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.

Keywords: embodied cognition; heart evoked potential; hypertension; interoception; neuroimaging.

Figure 1

Behavioral performance and HEP modulations in the HBD task. (a) Behavioral performance of patients and controls. (A1) The asterisk indicates significant differences (p < .05). Individual performance is represented inside and outside of the box as dark points. The middle box line indicates the group's mean values. The precision score can vary between 0 and 1, with higher scores indicating better performance. (A2) Individual performance comparison between conditions (per group). (b) HEP analysis. All differences reported were calculated via Monte Carlo permutations analysis (5000 permutations, p < .05) point by point (Manly, 2007). A minimum extension of five consecutive points was selected as criteria to graph clusters. Shadowed lines indicate SEM. Green bars indicate significant differences. HTD: hypertensive disease; EC: exteroceptive condition; IC: interoceptive condition [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

HEP amplitude in three regions of interest (ROIs): central frontal ROI, left frontal ROI, and right frontal ROI. All differences reported were calculated via Monte Carlo permutations analysis (5000 permutations, p < .05) by point (Manly, 2007). Shadowed lines indicate SEM. Green bars indicate significant differences. Yellow dots in the channel location diagrams illustrate the electrodes included in each ROI [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Association between interoceptive and MRI measures. (a) Linear regression between gray matter volume and performance during the IC in favor of the control group. Brain images are presented according to neurological convention. (b) Seed analysis associated to interoceptive performance in controls. The light blue node represents the left insular seed. Pink nodes and edges represent the connections with the seed that were significantly associated with IC (Spearman's correlations) in controls. L: left; R: right; P: posterior; A: anterior; Ins: insula; ACC: anterior cingulated cortex; SOM: somatosensory cortex. (c) Scatter plots of the significant associations from panel B for both controls and HTD patients