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Parieto-occipital ERP indicators of gut mechanosensation in humans

Author

Listed:
  • Ahmad Mayeli

    (Laureate Institute for Brain Research
    University of Pittsburgh)

  • Obada Al Zoubi

    (Laureate Institute for Brain Research
    Harvard Medical School/McLean Hospital)

  • Evan J. White

    (Laureate Institute for Brain Research)

  • Sheridan Chappelle

    (Laureate Institute for Brain Research)

  • Rayus Kuplicki

    (Laureate Institute for Brain Research)

  • Alexa Morton

    (Laureate Institute for Brain Research)

  • Jaimee Bruce

    (Laureate Institute for Brain Research)

  • Ryan Smith

    (Laureate Institute for Brain Research)

  • Justin S. Feinstein

    (Laureate Institute for Brain Research)

  • Jerzy Bodurka

    (Laureate Institute for Brain Research
    University of Oklahoma)

  • Martin P. Paulus

    (Laureate Institute for Brain Research
    University of Tulsa)

  • Sahib S. Khalsa

    (Laureate Institute for Brain Research
    University of Tulsa)

Abstract

Understanding the neural processes governing the human gut-brain connection has been challenging due to the inaccessibility of the body’s interior. Here, we investigated neural responses to gastrointestinal sensation using a minimally invasive mechanosensory probe by quantifying brain, stomach, and perceptual responses following the ingestion of a vibrating capsule. Participants successfully perceived capsule stimulation under two vibration conditions (normal and enhanced), as evidenced by above chance accuracy scores. Perceptual accuracy improved significantly during the enhanced relative to normal stimulation, which was associated with faster stimulation detection and reduced reaction time variability. Capsule stimulation induced late neural responses in parieto-occipital electrodes near the midline. Moreover, these ‘gastric evoked potentials’ showed intensity-dependent increases in amplitude and were significantly correlated with perceptual accuracy. Our results replicated in a separate experiment, and abdominal X-ray imaging localized most capsule stimulations to the gastroduodenal segments. Combined with our prior observation that a Bayesian model is capable of estimating computational parameters of gut-brain mechanosensation, these findings highlight a unique form of enterically-focused sensory monitoring within the human brain, with implications for understanding gut feelings and gut-brain interactions in healthy and clinical populations.

Suggested Citation

  • Ahmad Mayeli & Obada Al Zoubi & Evan J. White & Sheridan Chappelle & Rayus Kuplicki & Alexa Morton & Jaimee Bruce & Ryan Smith & Justin S. Feinstein & Jerzy Bodurka & Martin P. Paulus & Sahib S. Khals, 2023. "Parieto-occipital ERP indicators of gut mechanosensation in humans," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39058-4
    DOI: 10.1038/s41467-023-39058-4
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    References listed on IDEAS

    as
    1. Hwei-Ee Tan & Alexander C. Sisti & Hao Jin & Martin Vignovich & Miguel Villavicencio & Katherine S. Tsang & Yossef Goffer & Charles S. Zuker, 2020. "The gut–brain axis mediates sugar preference," Nature, Nature, vol. 580(7804), pages 511-516, April.
    2. Li He & Guangwei Si & Jiuhong Huang & Aravinthan D. T. Samuel & Norbert Perrimon, 2018. "Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel," Nature, Nature, vol. 555(7694), pages 103-106, March.
    3. Lukas Van Oudenhove & Philip A. Kragel & Patrick Dupont & Huynh Giao Ly & Els Pazmany & Paul Enzlin & Amandine Rubio & Chantal Delon-Martin & Bruno Bonaz & Qasim Aziz & Jan Tack & Shin Fukudo & Michik, 2020. "Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Sam Vesuna & Isaac V. Kauvar & Ethan Richman & Felicity Gore & Tomiko Oskotsky & Clara Sava-Segal & Liqun Luo & Robert C. Malenka & Jaimie M. Henderson & Paul Nuyujukian & Josef Parvizi & Karl Deisser, 2020. "Deep posteromedial cortical rhythm in dissociation," Nature, Nature, vol. 586(7827), pages 87-94, October.
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