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

Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatiotemporal 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, both genders), 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 (RSNs). 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.SIGNIFICANCE STATEMENT While there is growing interest for brain-body communication in general and brain-viscera communication in particular, little is known about how the brain interacts with the gastric rhythm, the slow electrical rhythm continuously produced in the stomach. Here, we show in human participants at rest that the gastric network, composed of brain regions synchronized with delays to the gastric rhythm, includes all motor and sensory (vision, audition, touch and interoception, olfaction) regions, but only few of the transmodal regions associated with higher-level cognition. Such results prompt for a reconsideration of the classical view of cortical organization, where the different sensory modalities are considered as relatively independent modules.

Conscious Vision Proceeds from Global to Local Content in Goal-Directed Tasks and Spontaneous Vision.

UNLABELLED: The reverse hierarchy theory (Hochstein and Ahissar, 2002) makes strong, but so far untested, predictions on conscious vision. In this theory, local details encoded in lower-order visual areas are unconsciously processed before being automatically and rapidly combined into global information in higher-order visual areas, where conscious percepts emerge. Contingent on current goals, local details can afterward be consciously retrieved. This model therefore predicts that (1) global information is perceived faster than local details, (2) global information is computed regardless of task demands during early visual processing, and (3) spontaneous vision is dominated by global percepts. We designed novel textured stimuli that are, as opposed to the classic Navon's letters, truly hierarchical (i.e., where global information is solely defined by local information but where local and global orientations can still be manipulated separately). In line with the predictions, observers were systematically faster reporting global than local properties of those stimuli. Second, global information could be decoded from magneto-encephalographic data during early visual processing regardless of task demands. Last, spontaneous subjective reports were dominated by global information and the frequency and speed of spontaneous global perception correlated with the accuracy and speed in the global task. No such correlation was observed for local information. We therefore show that information at different levels of the visual hierarchy is not equally likely to become conscious; rather, conscious percepts emerge preferentially at a global level. We further show that spontaneous reports can be reliable and are tightly linked to objective performance at the global level. SIGNIFICANCE STATEMENT: Is information encoded at different levels of the visual system (local details in low-level areas vs global shapes in high-level areas) equally likely to become conscious? We designed new hierarchical stimuli and provide the first empirical evidence based on behavioral and MEG data that global information encoded at high levels of the visual hierarchy dominates perception. This result held both in the presence and in the absence of task demands. The preferential emergence of percepts at high levels can account for two properties of conscious vision, namely, the dominance of global percepts and the feeling of visual richness reported independently of the perception of local details.

Vagus nerve stimulation increases stomach-brain coupling via a vagal afferent pathway.

BACKGROUND: Maintaining energy homeostasis is vital and supported by vagal signaling between digestive organs and the brain. Previous research has established a gastric network in the brain that is phase synchronized with the rhythm of the stomach, but tools to perturb its function were lacking. OBJECTIVE: To evaluate whether stomach-brain coupling can be acutely increased by non-invasively stimulating vagal afferent projections to the brain. METHODS: Using a single-blind randomized crossover design, we investigated the effect of acute right-sided transcutaneous auricular vagus nerve stimulation (taVNS) versus sham stimulation on stomach-brain coupling. RESULTS: In line with preclinical research, taVNS increased stomach-brain coupling in the nucleus of the solitary tract (NTS) and the midbrain while boosting coupling across the brain. Crucially, in the cortex, taVNS-induced changes in coupling occurred primarily in transmodal regions and were associated with changes in hunger ratings as indicators of the subjective metabolic state. CONCLUSIONS: taVNS increases stomach-brain coupling via an NTS-midbrain pathway that signals gut-induced reward, indicating that communication between the brain and the body is effectively modulated by vago-vagal signaling. Such insights may help us better understand the role of vagal afferents in orchestrating the recruitment of the gastric network which could pave the way for novel neuromodulatory treatments.

