Mapping the cortical architecture of sleep deprivation: insights from fMRI, neurotransmission, and metabolic activity.

BACKGROUND

Sleep deprivation (SD) produces profound cognitive deficits, yet its integrative effects on large-scale cortical organization, metabolic alterations, and cognitive function remain unclear.

METHODS

Based on meta-analytic seeds, lesion network mapping was applied to connectome data from 1000 healthy individuals to generate an SD-related cortical weight map (SD-CWM). Thirty participants then completed a 24-hour acute SD protocol, during which resting-state and memory-task-evoked brain activities, untargeted metabolomics, and memory performance were measured under both rested wakefulness (RW) and SD.

RESULTS

(1) After SD, alterations in both resting-state and task-evoked activities within the SD-CWM were associated with memory performance decline, with resting-state changes showing stronger associations. (2) The SD-CWM was predominantly localized to the occipital cortex and encompassed the visual and ventral attention networks, showing spatial correspondence with nine neurotransmitter receptors that also tracked individual differences in resting-state changes. (3) Granger causality analysis indicated cortex-subcortex directional influences between the SD-CWM and subcortical nuclei under RW, whereas SD exhibited a shift toward subcortex-cortex patterns, centered on the caudal temporal thalamus. (4) Four metabolites were associated with resting-state changes within the SD-CWM, with cortical activity alterations showing stronger associations with metabolic variation than subcortical activity.

CONCLUSIONS

This study identifies an SD-related cortical map and characterizes its functional, directional, and metabolic associations, offering a systems-level perspective on the neural vulnerability underlying cognitive impairment after sleep loss.