Distinct Convergent Brain Alterations in Sleep Disorders and Sleep Deprivation

Abstract

ImportanceSleep disorders have different etiologies yet share some nocturnal and daytime symptoms, suggesting common neurobiological substrates; healthy individuals undergoing experimental sleep deprivation also report analogous daytime symptoms. However, brain similarities and differences between long-term sleep disorders and short-term sleep deprivation are unclear.ObjectiveTo investigate the shared and specific neural correlates across sleep disorders and sleep deprivation.Data SourcesPubMed, Web of Science, Embase, Scopus, and BrainMap were searched up to January 2024 to identify relevant structural and functional neuroimaging articles.Study SelectionWhole-brain neuroimaging articles reporting voxel-based group differences between patients with different sleep disorders and healthy control participants or between total or partial sleep-deprived and well-rested individuals were included.Data Extraction and SynthesisSignificant coordinates of group comparisons, their contrast direction (eg, patients < controls), and imaging modality were extracted. For each article, 2 raters independently evaluated eligibility and extracted data. Subsequently, several meta-analyses were performed with the revised activation likelihood estimation algorithm using P < .05 cluster-level familywise error correction.Main Outcomes and MeasuresTransdiagnostic regional brain alterations were identified across sleep disorders and among articles reporting sleep deprivation. Their associated behavioral functions and task-based or task-free connectivity patterns were explored using 2 independent datasets (BrainMap and the enhanced Nathan Kline Institute–Rockland Sample).ResultsA total of 231 articles (140 unique experiments, 3380 unique participants) were retrieved. The analysis across sleep disorders (n = 95 experiments) identified the subgenual anterior cingulate cortex (176 voxels, z score = 4.86), associated with reward, reasoning, and gustation, and the amygdala and hippocampus (130 voxels, z score = 4.00), associated with negative emotion processing, memory, and olfaction. Both clusters had positive functional connectivity with the default mode network. The right thalamus (153 voxels, z score = 5.21) emerged as a consistent regional alteration following sleep deprivation (n = 45 experiments). This cluster was associated with thermoregulation, action, and pain perception and showed positive functional connectivity with subcortical and (pre)motor regions. Subanalyses regarding the direction of alterations demonstrated that the subgenual anterior cingulate cortex exhibited decreased activation, connectivity, and/or volume, while the amygdala and hippocampus cluster and the thalamus cluster demonstrated increased activation, connectivity, and/or volume.Conclusions and RelevanceDistinct convergent brain abnormalities were observed between long-term sleep disorders (probably reflecting shared symptoms) and short-term sleep deprivation.