Interoception primes emotional processing: Multimodal evidence from neurodegeneration

SALAMONE, PAULA C.; LEGAZ, AGUSTINA; SEDEÑO, LUCAS; MOGUILNER, SEBASTIÁN; FRAILE-VAZQUEZ, MATÍAS; CAMPO, CECILIA GONZALEZ; FITTIPALDI, SOL; YORIS, ADRIÁN; MIRANDA, MAGDALENA; BIRBA, AGUSTINA; GALIANI, AGOSTINA; ABREVAYA, SOFÍA; NEELY, ALEJANDRA; CARO, MIGUEL MARTORELL; ALIFANO, FLORENCIA; VILLAGRA, ROQUE; ANUNZIATA, FLORENCIA; OLIVEIRA, MAIRA OKADA DE; PAUTASSI, RICARDO M.; SLACHEVSKY, ANDREA; SERRANO, CECILIA; GARCÍA, ADOLFO M.; IBAÑEZ, AGUSTÍN

JOURNAL OF NEUROSCIENCE

SOC NEUROSCIENCE

Lugar: Washington; Año: 2021 vol. 41 p. 4276 - 4292

0270-6474

Recent frameworks in cognitive neuroscience and behavioral neurology underscore interoceptive priors as core modulators of negative emotions. However, the field lacks experimental designs manipulating the priming of emotions via interoception and exploring their multimodal signatures in neurodegenerative models. Here, we designed a novel task that involves interoceptive and control-exteroceptive priming conditions followed by post-Intero and post-Extero facial emotion recognition (FER). We recruited 114 participants, including healthy controls (HCs) as well as patients with behavioral variant frontotemporal dementia (bvFTD), Parkinson?s disease (PD), and Alzheimer?s disease (AD). We measured online EEG modulations of the heart-evoked potential (HEP), and associations with both brain structural and resting-state functional connectivity patterns. Behaviorally, post-Intero negative FER was enhanced in HCs but selectively disrupted in bvFTD and PD, with AD presenting generalized disruptions across emotion types. Only BvFTD presented impaired interoceptive accuracy. Increased HEP modulations during post-Intero negative FER was observed in HCs and AD, but not in bvFTD or PD patients. Across all groups, post-Intero negative FER correlated with the volume of the insula and the anterior cingulate cortex. Also, negative FER was associated with functional connectivity along the (a) salience network in the post-Intero condition, and along the (b) executive network in the post-Extero condition. These patterns were selectively disrupted in bvFTD (a) and PD (b), respectively. Our approach underscores the multidimensional impact of interoception on emotion, while revealing a specific pathophysiological marker of bvFTD. These findings inform a promising theoretical and clinical agenda in the fields of interoception, emotion, allostasis, and neurodegeneration.