Influence of visual food cues on autonomic activity and craving.

In this study, we tested the hypothesis that autonomic control of the stomach is related to craving and is modulated by visual food cues. Twenty-nine healthy human participants were shown pictures of either high- or low-appeal food, as well as non-food pictures, and were asked to rate how much they wanted to eat each item using a 7-point Likert scale. Simultaneously, the electrogastrogram, electrocardiogram, electrodermal activity, respiration rate, and pupil diameter were recorded. After the ingestion of a 500-kcal liquid meal, participants were asked to perform the task a second time. Despite changes in craving ratings, we did not find changes in the amplitude of the gastric rhythm, but we found increases in pupil diameter for the high appeal food pictures. Moreover, craving ratings were mostly related to increases in pupil and tonic electrodermal activity, compatible with an increase in arousal and a heightened motivational response to food.

Electrogastrography for psychophysiological research: Practical considerations, analysis pipeline, and normative data in a large sample.

Electrogastrography (EGG) is the noninvasive electrophysiological technique used to record gastric electrical activity by means of cutaneous electrodes placed on the abdomen. EGG has been so far mostly used in clinical studies in gastroenterology, but it represents an attractive method to study brain-viscera interactions in psychophysiology. Compared to the literature on electrocardiography for instance, where practical recommendations and normative data are abundant, the literature on EGG in humans remains scarce. The aim of this article is threefold. First, we review the existing literature on the physiological basis of the EGG, pathways of brain-stomach interactions, and experimental findings in the cognitive neuroscience and psychophysiology literature. We then describe practical issues faced when recording the EGG in young healthy participants, from data acquisition to data analysis, and propose a semi-automated analysis pipeline together with associated MATLAB code. The analysis pipeline aims at identifying a regular rhythm that can be safely attributed to the stomach, through multiple steps. Finally, we apply these recording and analysis procedures in a large sample (N = 117) of healthy young adult male and female participants in a moderate (<5 hr) to prolonged (>10 hr) fasting state to establish the normative distribution of several EGG parameters. Our results are overall congruent with the clinical gastroenterology literature, but suggest using an electrode coverage extending to lower abdominal locations than current clinical guidelines. Our results indicate a marginal difference in EGG peak frequency between male and female participants, and that the gastric rhythm becomes more irregular after prolonged fasting.

Visceral Signals Shape Brain Dynamics and Cognition.

Most research in cognitive neuroscience explores how external stimuli are processed by the brain. However, the brain also receives input from the internal body. We discuss here how the heart and gastrointestinal (GI) tract intrinsically generate their own electrical activity, thereby continuously sending information to the brain. These ongoing ascending signals actively shape brain dynamics at rest, complementing canonical resting-state networks (RSNs). Cardiac signals also influence the processing of external sensory information and the production of spontaneous, internal cognition. These findings are discussed in relation to interpretative frameworks regarding the functional role of visceral inputs. This active field of research offers a unique opportunity to draw new theories blurring the border between cognition, emotion, and consciousness, as well as between mind and body.

Stomach-brain synchrony reveals a novel, delayed-connectivity resting-state network in humans.

Resting-state networks offer a unique window into the brain's functional architecture, but their characterization remains limited to instantaneous connectivity thus far. Here, we describe a novel resting-state network based on the delayed connectivity between the brain and the slow electrical rhythm (0.05 Hz) generated in the stomach. The gastric network cuts across classical resting-state networks with partial overlap with autonomic regulation areas. This network is composed of regions with convergent functional properties involved in mapping bodily space through touch, action or vision, as well as mapping external space in bodily coordinates. The network is characterized by a precise temporal sequence of activations within a gastric cycle, beginning with somato-motor cortices and ending with the extrastriate body area and dorsal precuneus. Our results demonstrate that canonical resting-state networks based on instantaneous connectivity represent only one of the possible partitions of the brain into coherent networks based on temporal dynamics.