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

Abstract

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.

Intracortical brain‐heart interplay: An EEG model source study of sympathovagal changes

“…These physiological dynamics have been captured through physiological modeling of the BHI, in which the ascending BHI information flow (i.e., heart‐to‐brain) is the first response to the CPT stimulus, which is followed by the descending flow (Candia‐Rivera, Catrambone, Barbieri, & Valenza, 2022). Interestingly, these results are consistent with those reported in high‐arousal conditions, such as emotional elicitation (Candia‐Rivera et al, 2023; Candia‐Rivera, Catrambone, Thayer, et al, 2022), suggesting a leading role for BHI in the physiology of arousal. The current study, even without investigating the timing and direction of the interaction, supports the literature on the brain frequency bands involved in the BHI (Candia‐Rivera, Catrambone, Barbieri, & Valenza, 2022; Catrambone et al, 2019), mainly $$$ \delta $$$ and $$$ \gamma $$$, and bridges fMRI and electrophysiological studies pointing at the CAN as the main player in CNS and ANS interaction (Benarroch, 2012; Valenza et al, 2019).…”

“…In this framework, heartbeat and breathing dynamics might induce the pressure pulsatility to which the mechano‐sensitive pyramidal neurons responds in a frequency range belonging to the $$$ \delta $$$ band (Hamill, 2023; Klimesch, 2023). Moreover, the absence of correlation with the higher frequency bands of the HRV series may be attributed to the specificity of CPT stimuli, which act as physical stressors and may elicit specific changes other than other cognitive stressors (Candia‐Rivera et al, 2023; Young & Benton, 2015).…”

Autonomic modulations to cardiac dynamics in response to affective touch: Differences between social touch and self-touch

“…Further supporting this idea, the insula — a brain region involved in interoceptive processing—plays a role in distinguishing between observing others’ somatosensory experiences and one’s own somatosensory experiences [59], and its damage disrupts affective touch perception [60]. Finally, the reported relationship of brain-heart interactions with self-other distinctions [61]–[64] and emotion processing [47], [64]–[68] further supports the role of autonomic dynamics in the processing of affective stimuli.…”

Impaired functional brain-heart interplay sustains emotion dysregulation in depressed individuals

“…Recent findings highlight that BHI dynamics are highly directional Candia-Rivera et al (2022 ); Catrambone and Valenza (2021 ); Pereira et al (2013 ); Catrambone et al (2021a ); Malandrone et al (2024 ). In healthy individuals, on the one hand, directional BHI is modulated by stress Catrambone et al (2024 ); Candia-Rivera et al (2023 ), as well as emotional processing Candia-Rivera et al (2022 ), with the ascending heart-to-brain changes occurring first in time. On the other hand, directed brain-to-heart dynamics have a specific response timing with a s period in response to sympathovagal elicitation Catrambone et al (2021c ).…”