Hippocampal atrophy and altered functional connectivity are prominent features of mild cognitive impairment (MCI), yet their relationships and joint contribution to cognitive impairment remain unclear. We evaluated multidomain cognitive-sensorimotor performance, whole-brain gray matter atrophy patterns, associated functional connectivity, and their coupling in MCI and HC. We conducted this cross-sectional study in 25 clinically diagnosed amnestic and non-amnestic MCI patients and 15 age- and education-matched healthy controls (HC). Participants (57-81 years old) completed a battery assessing general cognition, executive functions, attention, speech-in-noise perception, manual dexterity, and balance, combined with structural and resting-state functional magnetic resonance imaging. Among the 25 MCI patients, 8 (32%) presented with amnestic MCI, 15 (60%) with non-amnestic MCI, and 2 (8%) with subjective cognitive decline. Linear mixed models revealed that semantic fluency (g = 0.74) was the largest discriminator of MCI, followed by attention (g = 0.61), phonemic fluency (g = 0.59), and speech-in-noise perception (g = 0.56). Voxel-based morphometry showed bilateral hippocampal and anteromedial cerebellar gray matter atrophy in MCI. Seed-based functional connectivity analyses indicated that atrophy was not uniformly associated with reduced connectivity. Cortico-subcortical hypoconnectivity emerged only in networks associated with left hippocampal atrophy in MCI compared with HC. Network-based analyses showed disrupted brain-behavior coupling and a stronger detrimental influence of age in MCI than in HC. These findings confirm the critical role of hippocampal structure-function relationships in multidomain MCI symptoms. A decoupled brain-cognition aging profile suggests that multimodal indices integrating hippocampal structure, connectivity, and behavioral performance may strengthen MCI diagnosis.
Marie, D., Kokkinou, D., Junker-Tschopp, C., Kliegel, M., Allali, G., Brioschi Guevara, A., Frisoni, G. B., James, C. E.
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