Multilevel convergence of interoceptive impairments in hypertension: New evidence of disrupted body–brain interactions

Abstract

Interoception, the sensing of visceral body signals, involves an interplay between neural and autonomic mechanisms. Clinical studies into this domain have focused on patients with neurological and psychiatric disorders, showing that damage to relevant brain mechanisms can variously alter interoceptive functions. However, the association between peripheral cardiac-system alterations and neurocognitive markers of interoception remains poorly understood. To bridge this gap, we examined multidimensional neural markers of interoception in patients with early stage of hypertensive disease (HTD) and healthy controls. Strategically, we recruited only HTD patients without cognitive impairment (as shown by neuropsychological tests), brain atrophy (as assessed with voxel-based morphometry), or white matter abnormalities (as evidenced by diffusion tensor imaging analysis). Interoceptive domains were assessed through (a) a behavioral heartbeat detection task; (b) measures of the heart-evoked potential (HEP), an electrophysiological cortical signature of attention to cardiac signals; and (c) neuroimaging recordings (MRI and fMRI) to evaluate anatomical and functional connectivity properties of key interoceptive regions (namely, the insula and the anterior cingulate cortex). Relative to controls, patients exhibited poorer interoceptive performance and reduced HEP modulations, alongside an abnormal association between interoceptive performance and both the volume and functional connectivity of the above regions. Such results suggest that peripheral cardiac-system impairments can be associated with abnormal behavioral and neurocognitive signatures of interoception. More generally, our findings indicate that interoceptive processes entail bidirectional influences between the cardiovascular and the central nervous systems.

Altered neural signatures of interoception in multiple sclerosis

“…As expected, given these previous inconsistencies, we found no differences between groups in any of them (see Supporting Information Data S1 and Supporting Information Table S1). More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011). More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011).…”

“…Thus, following previous studies (Muller et al, 2015;Schulz et al, 2015), we focused our main analysis on HEP modulations, which provide critical information about the temporal dynamics of interoception. More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011). These properties highlight the relevance of the HEP as a reliable and self-sufficient nonbehavioral subclinical measure to afford critical insights of the cortical monitoring of internal signals.…”

“…done in previous reports, to avoid redundant comparisons and get a robust signal per condition(Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017). This permutation analysis is a robust approach to EEG data which has been applied in several studies assessing modulations of the HEPCouto, Adolfi, Velasquez, et al, 2015;Couto et al, 2014;Craig, 2002;Critchley & Harrison, 2013;Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004;Garcia-Cordero et al, 2016) and other ERPs(Amoruso et al, 2014;Chennu et al, 2013;Gonzalez-Gadea et al, 2015;Ibanez et al, 2013;Melloni et al, 2015;Melloni et al, 2016).This method gives a straightforward solution for the multiple comparison problems and does not depend on multiple comparison corrections or Gaussian distribution assumptions.…”

Early bilateral and massive compromise of the frontal lobes

“…Conversely, a set of sensorimotor (basic walking and sensory abilities) and cognitive (basic levels of consciousness, language, memory, social interaction) functions were partially spared. Among the affected frontal areas, the anterior insula is also involved in some of the preserved functions, such as a consciousness, social cognition, interoception, and emotion processing ( Adolfi et al, 2017 ; Baez et al, 2014 ; Couto et al, 2015 ; Couto et al, 2013 ; Garcia-Cordero et al, 2017 ; Ibanez et al, 2010 ; Ibanez et al, 2013 ; Melloni et al, 2014 ; Santamaria-Garcia et al, 2017 ; Vicario et al, 2017 ; Yoris et al, 2017 ). Though deficits in these domains were clearly present, they were much less pervasive than would be expected in the face of fronto-insular underdevelopment.…”

“…Preprocessing and resting-state network estimations were implemented with the DPARSF toolbox ( Chao-Gan and Yu-Feng, 2010 ), as in previous works of our group ( Abrevaya et al, 2017 ; Garcia-Cordero et al, 2016 ; Melloni et al, 2016 ; Sedeno et al, 2016 ; Sedeno et al, 2014 ; Sedeno et al, 2017 ; Yoris et al, 2017 ). The first functional images were discarded; the rest were slice-time corrected, realigned to the middle slice of the volume, band-pass filtered (0.01–0.08 Hz), and finally smoothed with an 8-mm full-width half-maximum kernel.…”