TY - JOUR
T1 - Interoception primes emotional processing
T2 - Multimodal evidence from neurodegeneration
AU - Salamone, Paula C.
AU - Legaz, Agustina
AU - Sedeño, Lucas
AU - Moguilner, Sebastián
AU - Fraile-Vazquez, Matías
AU - Campo, Cecilia Gonzalez
AU - Fittipaldi, Sol
AU - Yoris, Adrián
AU - Miranda, Magdalena
AU - Birba, Agustina
AU - Galiani, Agostina
AU - Abrevaya, Sofía
AU - Neely, Alejandra
AU - Caro, Miguel Martorell
AU - Alifano, Florencia
AU - Villagra, Roque
AU - Anunziata, Florencia
AU - De Oliveira, Maira Okada
AU - Pautassi, Ricardo M.
AU - Slachevsky, Andrea
AU - Serrano, Cecilia
AU - García, Adolfo M.
AU - Ibañez, Agustín
N1 - Publisher Copyright:
Copyright © 2021 Salamone, Legaz et al.
PY - 2021/5/12
Y1 - 2021/5/12
N2 - 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.
AB - 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.
KW - Alzheimer's disease
KW - Behavioral variant frontotemporal dementia
KW - Emotion
KW - Interoception
KW - Parkinson's disease
KW - Priming
UR - http://www.scopus.com/inward/record.url?scp=85104416573&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.2578-20.2021
DO - 10.1523/JNEUROSCI.2578-20.2021
M3 - Article
C2 - 33827935
AN - SCOPUS:85104416573
SN - 0270-6474
VL - 41
SP - 4276
EP - 4292
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 19
ER -