Interoception primes emotional processing: Multimodal evidence from neurodegeneration

Paula C. Salamone, Agustina Legaz, Lucas Sedeño, Sebastián Moguilner, Matías Fraile-Vazquez, Cecilia Gonzalez Campo, Sol Fittipaldi, Adrián Yoris, Magdalena Miranda, Agustina Birba, Agostina Galiani, Sofía Abrevaya, Alejandra Neely, Miguel Martorell Caro, Florencia Alifano, Roque Villagra, Florencia Anunziata, Maira Okada De Oliveira, Ricardo M. Pautassi, Andrea SlachevskyCecilia Serrano, Adolfo M. García, Agustín Ibañez

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

Abstract

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-interoception and post-exteroception 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-interoception 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-interoception negative FER was observed in HCs and AD, but not in bvFTD or PD patients. Across all groups, post-interoception negative FER correlated with the volume of the insula and the ACC. Also, negative FER was associated with functional connectivity along the (a) salience network in the post-interoception condition, and along the (b) executive network in the post-exteroception 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 nteroception, emotion, allostasis, and neurodegeneration.

Original languageEnglish
Pages (from-to)4276-4292
Number of pages17
JournalJournal of Neuroscience
Volume41
Issue number19
DOIs
StatePublished - 12 May 2021
Externally publishedYes

Keywords

  • Alzheimer's disease
  • Behavioral variant frontotemporal dementia
  • Emotion
  • Interoception
  • Parkinson's disease
  • Priming

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