Multimodal Neurocognitive Markers of Naturalistic Discourse Typify Diverse Neurodegenerative Diseases

BIRBA, AGUSTINA; FITTIPALDI, SOL; CEDIEL ESCOBAR, JUDITH C.; GONZALEZ CAMPO, CECILIA; LEGAZ, AGUSTINA; GALIANI, AGOSTINA; DÍAZ RIVERA, MARIANO N.; MARTORELL CARO, MIQUEL; ALIFANO, FLORENCIA; PIÑA-ESCUDERO, STEFANIE D.; CARDONA, JUAN FELIPE; NEELY, ALEJANDRA; FORNO, GONZALO; CARPINELLA, MARIELA; SLACHEVSKY, ANDREA; SERRANO, CECILIA; SEDEÑO, LUCAS; IBÁÑEZ, AGUSTÍN; GARCÍA, ADOLFO M.

Cerebral cortex (New York, N.Y. : 1991)

NLM (Medline)

Año: 2022 vol. 32 p. 3377 - 3391

Neurodegeneration has multiscalar impacts, including behavioral, neuroanatomical, and neurofunctional disruptions. Can disease-differential alterations be captured across such dimensions using naturalistic stimuli? To address this question, we assessed comprehension of four naturalistic stories, highlighting action, nonaction, social, and nonsocial events, in Parkinson´s disease (PD) and behavioral variant frontotemporal dementia (bvFTD) relative to Alzheimer´s disease patients and healthy controls. Text-specific correlates were evaluated via voxel-based morphometry, spatial (fMRI), and temporal (hd-EEG) functional connectivity. PD patients presented action-text deficits related to the volume of action-observation regions, connectivity across motor-related and multimodal-semantic hubs, and frontal hd-EEG hypoconnectivity. BvFTD patients exhibited social-text deficits, associated with atrophy and spatial connectivity patterns along social-network hubs, alongside right frontotemporal hd-EEG hypoconnectivity. Alzheimer´s disease patients showed impairments in all stories, widespread atrophy and spatial connectivity patterns, and heightened occipitotemporal hd-EEG connectivity. Our framework revealed disease-specific signatures across behavioral, neuroanatomical, and neurofunctional dimensions, highlighting the sensitivity and specificity of a single naturalistic task. This investigation opens a translational agenda combining ecological approaches and multimodal cognitive neuroscience for the study of neurodegeneration.