Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal

Candia-Rivera, Diego; Catrambone, Vincenzo; Thayer, Julian F.; Gentili, Claudio; Valenza, Gaetano

doi:10.1073/pnas.2119599119

Cited by 87 publications

(118 citation statements)

References 89 publications

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“…For instance, the descending interplay to the heart is usually associated to arousal only [6]. However, the analysis of the bidirectional interactions of the brain with peripheral cardiac activity showed that the reported arousal was correlated with ascending modulations from cardiac vagal activity [141]. The hypothesis introduced here is that the physiological and cognitive processes involved in interoception, and subjectivity, would involve a dynamic and cyclic information exchange.…”

Section: Uncovering Brain-heart Interactions Through Physiological Mo...mentioning

confidence: 83%

“…Importantly, the changes in sympathetic activity precede the brain network organization, suggesting causal interactions [138]. Sympathovagal modulations towards brain oscillations shape emotional and physical arousal [140,141]. The locus coeruleus in the brainstem, which regulates arousal and autonomic function, also shapes neuronal excitability across the brain [142][143][144], suggesting further links between autonomic activity and the orchestrating of neuronal dynamics during conscious processing.…”

Section: Consciousness and Complexity In The Brain-heart Communicatio...mentioning

confidence: 99%

“…One could hypothesize that changes in the heart rate are related to a posteriori process, therefore to the content of consciousness, and that conscious processing modulates the changes in HRV. However, consciousness may be necessary to feel emotions [10,11], and emotional processing is initiated by changes in cardiac vagal activity in emotion elicitation, as shown through mathematical modeling [141]. Upcoming research in the field needs to discern whether brain-heart interactions have a causal role to subjective experiences; or whether brain-heart interactions correspond to a consequence of the brain processing for the contents of consciousness.…”

Section: Consciousness and Complexity In The Brain-heart Communicatio...mentioning

confidence: 99%

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Brain-heart interactions in the neurobiology of consciousness

Candia-Rivera¹

2022

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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 the heart 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 communications 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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Section: Uncovering Brain-heart Interactions Through Physiological Mo...mentioning

confidence: 83%

Section: Consciousness and Complexity In The Brain-heart Communicatio...mentioning

confidence: 99%

Section: Consciousness and Complexity In The Brain-heart Communicatio...mentioning

confidence: 99%

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Brain-heart interactions in the neurobiology of consciousness

Candia-Rivera¹

2022

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“…For instance, it has been shown that the respiratory rate shapes olfactory memory 70,71 , emotions 72 , and reaction time 73 , and coordinates the coupling of brain oscillations during sleep 74–76 as well as during wakefulness 77–82 . These results indicate that cardiorespiratory activity contribute to the shaping of attention and perception, and relative changes in respiration and heart rates are part of ongoing bidirectional brain-heart interplay processes 83 , similar to emotions or stress 84,85 .…”

Section: Discussionmentioning

confidence: 83%

Confounding effects of heart rate, breathing rate, and frontal fNIRS on interoception

Candia-Rivera

Sappia

Horschig³

et al. 2022

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Recent studies have established that cardiac and respiratory phases can modulate perception and related neural dynamics. While heart rate and respiratory sinus arrhythmia are possibly affecting interoception biomarkers, such as heartbeat-evoked potentials, the relative changes in heart rate and cardiorespiratory dynamics in interoceptive processes have not yet been investigated. In this study, we investigated the variation in heart and respiration rates, as well as higher functional dynamics including cardiorespiratory correlation and frontal hemodynamics, during cardiac awareness tasks. To further investigate the functional physiology linked to changes in vagal activity caused by specific respiratory rates, we studied cardiac awareness and controlled respiration rate. The results demonstrate that focusing on heartbeats decreases respiration and heart rates in comparison, which may be part of the physiological mechanisms related to 'listening' to the heart, the focus of attention, and self-awareness. Focusing on heartbeats was also observed to increase frontal connectivity, supporting the role of frontal structures in the neural monitoring of visceral inputs. However, cardiorespiratory correlation is affected by both interoceptive and controlled respiration. Based on these results, we concluded that variations in heart and respiratory rates are confounding factors in the assessment of interoceptive abilities and relative fluctuations in respiration and heart rates should be considered to be a mode of covariate measurement of interoceptive processes.

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“…It has been shown that indeed there is an information exchange between the brain and the visceral signals when studying the brain-heart axis as a proxy for sympathovagal-cortical interactions during stress [23]. Though, the stress and emotion arousal effects may diverge in the neurophysiology [21, 24, 25], having a comprehensive regional autonomic system activity response measure with the brain interactions provides an axis that can aid in studying the brain-body interactions during psychological emotional disorders using an all-in-one method.…”

Section: Introductionmentioning

confidence: 99%

Nonlinear Neural Patterns Are Revealed In High Frequency fNIRS Analysis

Ghouse

Candia-Rivera

Valenza

2022

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Vasomotor tone has a direct implication in oxygen transport to neural tissue, and its dynamics are known to be under constant control from feedback loops with visceral signals, such as sympathovagal interactions. Functional Near Infrared Spectroscopy (fNIRS) offers a nuanced measure of hemoglobin concentration that also comprises high frequencies, though most fNIRS literature studies traditional frequency ranges of hemodynamics (< 0.2 Hz). Linear theory of the hemodynamic response function supports this low frequency band, but we hypothesize that nonlinear effects elicited from the complex system sustaining vasomotor tone presents itself in higher frequencies. To characterize these effects, we investigate how plausible modulation of autoregulatory effects impact aforementioned high frequency components of fNIRS through simulations of mechanistic hemodynamic models. Then, we compare representational similarities between fast (0.2 Hz to 0.6 Hz) and slow (< 0.2 Hz) wave fNIRS to demonstrate that representations acquired through nonlinear analysis are distinct between the frequency bands, whereas when using linear time-domain analysis they are not. Furthermore, by comparing topoplots of significant detectors using nonlinear random vector correlation methods (distance correlation), we demonstrate through a 2nd level group analysis that the median concentrations acquired by fNIRS are independent when analyzing the nonlinearity of their dynamics in their fast and slow component, while they are dependent when utilizing linear time-domain analysis. This study not only provides motivation for researchers to also include higher frequency components in their analysis, but also provides motivation to explore nonlinear effects, e.g. topological entropy. The results of this study motivate future research to explore the nonlinear autoregulatory impacts of regional blood flow and hemoglobin concentrations.

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Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal

Cited by 87 publications

References 89 publications

Brain-heart interactions in the neurobiology of consciousness

Brain-heart interactions in the neurobiology of consciousness

Confounding effects of heart rate, breathing rate, and frontal fNIRS on interoception

Nonlinear Neural Patterns Are Revealed In High Frequency fNIRS Analysis

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