White matter microstructural perturbations after total sleep deprivation in depression - PubMed (original) (raw)

White matter microstructural perturbations after total sleep deprivation in depression

Brandon Taraku et al. Front Psychiatry. 2023.

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.

Copyright © 2023 Taraku, Zavaliangos-Petropulu, Loureiro, Al-Sharif, Kubicki, Joshi, Woods, Espinoza, Narr and Sahib.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1

FIGURE 1

Box plots showing the distribution of HDRS and rumination scores in healthy controls (Blue) and patients (Red) pre-to-post TSD (**p < 0.01 and ***p < 0.001).

FIGURE 2

FIGURE 2

(A) White matter clusters showing significant decrease (in blue, p < 0.05 FWE corrected) in fractional anisotropy (FA) in the corpus callosum and the anterior corona radiata. (B) Box plots showing the distribution of FA values for healthy controls (Blue) and patients (Red) for the corpus callosum and anterior corona radiata (*p < 0.05, **p < 0.01, and ***p < 0.001). R, right, L, left.

FIGURE 3

FIGURE 3

(A) White matter clusters showing significant difference (orange, p < 0.05 FWE corrected) for change in fractional anisotropy (FA) pre-to-post TSD between controls and patients. (B) Box plots showing distribution of FA, axial (C), radial (D), and mean (E) diffusivity values for healthy controls (Blue) and patients (Red) in the superior corona radiata, frontal lobe and the posterior thalamic radiation pre and post TSD. (*p < 0.05, **p < 0.01, and ***p < 0.001). R, right, L, left.

FIGURE 4

FIGURE 4

(A) Regional correlates of DTI measures from the superior corona radiata. (B) Change in fractional anisotropy (FA) showed a significant (p = 0.01) positive correlation with change in rumination. (C) Change in axial diffusivity (AD) showed a significant (p = 0.038) positive correlation with change in rumination. R, right, L, left.

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