Relationship between psychosocial stress-induced prefrontal cortex activity and gut microbiota in healthy Participants-A functional near-infrared spectroscopy study

Kao Yamaoka; Nobuo Uotsu; Eiichi Hoshino

doi:10.1016/j.ynstr.2022.100479

Relationship between psychosocial stress-induced prefrontal cortex activity and gut microbiota in healthy Participants-A functional near-infrared spectroscopy study

Neurobiol Stress. 2022 Aug 12:20:100479. doi: 10.1016/j.ynstr.2022.100479. eCollection 2022 Sep.

Authors

Kao Yamaoka¹, Nobuo Uotsu¹, Eiichi Hoshino²

Affiliations

¹ FANCL Corporation Research Institute, 12-13 Kamishinano, Totsuka-ku, Yokohama, Kanagawa, 244-0806, Japan.
² Keio University Global Research Institute (KGRI), 2-15-45 Mita, Minato-ku, Tokyo, 108-8345, Japan.

Abstract

Brain and gut microbes communicate in a bidirectional manner with each affecting a person's response to psychosocial stress. Although human studies demonstrated that the intake of probiotics can alter stress-related behavior in both patients and healthy participants, the association between stress-related brain functions and the gut microbiota has mostly been investigated in patients with depression. However, the response to psychosocial stress differs, even among healthy individuals, and elucidating the natural state of the gut microbiota would broaden the understanding of responses to psychosocial stress. We investigated the relationship between psychosocial stress response in the prefrontal cortex and the abundance of gut microbes in healthy male participants. The participants were exposed to psychosocial stress during a task while brain activation data were recorded using functional near-infrared spectroscopy. The heart rate and subjective stress were recorded, and fecal samples were collected. The stressful condition was accompanied by high subjective stress, high heart rate, and higher prefrontal activation in the right pre-motor cortex/supplementary motor area, right dorsolateral prefrontal cortex, right frontal pole, and right inferior prefrontal gyrus. The psychosocial stress response in the prefrontal cortex was also associated with changes in the gut microbiota abundance. The abundance of Alistipes, Clostridium IV, Clostridium XI, Faecalibacterium, and Blautia in healthy participants who had high psychosocial stress resembled that noted in patients with depression. These results suggest that the gut microbiota differs, among healthy participants, depending on the psychosocial stress response. We believe that this study is the first to report a direct relationship between brain function and the gut microbiota in healthy participants, and our findings would shed a new light on this field in the near future.

Keywords: ANOVA, Analysis of variance; BD, Bipolar disorder; BMI, Body mass index; CH, Channel; CRH, Corticotropin-releasing hormone; DNA, Deoxynucleic acid; Depression; FP, Frontal pole; Functional near-infrared spectroscopy; GABA, Gamma Amino Butyric Acid; Gut microbiome; HPA-axis, Hypothalamic-pituitary-adrenal axis; IFG, Inferior prefrontal gyrus; MDD, Major depressive disorder; MIST, Montreal Imaging Stress Task; PANAS, Positive and Negative Affect Schedule; PET, Positron emission tomography; PFC, Prefrontal cortex; PMC/SMA, Pre-motor cortex/supplementary motor area; POMS2, Profile of Mood States 2 short version; Prefrontal cortex; Psychosocial stress; SSES, State Self-Esteem Scale; STAI, State-Trait Anxiety Inventory; VAS, Visual analog scale; bpm, Beat per minute; deoxy-Hb, Deoxygenated hemoglobin; dlPFC, Dorsolateral prefrontal cortex; fMRI, Functional magnetic resonance imaging; fNIRS, Functional near-infrared spectroscopy; oxy-Hb, Oxygenated hemoglobin.