Allostatic-Interoceptive Overload in Frontotemporal Dementia

BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly comprom...

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Bibliographic Details
Authors: Birba, Agustina; Santamaría García, Hernando; Prado, Pavel; Cruzat, Josefina; Sainz Ballesteros, Agustín; Legaz, Agustina; Fittipaldi, Sol; Duran Aniotz, Claudia; Slachevsky, Andrea; Santibañez, Rodrigo; Sigman, Mariano; García, Adolfo Martín; Whelan, Robert; Moguilner, Sebastian Gabriel; Ibañez, Agustin Mariano
Format: Article
Status:Published version
Publication date:2022
Country:Argentina
Institution:Consejo Nacional de Investigaciones Científicas y Técnicas
Repository:CONICET Digital (CONICET)
Language:English
OAI Identifier:oai:ri.conicet.gov.ar:11336/234392
Online Access:http://hdl.handle.net/11336/234392
Access Level:Open access
Keyword:ALLOSTASIS
ALLOSTATIC-INTEROCEPTIVE NETWORK
FRONTOTEMPORAL DEMENTIA
HEP
INTEROCEPTION
MULTIMODAL IMAGING
PREDICTIVE CODING
rsHEP
https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
Description
Summary:BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload. METHODS: We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks). RESULTS: Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group. CONCLUSIONS: Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.