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      Brain-heart interactions in the neurobiology of consciousness

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          Abstract

          Recent experimental evidence on patients with disorders of consciousness revealed that observing brain-heart interactions helps to detect residual consciousness, even in patients with absence of behavioral signs of consciousness. Those findings support hypotheses suggesting that visceral activity is involved in the neurobiology of consciousness, and sum to the existing evidence in healthy participants in which the neural responses to heartbeats reveal perceptual and self-consciousness. More evidence obtained through mathematical modeling of physiological dynamics revealed that emotion processing is prompted by an initial modulation from ascending vagal inputs to the brain, followed by sustained bidirectional brain-heart interactions. Those findings support long-lasting hypotheses on the causal role of bodily activity in emotions, feelings, and potentially consciousness. In this paper, the theoretical landscape on the potential role of heartbeats in cognition and consciousness is reviewed, as well as the experimental evidence supporting these hypotheses. I advocate for methodological developments on the estimation of brain-heart interactions to uncover the role of cardiac inputs in the origin, levels, and contents of consciousness. The ongoing evidence depicts interactions further than the cortical responses evoked by each heartbeat, suggesting the potential presence of non-linear, complex, and bidirectional communication between brain and heartbeat dynamics. Further developments on methodologies to analyze brain-heart interactions may contribute to a better understanding of the physiological dynamics involved in homeostatic-allostatic control, cognitive functions, and consciousness.

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          Highlights

          • Neural responses to heartbeats reveal residual consciousness after brain damage.

          • Brain-heart interactions (BHI) may be involved in the neurobiology of consciousness.

          • Emotions and feelings imply bidirectional BHI and are prompted by ascending vagal inputs.

          • Developments on BHI measurement may help to uncover further links with consciousness.

          • Hypotheses on the role of BHI in consciousness should consider complex interactions.

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          The free-energy principle: a unified brain theory?

          A free-energy principle has been proposed recently that accounts for action, perception and learning. This Review looks at some key brain theories in the biological (for example, neural Darwinism) and physical (for example, information theory and optimal control theory) sciences from the free-energy perspective. Crucially, one key theme runs through each of these theories - optimization. Furthermore, if we look closely at what is optimized, the same quantity keeps emerging, namely value (expected reward, expected utility) or its complement, surprise (prediction error, expected cost). This is the quantity that is optimized under the free-energy principle, which suggests that several global brain theories might be unified within a free-energy framework.
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            How do you feel--now? The anterior insula and human awareness.

            The anterior insular cortex (AIC) is implicated in a wide range of conditions and behaviours, from bowel distension and orgasm, to cigarette craving and maternal love, to decision making and sudden insight. Its function in the re-representation of interoception offers one possible basis for its involvement in all subjective feelings. New findings suggest a fundamental role for the AIC (and the von Economo neurons it contains) in awareness, and thus it needs to be considered as a potential neural correlate of consciousness.
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              Interoception: the sense of the physiological condition of the body.

              Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.
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                Author and article information

                Contributors
                Journal
                Curr Res Neurobiol
                Curr Res Neurobiol
                Current Research in Neurobiology
                Elsevier
                2665-945X
                06 August 2022
                2022
                06 August 2022
                : 3
                : 100050
                Affiliations
                [1]Bioengineering and Robotics Research Center E. Piaggio and the Department of Information Engineering, School of Engineering, University of Pisa, Pisa, Italy
                Article
                S2665-945X(22)00023-7 100050
                10.1016/j.crneur.2022.100050
                9846460
                36685762
                5e3b9e97-7565-4613-94d4-9619b8f7baf1
                © 2022 The Author(s)

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 13 February 2022
                : 23 July 2022
                : 27 July 2022
                Categories
                Review Article

                physiological modeling,brain-heart interplay,heartbeat-evoked responses,heart rate variability,interoception,consciousness

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