Brain-heart interactions in the neurobiology of consciousness

American Journal of Physiology-Regulatory, Integrative and Comp

Norouzi

Ramsøy

et al. 2023

Self Cite

Dynamical information exchange between central and autonomic nervous systems, as referred to functional brain-heart interplay, occurs during emotional and physical arousal. It is well documented that physical and mental stress lead to sympathetic activation. Nevertheless, the role of autonomic inputs in nervous-system-wise communication under mental stress is yet unknown. In this study, we estimated the causal and bidirectional neural modulations between EEG oscillations and peripheral sympathetic and parasympathetic activities using a recently proposed computational framework for a functional brain-heart interplay assessment, namely the sympathovagal synthetic data generation model. Mental stress was elicited in 37 healthy volunteers by increasing their cognitive demands throughout three tasks associated with increased stress levels. Stress elicitation induced an increased variability in sympathovagal markers, as well as increased variability in the directional brain-heart interplay. The observed heart-to-brain interplay was primarily from sympathetic activity targeting a wide range of EEG oscillations, whereas variability in the efferent direction seemed mainly related to EEG oscillations in the gamma band. These findings extend current knowledge on stress physiology, which mainly referred to top-down neural dynamics. Our results suggest that mental stress may not cause an increase in sympathetic activity exclusively as it initiates a dynamic fluctuation within brain-body networks including bidirectional interactions at a brain-heart level. We conclude that directional brain-heart interplay measurements may provide suitable biomarkers for a quantitative stress assessment and bodily feedback may modulate the perceived stress caused by increased cognitive demand.

Section: Discussionsupporting

confidence: 81%

Dynamic fluctuations in ascending heart-to-brain communication under mental stress

American Journal of Physiology-Regulatory, Integrative and Comp

Norouzi

Ramsøy

et al. 2023

Self Cite

“…The study of mental stress elicited in other paradigms, such as mental arithmetic, could give a broader view of the physiological processes involved in brain– heart information exchange. Our study confirms the advantages of analyzing the interactions between brain and heart, instead of studying heart rate and brain dynamics exclusively (82, 83). The understanding of brain–heart dynamics and the neurophysiological substrates of stress has a clinical relevance.…”

Section: Discussionsupporting

confidence: 81%

Dynamic fluctuations in ascending heart–to–brain communication under mental stress

Norouzi

Ramsøy

et al. 2022

Preprint

Self Cite

Previous endeavors have revealed how the dynamical information exchange between central and autonomous nervous systems, as measured from brain-heart interplay, can explain emotional arousal and physical stress. In this study, we test our recently proposed computational framework for a functional brain-heart interplay assessment; the Sympatho-Vagal Synthetic Data Generation Model. The model estimates the causal and bidirectional neural modulations between EEG oscillations and sympathetic/parasympathetic activity. Here, mental stress is elicited by increasing the cognitive demand and quantified on 37 human volunteers. The increase on mental stress induced an increased variability on heart-to-brain functional interplay, primarily from sympathetic activity on EEG oscillations in the delta and beta bands. Existing theoretical and experimental evidence has shown that stress involves top-down neural dynamics in the brain. Therefore, our results show that mental stress involves dynamic and bidirectional neural interactions at a brain-body level as well, where bodily feedback shapes the perceived stress caused by an increased cognitive demand. We conclude that brain-heart interplay estimators are suitable biomarkers for stress measurements.

“…On the other hand, this disruption of brain-heart interplay was characterized by a lower heart-to-brain coupling strength and complexity in patients with severe HIBI, reflecting the impairment of bottom-up signaling and integration of peripheral signal. The integration of visceral signals seems to be a hallmark in conscious processing, as evidenced by a recently growing body of literature on perceptual awareness tasks in healthy subjects 14,46 . The potential role of visceral signals in consciousness was tested and confirmed in patients suffering from disorders of consciousness 15,16 .…”

Section: Discussionmentioning

confidence: 99%

Aberrant brain-heart coupling is associated with the severity and prognosis of hypoxic-ischemic brain injury after cardiac arrest

Hermann

Sharshar

et al. 2023

Preprint

Self Cite

Background and Objectives: Approximately 50% of post-cardiac arrest survivors remain comatose after 72h, a substantial proportion of which will have a poor neurological outcome, predominantly due to irreversible hypoxic-ischemic brain injury. Recent findings in healthy subjects and patients suggested that autonomic nervous system activity measured by brain-heart interactions could be reliable markers of consciousness and cognitive processing. Thus, we hypothesized that brain-heart interactions are associated with the severity of hypoxic-ischemic brain injury and the prognosis of these patients. Methods: In post-cardiac arrest patients still comatose 48h after sedation weaning, brain-heart interaction markers were computed on 5 minutes of continuous EEG/ECG recording using a synthetic data generation model, gathering bidirectional interactions between EEG frequency bands (delta, theta and alpha) and heart-rate variability frequency bands (low and high frequency). The strength and complexity of the interactions were quantified using medians and refined composite multiscale entropy. Primary outcome was the severity of brain injury, assessed by: (i) standardized qualitative EEG classification, (ii) somatosensory evoked potentials (N20), and (iii) neuron-specific enolase levels. Secondary outcome was the 3-month neurological status, assessed by the Cerebral Performance Category score [good (1-2) vs. poor outcome (3-4-5)]. Results: Between January 2007 and July 2021, 181 patients [116 males (64%), median age 61 years, age range 49-72 years] were admitted to ICU for a resuscitated cardiac arrest (76% out-of-hospital, 69% non-shockable rhythm). Poor neurological outcome was observed in 134 patients (74%). Qualitative EEG patterns suggesting high severity were associated with a decreased sympatho-vagal balance. Severity of EEG changes were proportional to higher absolute values of brain-to-heart coupling strength (p<2x10-3 for all brain-to-heart frequencies) and lower values of complexity (all p-values<0.05 except for alpha-to-low frequency). Brain-to-heart coupling strength was significantly higher in patients with bilateral absent N20 and correlated with neuron-specific enolase levels at day 3. This aberrant brain-to-heart coupling (increased strength, decreased complexity) was also associated with 3-month poor neurological outcome. Discussion : Our results suggest that autonomic dysfunctions may well represent hypoxic-ischemic brain injury post-cardiac arrest pathophysiology. These results open avenues for integrative monitoring of autonomic functioning in critical care patients with potential prognostic applications.