Brain dynamics alterations induced by partial sleep deprivation: An energy landscape study.

Neuroimage

Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Health and Rehabilitation Science, School of Life Science and Technology, Xi'an Jiaotong University, Key Laboratory of Neuro-informatics & Rehabilitation Engineering of Ministry of Civil Affairs, Xi'an, Shaanxi, 710049, China; Research Center for Brain-inspired Intelligence, Xi'an Jiaotong University, Xi'an, Shaanxi, 710049, China. Electronic address:

Published: March 2025

Partial sleep deprivation (PSD) alters neural activity of intrinsic brain networks involved in cognitive functions. However, the age-related time-varying properties of large-scale brain functional networks after PSD remain unknown. Our study applied energy landscape analysis to resting-state functional magnetic resonance imaging data to characterize the dominant brain activity patterns in 36 healthy young (19 females, 23.53 ± 2.36 years) and 33 healthy older (18 females, 68.81 ± 2.41 years) adults after full sleep (FS) and PSD. Dynamic properties of these patterns, including appearance probability, duration and transitions, were then calculated. Finally, a 10 steps numerical simulation was performed on each energy landscape. We found that the energy landscapes of the younger and older groups had similar hierarchical structures, including two major states and two minor states. The two major states showed complementary spontaneous activation patterns. But the PSD has altered the temporal evolution of these major brain states in younger participants, manifested by significantly higher appearance frequency of the major states and the direct transitions between major states than FS. These changes were not significant in older participants. Additionally, the weaker functional segregation between two modules assigned by two complementary major states was found during PSD than FS in young group. We further demonstrated that such abnormal brain network functional coordination was associated with the atypical brain dynamics and behaviors. These findings suggested a low-dimensional and restricted dynamic landscape of brain activity in young adults after PSD and provided new insight into understand the neural effects of PSD.

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http://dx.doi.org/10.1016/j.neuroimage.2025.121108DOI Listing

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