Visceral Signals Shape Brain Dynamics and Cognition

Abstract

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. A Paradigm Shift in Cognitive Neuroscience 'The brain is bombarded by information from the environment.' This sentence, in one form or another, acts as an introduction to many textbooks and articles about perception and cognition (e.g., [1]). Although the internal environment is sometimes mentioned, the vast majority of the experimental work pertains to the processing of external stimuli. This reflects the dominant paradigm in cognitive neuroscience, where an agent collects information from the external environment via the senses and then reacts to this environment by producing actions (Figure 1A). By studying the brain, cognitive neuroscience has been highly successful at providing mechanistic explanations of behavior and at revealing the existence of hidden rules and variables, such as for instance the reward prediction error [2]. In the following we review extensions of this paradigm that include the interplay between the brain and the internal bodily environment (Figure 1B) to account for the neural implementation of cognition. More specifically, we focus on the heart and the gastrointestinal (GI) tract (see Glossary), and refer the reader to [3] for a comprehensive review of other types of somatic influences, including notably humoral and immune factors.

Skipping a beat: heartbeat-evoked potentials reflect predictions during interoceptive-exteroceptive integration

“…This is supported by studies which demonstrated the contribution of integrative interoceptive signals with visual cues to enhance body ownership and self-recognition (Aspell et al, 2013;Heydrich et al, 2018;Sel et al, 2017;Suzuki et al, 2013). Additionally, interoceptive and exteroceptive integration has been suggested to explain the generation of a first-person perspective, describing how our unified conscious experience of the external world is integrated with the experience of the self, with particular focus on interoception as a binding agent (Azzalini et al, 2019). These viewpoints, therefore, demonstrate the potential function of the integrated interoceptive and exteroceptive mechanisms observed in our study.…”

“…Therefore, measuring pure predictive signals during omissions, which reflect interoceptive and exteroceptive integration, may be useful for diagnosing dissociative disorders, schizophrenia, or anxiety (Paulus & Stein, 2010;Petzschner et al, 2017;Seth, 2013;Seth et al, 2012;Synofzik et al, 2010). Additionally, if interoceptive and exteroceptive integrative mechanisms contribute towards a unified conscious first-person perspective, then observing preserved mechanisms could be useful for diagnosing awareness in patients with disorders of consciousness (Azzalini et al, 2019). This would be advantageous because current methods of assessing awareness focus almost exclusively on responses to external stimuli, whereas assessing interoceptive and exteroceptive integration could provide a method of assessing both external perceptual and internal self-related aspects of awareness.…”

Respiration competes with theta for modulating parietal cortex neurons

“…Among them, the digestive, cardiovascular and respiratory systems are well known to exhibit rhythmicity at the ultradian timescale [6][7][8][9]. Recent research has started to unveil links between the brain and other body rhythms [12,26]. In particular, the coupling between neuronal activity and the cycles of nasal breathing has been increasingly recognized [14,15,19].…”

“…Interestingly, recent studies are starting to unveil relationships between oscillatory activity produced by different organ systems. For instance, Tallon-Baudry and collaborators have shown that ascending signals from the heart and gastrointestinal tract modulate brain dynamics and affect perception, emotion and cognition [10][11][12][13]. In particular, the EEG alpha rhythm was shown to be modulated by the phase of the gastric cycle [7].…”

Measuring the Brain-Gut Axis in Psychological Sciences: A Necessary Challenge

“…The paradigmatic turn can be evidenced in an increment in scientific research considering both brain and bodily signals, such as the heart (Pollatos et al, 2007b;Villena-Gonzalez et al, 2017), respiration (Yuan et al, 2013;Ahani et al, 2014), gastrointestinal (Richter et al, 2017;Rebollo et al, 2018), and muscular dynamics (Boonstra et al, 2009(Boonstra et al, , 2015Kerkman et al, 2018). Recent evidence has furthermore revealed the many ways in which psychological processes influence the body, and vice-versa, with behavioral and health implications (Pollatos et al, 2007a;Mattson, 2015;Babo-Rebelo et al, 2016;Azzalini et al, 2019).…”