Heart–brain interactions during social and cognitive stress in hypertensive disease: A multidimensional approach

Abstract

Hypertensive disease (HTD), a prominent risk factor for cardiovascular and cerebrovascular diseases, is characterized by elevated stress-proneness. Since stress levels are underpinned by both cardiac and neural factors, multidimensional insights are required to robustly understand their disruption in HTD. Yet, despite their crucial relevance, heart rate variability (HRV) and multimodal neurocognitive markers of stress in HTD remain controversial and unexplored, respectively. To bridge this gap, we studied cardiodynamic as well as electrophysiological and neuroanatomical measures of stress in HTD patients and healthy controls. Both groups performed the Trier Social Stress Test (TSST), a validated stress-inducing task comprising a baseline and a mental stress period. During both stages, we assessed a sensitive HRV parameter (the low frequency/high frequency [LF/HF ratio]) and an online neurophysiological measure (the heartbeatevoked potential [HEP]). Also, we obtained neuroanatomical data via voxel-based morphometry (VBM) for correlation with online markers. Relative to controls, HTD patients exhibited increased LF/HF ratio and greater HEP modulations during baseline, reduced changes between baseline and stress periods, and lack of significant stress-related HRV modulations associated with the grey matter volume of putative frontrostriatal regions. Briefly, HTD patients presented signs of stressrelated autonomic imbalance, reflected in a potential basal stress overload and a lack of responsiveness to acute psychosocial stress, accompanied by neurophysiological and neuroanatomical alterations. These multimodal insights underscore the relevance of neurocognitive data for developing innovations in the characterization, prognosis, and treatment of Accepted ArticleThis article is protected by copyright. All rights reserved HTD and other conditions with autonomic imbalance. More generally, these findings may offer new insights into heart-brain interactions.

Interoception Primes Emotional Processing: Multimodal Evidence from Neurodegeneration

“…Eye movements or blink artifacts were corrected with independent component analysis ( D. Kim and Kim, 2012 ) and with a visual inspection protocol ( Schandry and Montoya, 1996 ; Dirlich et al, 1997 ; Pollatos and Schandry, 2004 ; Terhaar et al, 2012 ; García-Cordero et al, 2016 , 2017 ; Yoris et al, 2017 , 2018 ; Salamone et al, 2018 ). R-wave values from the ECG signal were identified with a peakfinder function on MATLAB and used to segment continuous hd-EEG data for HEP analysis ( Canales-Johnson et al, 2015 ; García-Cordero et al, 2016 , 2017 ; Yoris et al, 2017 ; Salamone et al, 2018 , 2020 ; Abrevaya et al, 2020 ; Legaz et al, 2020 ; Richter and Ibáñez, 2021 ). To examine the HEP occurring during the facial emotion stimuli presentation, we first segmented continuous EEG into epochs from −200 to 800 ms relative to the onset of facial stimuli (= 0).…”

“…Comparisons of HEP modulations were performed using a 5000 point-by-point Monte Carlo permutation test with bootstrapping ( Manly, 2006 ). This analysis constitutes a robust approach for HEP analyses ( Couto et al, 2014 , 2015 ; Canales-Johnson et al, 2015 ; García-Cordero et al, 2016 , 2017 ; Yoris et al, 2017 , 2018 ; Salamone et al, 2018 , 2020 ; Abrevaya et al, 2020 ; Legaz et al, 2020 ; Richter and Ibáñez, 2021 ), providing a solution for the multiple comparison problems and circumventing Gaussian distribution assumptions ( Nichols and Holmes, 2002 ). To avoid cardiac field artifacts ( Kern et al, 2013 ), we only analyzed time points between 200 and 500 ms, as these time points are proposed to be less affected by cardiac field artifacts ( Dirlich et al, 1997 ; Kern et al, 2013 ; Park et al, 2014 ), and they capture a typical HEP latency ( Pollatos and Schandry, 2004 ; Canales-Johnson et al, 2015 ; Müller et al, 2015 ; Pollatos et al, 2016 ).…”

Allostatic-Interoceptive Overload in Frontotemporal Dementia

“…Moreover, theoretical accounts (24) and metanalytic evidence (39) suggest that cognitive processes usually impaired in bvFTD (social cognition, emotion recognition, and interoception) are interlinked. Patients with bvFTD have poorer responses to external demands (disinhibition, disruptive or inappropriate behaviors; for a review: (40)) and exacerbated reactions in social settings (i.e., increased experience of envy and Schadenfreude (41); violation of social norms (42)). These socio-cognitive inappropriate responses in bvFTD have been theoreticallybut not empirically)linked to allostatic-interoceptive overload (24,(43)(44)(45)(46).…”

A predictive coding framework of allostatic–interoceptive overload in frontotemporal dementia

“…In addition to traditional active heartbeat detection tasks, where participants must press a key each time they feel a heartbeat [27][28][29][30][31][32][33][34][35], novel evidence has shown that HEP changes (commonly measured with the amplitude difference, but also with latency and power [36,37]) during noncardiac monitoring tasks, as well as resting-state, increased amplitude. Such changes have been associated with a hypervigilance to interoceptive signals and linked to stress-related allostatic overload in both hypertensive patients and healthy controls [38]. Similarly, external demanding somatosensorial stimuli (i.e., electrical pulse) triggers increased HEP modulation [26].…”