White matter microstructural perturbations after total sleep deprivation in depression

Brandon Taraku; Artemis Zavaliangos-Petropulu; Joana R Loureiro; Noor B Al-Sharif; Antoni Kubicki; Shantanu H Joshi; Roger P Woods; Randall Espinoza; Katherine L Narr; Ashish K Sahib

doi:10.3389/fpsyt.2023.1195763

White matter microstructural perturbations after total sleep deprivation in depression

Front Psychiatry. 2023 Jun 28:14:1195763. doi: 10.3389/fpsyt.2023.1195763. eCollection 2023.

Authors

Affiliations

¹ Department of Neurology, Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, United States.
² Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, United States.

Abstract

Background: Total sleep deprivation (TSD) transiently reverses depressive symptoms in a majority of patients with depression. How TSD modulates diffusion tensor imaging (DTI) measures of white matter (WM) microstructure, which may be linked with TSD's rapid antidepressant effects, remains uncharacterized.

Methods: Patients with depression (N = 48, mean age = 33, 26 women) completed diffusion-weighted imaging and Hamilton Depression Rating (HDRS) and rumination scales before and after >24 h of TSD. Healthy controls (HC) (N = 53, 23 women) completed the same assessments at baseline, and after receiving TSD in a subset of HCs (N = 15). Tract based spatial statistics (TBSS) investigated voxelwise changes in fractional anisotropy (FA) across major WM pathways pre-to-post TSD in patients and HCs and between patients and HCs at baseline. Post hoc analyses tested for TSD effects for other diffusion metrics, and the relationships between change in diffusion measures with change in mood and rumination symptoms.

Results: Significant improvements in mood and rumination occurred in patients with depression (both p < 0.001), but not in HCs following TSD. Patients showed significant (p < 0.05, corrected) decreases in FA values in multiple WM tracts, including the body of the corpus callosum and anterior corona radiata post-TSD. Significant voxel-level changes in FA were not observed in HCs who received TSD (p > 0.05). However, differential effects of TSD between HCs and patients were found in the superior corona radiata, frontal WM and the posterior thalamic radiation (p < 0.05, corrected). A significant (p < 0.05) association between change in FA and axial diffusivity within the right superior corona radiata and improvement in rumination was found post-TSD in patients.

Conclusion: Total sleep deprivation leads to rapid microstructural changes in WM pathways in patients with depression that are distinct from WM changes associated with TSD observed in HCs. WM tracts including the superior corona radiata and posterior thalamic radiation could be potential biomarkers of the rapid therapeutic effects of TSD. Changes in superior corona radiata FA, in particular, may relate to improvements in maladaptive rumination.

Keywords: depression; diffusion imaging; rumination; sleep deprivation; white matter.

Grants and funding

This work was supported by the National Institute of Mental Health, Grant/Award Number: U01MH110008-01 to KN and RE and the National Institute of Neurological Disorders and Stroke, Grant/Award Number: T32NS048004 to AZ-P. This research was also supported by the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health under the UCLA Clinical and Translational Science Institute (grant number UL1TR001881).