{"title":"Beyond language: empathy and emotion recognition deficits in primary progressive aphasias","authors":"Giulia Giacomucci , Alice Pieri , Valentina Moschini , Chiara Crucitti , Sonia Padiglioni , Carmen Morinelli , Giulia Galdo , Filippo Emiliani , Matilde Nerattini , Silvia Bagnoli , Assunta Ingannato , Sandro Sorbi , Benedetta Nacmias , Valentina Berti , Valentina Bessi","doi":"10.1016/j.nicl.2025.103852","DOIUrl":null,"url":null,"abstract":"<div><div>Although primary progressive aphasia (PPA) is considered a language disorder, increasing evidence points to the presence of social cognition impairments in PPA variants. The aims of this study were to explore empathy and emotion recognition deficits in the three PPA variants (sv-PPA, lv-PPA, nfv-PPA) and to identify their neural correlates.</div><div>Eleven sv-PPA, 34 lv-PPA,11 nfv-PPA patients and 34 healthy controls (HC) were included in this study. Empathy was explored with the Interpersonal Reactivity Index (IRI) (Perspective Taking – PT, Fantasy – FT, Empathic Concern – EC, Personal Distress – PD), rated by caregivers before (T0) and after (T1) the onset of cognitive symptoms. Emotion recognition was evaluated with the Ekman 60Faces (EK-60F) Test and metabolic activity with [18F]FDG-PET.</div><div>In all PPA variants, PT score was reduced from T0 to T1 (sv-PPA <em>p</em> = 0.014, lv-PPA <em>p</em> < 0.001, nfv-PPA <em>p</em> = 0.022) and PD score was increased (sv-PPA <em>p</em> = 0.033, lv-PPA <em>p</em> < 0.001, nfv-PPA <em>p</em> = 0.009). Only lv-PPA showed a decrease of FT score (<em>p</em> = 0.024), while EC was spared in all three variants. Sv-PPA patients had the worst performances in the EK-60F Test, followed by lv-PPA and, lastly, by nfv-PPA.</div><div>Correlations between EK-60F scores and metabolic activity were found in sv-PPA and lv-PPA, highlighting the involvement of areas participating in the emotion recognition network: cingulate cortex, insula, temporal and orbitofrontal cortices and inferior frontal gyrus.</div><div>All PPA variants exhibited impairments in cognitive empathy (PT) and heightened emotional contagion (PD). The most severe deficits in emotion recognition were shown by sv-PPA, while nfv-PPA was the less impaired variant.</div></div>","PeriodicalId":54359,"journal":{"name":"Neuroimage-Clinical","volume":"48 ","pages":"Article 103852"},"PeriodicalIF":3.6000,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuroimage-Clinical","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2213158225001226","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
Although primary progressive aphasia (PPA) is considered a language disorder, increasing evidence points to the presence of social cognition impairments in PPA variants. The aims of this study were to explore empathy and emotion recognition deficits in the three PPA variants (sv-PPA, lv-PPA, nfv-PPA) and to identify their neural correlates.
Eleven sv-PPA, 34 lv-PPA,11 nfv-PPA patients and 34 healthy controls (HC) were included in this study. Empathy was explored with the Interpersonal Reactivity Index (IRI) (Perspective Taking – PT, Fantasy – FT, Empathic Concern – EC, Personal Distress – PD), rated by caregivers before (T0) and after (T1) the onset of cognitive symptoms. Emotion recognition was evaluated with the Ekman 60Faces (EK-60F) Test and metabolic activity with [18F]FDG-PET.
In all PPA variants, PT score was reduced from T0 to T1 (sv-PPA p = 0.014, lv-PPA p < 0.001, nfv-PPA p = 0.022) and PD score was increased (sv-PPA p = 0.033, lv-PPA p < 0.001, nfv-PPA p = 0.009). Only lv-PPA showed a decrease of FT score (p = 0.024), while EC was spared in all three variants. Sv-PPA patients had the worst performances in the EK-60F Test, followed by lv-PPA and, lastly, by nfv-PPA.
Correlations between EK-60F scores and metabolic activity were found in sv-PPA and lv-PPA, highlighting the involvement of areas participating in the emotion recognition network: cingulate cortex, insula, temporal and orbitofrontal cortices and inferior frontal gyrus.
All PPA variants exhibited impairments in cognitive empathy (PT) and heightened emotional contagion (PD). The most severe deficits in emotion recognition were shown by sv-PPA, while nfv-PPA was the less impaired variant.
期刊介绍:
NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging.
The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.