Interoception Primes Emotional Processing: Multimodal Evidence from Neurodegeneration.

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.SIGNIFICANCE STATEMENT We examined whether and how emotions are primed by interoceptive states combining multimodal measures in healthy controls and neurodegenerative models. In controls, negative emotion recognition and ongoing HEP modulations were increased after interoception. These patterns were selectively disrupted in patients with atrophy across key interoceptive-emotional regions (e.g., the insula and the cingulate in frontotemporal dementia, frontostriatal networks in Parkinson's disease), whereas persons with Alzheimer's disease presented generalized emotional processing abnormalities with preserved interoceptive mechanisms. The integration of both domains was associated with the volume and connectivity (salience network) of canonical interoceptive-emotional hubs, critically involving the insula and the anterior cingulate. Our study reveals multimodal markers of interoceptive-emotional priming, laying the groundwork for new agendas in cognitive neuroscience and behavioral neurology.

The Neural Blending of Words and Movement: Event-Related Potential Signatures of Semantic and Action Processes during Motor-Language Coupling.

Behavioral embodied research shows that words evoking limb-specific meanings can affect responses performed with the corresponding body part. However, no study has explored this phenomenon's neural dynamics under implicit processing conditions, let alone by disentangling its conceptual and motoric stages. Here, we examined whether the blending of hand actions and manual action verbs, relative to nonmanual action verbs and nonaction verbs, modulates electrophysiological markers of semantic integration (N400) and motor-related cortical potentials during a lexical decision task. Relative to both other categories, manual action verbs involved reduced posterior N400 amplitude and greater modulations of frontal motor-related cortical potentials. Such effects overlapped in a window of ∼380-440 msec after word presentation and ∼180 msec before response execution, revealing the possible time span in which both semantic and action-related stages reach maximal convergence. These results allow refining current models of motor-language coupling while affording new insights on embodied dynamics at large.

Time to Face Language: Embodied Mechanisms Underpin the Inception of Face-Related Meanings in the Human Brain.

In construing meaning, the brain recruits multimodal (conceptual) systems and embodied (modality-specific) mechanisms. Yet, no consensus exists on how crucial the latter are for the inception of semantic distinctions. To address this issue, we combined electroencephalographic (EEG) and intracranial EEG (iEEG) to examine when nouns denoting facial body parts (FBPs) and nonFBPs are discriminated in face-processing and multimodal networks. First, FBP words increased N170 amplitude (a hallmark of early facial processing). Second, they triggered fast (~100 ms) activity boosts within the face-processing network, alongside later (~275 ms) effects in multimodal circuits. Third, iEEG recordings from face-processing hubs allowed decoding ~80% of items before 200 ms, while classification based on multimodal-network activity only surpassed ~70% after 250 ms. Finally, EEG and iEEG connectivity between both networks proved greater in early (0-200 ms) than later (200-400 ms) windows. Collectively, our findings indicate that, at least for some lexico-semantic categories, meaning is construed through fast reenactments of modality-specific experience.

Implicit emotional awareness in frontotemporal dementia.

The preserved "implicit awareness" in patients with Alzheimer disease (AD) presenting anosognosia has opened a new branch of research regarding explicit-implicit integration. The behavioral variant of frontotemporal dementia (bvFTD), contrary to AD, would present impaired anosognosia-related implicit awareness due to a dysfunctional implicit integration of contextual information caused by an abnormal fronto-insular-temporal network. Loss of insight and anosognosia are pervasive in bvFTD, but no reports have assessed the implicit emotional awareness in this condition. We emphasize the need to investigate and extend our knowledge of implicit contextual integration impairments and their relation with anosognosia in bvFTD vs AD.