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Neural indicators of human gut feelings

Ahmad Mayeli, Obada Al Zoubi, Evan J. White, Sheridan Chappelle, Rayus Kuplicki, Ryan Smith, Justin S. Feinstein, Jerzy Bodurka, View ORCID ProfileMartin P. Paulus, View ORCID ProfileSahib S. Khalsa
doi: https://doi.org/10.1101/2021.02.11.430867
Ahmad Mayeli
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Obada Al Zoubi
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Evan J. White
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Sheridan Chappelle
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Rayus Kuplicki
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Ryan Smith
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Justin S. Feinstein
1Laureate Institute for Brain Research, Tulsa, OK, United States
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Jerzy Bodurka
1Laureate Institute for Brain Research, Tulsa, OK, United States
2Stephenson School of Biomedical Engineering, University of Oklahoma, Tulsa, OK, United States
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Martin P. Paulus
1Laureate Institute for Brain Research, Tulsa, OK, United States
3Oxley College of Health Sciences, University of Tulsa, Tulsa, OK, United States
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  • ORCID record for Martin P. Paulus
Sahib S. Khalsa
1Laureate Institute for Brain Research, Tulsa, OK, United States
3Oxley College of Health Sciences, University of Tulsa, Tulsa, OK, United States
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  • ORCID record for Sahib S. Khalsa
  • For correspondence: skhalsa@laureateinstitute.org
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Abstract

Understanding the neural processes that govern the human gut-brain connection has been challenging due to the inaccessibility of the body’s interior. In this study, we aimed to identify neural responses to gastrointestinal sensation (i.e., the neural basis of ‘gut feelings’) in healthy humans using a minimally invasive mechanosensory probe. Combining electroencephalography and electrogastrography with signal detection theory measures, we quantified brain, stomach, and perceptual (button-press) responses following the ingestion of a vibrating capsule. The relationship between vibration strength and perceptual sensitivity was evaluated using two stimulation conditions (normal and enhanced). Most individuals successfully perceived capsule stimulation in both conditions, as evidenced by above chance accuracy scores. Perceptual accuracy improved significantly during the enhanced relative to normal stimulation, which was associated with faster reaction time and reduced reaction time variability. Stomach stimulation induced responses in a cluster of parieto-occipital leads near the midline via a late positive potential emerging 300-600 milliseconds after stimulation onset. Moreover, these ‘gastric evoked potentials’ showed dose-dependent increases in amplitude and were significantly correlated with perceptual accuracy. Our findings are consistent with recent neurogastric and optogenetic studies demonstrating a role for posteromedial cortices in gastrointestinal interoception and body dissociation and highlight a unique form of enterically-focused sensory monitoring within the human brain. Overall, these results show that this minimally invasive approach could serve as a useful tool for understanding gut-brain interactions in healthy and clinical populations.

Significance Statement The human brain continuously receives input from the stomach and intestines. These sensations are intuitively incorporated as ‘gut feelings’ into decision-making during daily life, yet we still know very little about how the brain processes gut signals. Here, we developed a minimally invasive approach to studying human gut feelings. In healthy individuals we found that an ingestible vibrating capsule produced reliable changes in both stomach sensation and gastric-evoked brain activity. These changes were significantly associated, in a dose-dependent fashion. We propose that this approach provides an opportunity to better understand the role of gut-related symptoms in human pathological conditions and might yield fundamental insights into how gut feelings are communicated to the human brain.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: The authors declare that they have no competing interests.

  • Abbreviations

    (CPM)
    Cycles per minute,
    (EEG)
    Electroencephalogram,
    (EGG)
    Electrogastrogram,
    (ERP)
    Evoked response potential,
    (FP)
    False positive,
    (HR)
    Hit rate,
    (LPP)
    Late positive potential,
    (M)
    Mean,
    (μV)
    Microvolts,
    (STAI)
    Spielberger State Trait Anxiety Inventory,
    (STD)
    Standard deviation
  • Copyright 
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    Posted February 13, 2021.
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    Neural indicators of human gut feelings
    Ahmad Mayeli, Obada Al Zoubi, Evan J. White, Sheridan Chappelle, Rayus Kuplicki, Ryan Smith, Justin S. Feinstein, Jerzy Bodurka, Martin P. Paulus, Sahib S. Khalsa
    bioRxiv 2021.02.11.430867; doi: https://doi.org/10.1101/2021.02.11.430867
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    Neural indicators of human gut feelings
    Ahmad Mayeli, Obada Al Zoubi, Evan J. White, Sheridan Chappelle, Rayus Kuplicki, Ryan Smith, Justin S. Feinstein, Jerzy Bodurka, Martin P. Paulus, Sahib S. Khalsa
    bioRxiv 2021.02.11.430867; doi: https://doi.org/10.1101/2021.02.11.430867

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