. F., and Mayer, E. A. (2021). The microbiota-gut-brain axis: from motility to mood. Gastroenterology 160, 1486–1501. doi: 10.1053/j.gastro.2020.10.066

PubMed Abstract | Crossref Full Text | Google Scholar

Radjabzadeh, D., Bosch, J. A., Uitterlinden, A. G., Zwinderman, A. H., Ikram, M. A., van Meurs, J. B. J., et al. (2022). Gut microbiome-wide association study of depressive symptoms. Nat. Commun. 13, 7128. doi: 10.1038/s41467-022-34502-3

PubMed Abstract | Crossref Full Text | Google Scholar

Valles-Colomer, M., Falony, G., Darzi, Y., Tigchelaar, E. F., Wang, J., Tito, R. Y., et al. (2019). The neuroactive potential of the human gut microbiota in quality of life and depression. Nat. Microbiol. 4, 623–632. doi: 10.1038/s41564-018-0337-x

PubMed Abstract | Crossref Full Text | Google Scholar

Keywords: perception, microbiota-gut-brain axis, sensing, behavior, physiology

Citation: Hassouna R, Van Oudenhove L, Le Nevé B and Barwich A-S (2024) Editorial: The organs of sensibility: multimodal sensing within the microbiota-gut-brain axis and how it drives physiology, behavior and perception. Front. Neurosci. 18:1380039. doi: 10.3389/fnins.2024.1380039

Received: 31 January 2024; Accepted: 05 February 2024;
Published: 15 April 2024.

Edited and reviewed by: Paul Forsythe, University of Alberta, Canada

Copyright © 2024 Hassouna, Van Oudenhove, Le Nevé and Barwich. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Rim Hassouna, rim.hassouna@danone.com

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.