Nutrient infusion evoked magnetic resonance imaging signal in the human hypothalamus

ABSTRACT

Background

The hypothalamus receives ingested nutrient information via ascending gut-related projections and plays a significant role in the regulation of food intake. Human neuroimaging studies have observed changes in the activity or connectivity of the hypothalamus in response to nutrient ingestion. However, previous neuroimaging studies have not yet assessed differences in temporal changes of hypothalamic responses to various nutrients in humans. Thus a repeated measures functional magnetic resonance imaging (fMRI) study using 30-min scans was designed to examine differences in hypothalamic responses to various nutrients.

Methods

In this study, 18 healthy adults (mean age, 22.4 years; standard deviation, 4.8; age range, 19–39 years; 11 males and seven females) underwent fMRI sessions. On the day of each session, one of the four solutions (200 ml of monosodium glutamate, glucose, safflower oil emulsion, or saline) was administered to participants while fMRI scanning.

Results

Infused amino acid and glucose, but not lipid emulsion, increased lateral hypothalamic responses as compared to a saline infusion ([x, y, z] = [4, −4, −10], z = 2.96). In addition, only hypothalamic responses to saline, but not those to the infusion of other nutrients, elicited a subjective sensation of hunger.

Conclusion

These findings suggest that lateral hypothalamic responses to ingested nutrients may mediate homeostatic sensations in humans.

KEYWORDS:

• Gut–brain axis
• hypothalamus
• functional MRI
• monosodium glutamate
• glucose
• lipid emulsion
• appetite
• post-prandial nutrient information

Acknowledgments

The authors would like to thank all members of our laboratory for their aid in MRI data collection. The authors also thank Yukiko Yamada for x-ray examination.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

The data presented in this study are available upon request.

Authors’ contributions

Y.N. designed the research. Y.N. and M.T. collected fMRI data. Y.I. and S.Y. assisted the nasogastric tube placement. Y.N. performed statistical analysis and wrote the original draft. Y.N. and S.K reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Additional information

Funding

This research was supported by the Tojuro Iijima Foundation for Food Science and Technology, the Uehara Memorial Foundation, the Society for Research on Umami Taste, and the Japan Agency for Medical Research and Development (AMED; JP20dm0307001 and JP20dm0307004). This study was also supported by the UTokyo Center for Integrative Science of Human Behavior (CiSHuB) and the World Premier International Research Center for Neurointelligence (WPI-IRCN).

Notes on contributors

Yuko Nakamura

Yuko Nakamura is a project assistant professor at the UTokyo Center for Integrative Science of Human Behavior (CiSHuB), Tokyo, Japan. She obtained a doctoral degree and Doctor of Dental Surgery at Kyushu University, and since then, has dedicated herself to research about central gustatory circuits in humans.

Mariko Takahashi

Mariko Takahashi has obtained a doctoral degree at the University of Tokyo and works as a research assistant for neuroimaging studies.

Yukiko Inoue

Yukiko Inoue has obtained a doctoral degree and Doctor of Medicine at the University of Tokyo and works as a physician at the University of Tokyo Health Service Center. Her area of expertise is the research of hepatic regeneration.

Shintaro Yanagimoto

Shintaro Yanagimoto has obtained a doctoral degree and Doctor of Medicine at the University of Tokyo, and dedicated himself to public health research.

Kazuo Okanoya

Kazuo Okanoya has obtained a doctoral degree at the University of Tokyo and dedicated himself to research in cognitive neuroscience.

Shinsuke Koike

Shinsuke Koike has obtained a doctoral degree and Doctor of Medicine at the University of Tokyo and dedicated himself to research in psychiatric disorders.