Brain–stomach coupling: Anatomy, functions, and future avenues of research

Rebollo, Ignacio; Wolpert, Nicolai; Tallon‐Baudry, Catherine

doi:10.1016/j.cobme.2021.100270

Cited by 22 publications

(30 citation statements)

References 45 publications

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“…Whether and how our findings pertain to interoceptive prediction models ( Barrett and Simmons, 2015 ; Petzschner et al, 2021 ) remains an open question, since neither the spatial resolution nor the gradients ( Margulies et al, 2016 ; Huntenburg et al, 2018 ) we used provide information on the laminar origin of gastric-BOLD coupling. Finally, neuromodulation might also be involved ( Rinaman and Schwartz, 2004 ; Rebollo et al, 2021 ). In particular, activity in the locus coeruleus, the main source of norepinephrine to the forebrain, is modulated by gastric, colonic and bladder distension ( Elam et al, 1986 ; Saito et al, 2002 ), inducing fluctuations in arousal that can also be obtained with distension of the small intestine ( Kukorelli and Juhász, 1977 ).…”

Section: Discussionmentioning

confidence: 99%

The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest

Rebollo

Tallon‐Baudry

2022

J. Neurosci.

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Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatio-temporal organization of spontaneous brain activity. Here, we follow up on the discovery of the gastric restingstate network (Rebollo et al, 2018), composed of brain regions in which the fMRI signal is phasesynchronized to the slow (0.05 Hz) electrical rhythm of the stomach. Using a larger sample size (n=63 human participants, both genders), we further characterize the anatomy and effect sizes of gastricbrain coupling across resting-state networks, a fine grained cortical parcellation, as well as along the main gradients of cortical organization. Most (67%) of the gastric network is included in the somatomotor-auditory (38%) and visual (29%) resting state networks. Gastric brain coupling also occurs in the granular insula and, to a lesser extent, in the piriform cortex. Thus, all sensory and motor cortices corresponding to both exteroceptive and interoceptive modalities are coupled to the gastric rhythm during rest. Conversely, little gastric-brain coupling occurs in cognitive networks and transmodal regions. These results suggest not only that gastric rhythm and sensory-motor processes are likely to interact, but also that gastric-brain coupling might be a mechanism of sensory and motor integration that mostly bypasses cognition, complementing the classical hierarchical organization of the human brain.

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Section: Discussionmentioning

confidence: 99%

The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest

Rebollo

Tallon‐Baudry

2022

J. Neurosci.

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“…For instance, direct connections have been reported between secondary somatosensory cortex to auditory regions, between visual area MT and primary somatosensory (Cappe & Barone, 2005). Finally, neuromodulation might also be involved (Rebollo et al, 2021; Rinaman & Schwartz, 2004). In particular, activity in the locus coeruleus, the main source of norepinephrine to the forebrain, is modulated by gastric, colonic and bladder distension (Elam et al, 1986; Saito et al, 2002), inducing fluctuations in arousal that can also be obtained with distension of the small intestine (Kukorelli & Juhász, 1977).…”

Section: Discussionmentioning

confidence: 99%

“…Direct connections have been reported between secondary somatosensory cortex to auditory regions, between visual area MT and primary somatosensory (Cappe & Barone, 2005) and between auditory regions and primary (Falchier et al, 2002) and secondary (Rockland & Ojima, 2003) visual cortices. Another potential source of visceral signals to thalamocortical circuits are the noradrenergic, serotoninergic, cholinergic, dopaminergic, histaminic and glutamatergic neuromodulatory nuclei, which receive anatomical projections from the stomach via the parabrachial nuclei, and provide separate inputs to the thalamus and cortex (Rebollo et al, 2021;Rinaman & Schwartz, 2004). To the best of our knowledge, direct functional evidence for a link between the spontaneous gastric rhythm and neuromodulation does not exist.…”

Section: Anatomical Pathways For Gastric Brain Couplingmentioning

confidence: 98%

The sensory and motor components of the cortical hierarchy are coupled to the rhythm of the stomach during rest

Rebollo

Tallon‐Baudry

2021

Preprint

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Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatio-temporal organization of spontaneous brain activity. Here, we follow up on the discovery of the gastric resting-state network (Rebollo et al, 2018), composed of brain regions in which the fMRI signal is phase-synchronized to the slow (0.05 Hz) electrical rhythm of the stomach. Using a larger sample size (n=63 human participants), we further characterize the anatomy and effect sizes of gastric-brain coupling across resting-state networks, a fine grained cortical parcellation, as well as along the main gradients of cortical organization. Most (67%) of the gastric network is included in the somato-motor-auditory (38%) and visual (29%) resting state networks. Gastric brain coupling also occurs in the granular insula and, to a lesser extent, in the piriform cortex. Thus, all sensory and motor cortices corresponding to both exteroceptive and interoceptive modalities are coupled to the gastric rhythm during rest. Conversely, little gastric-brain coupling occurs in cognitive networks and transmodal regions. These results suggest not only that gastric rhythm and sensory-motor processes are likely to interact, but also that gastric-brain coupling might be a mechanism of sensory and motor integration that mostly bypasses cognition, complementing the classical hierarchical organization of the human brain.

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“…Such interactions are partly mediated by bidirectional neural signaling along the so-called stomach-brain neuroaxis (Powley et al, 2019; Liu et al, 2018; Kaelberer et al, 2018; Levinthal and Strick, 2020; Browning and Travagli, 2014; Holtmann and Talley, 2014). It includes neural circuits and pathways in both peripheral and central nervous systems (Powley et al, 2019; Mayer et al, 2019; Rebollo et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

The vagus nerve mediates the stomach-brain coherence in rats

Cao

Wang

Chen

et al. 2022

Preprint

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Interactions between the brain and the stomach shape both cognitive and digestive functions. Recent human studies report spontaneous synchronization between brain activity and gastric slow waves in the resting state. However, this finding has not been replicated in any animal models. The neural pathways underlying this apparent stomach-brain synchrony is also unclear. Here, we performed functional magnetic resonance imaging while simultaneously recording body-surface gastric slow waves from anesthetized rats in the fasting vs. postprandial conditions and performed a bilateral cervical vagotomy to assess the role of the vagus nerve. The coherence between brain fMRI signals and gastric slow waves was found in a distributed gastric network, including subcortical and cortical regions in the sensory, motor, and limbic systems. The stomach-brain coherence was largely reduced by the bilateral vagotomy and was different between the fasting and fed states. These findings suggest that the vagus nerve mediates the spontaneous coherence between brain activity and gastric slow waves, which is likely a signature of real-time stomach-brain interactions. However, its functional significance remains to be established.

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Brain–stomach coupling: Anatomy, functions, and future avenues of research

Cited by 22 publications

References 45 publications

The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest

The Sensory and Motor Components of the Cortical Hierarchy Are Coupled to the Rhythm of the Stomach during Rest

The sensory and motor components of the cortical hierarchy are coupled to the rhythm of the stomach during rest

The vagus nerve mediates the stomach-brain coherence in rats

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