Brain Structural and Functional Alterations Specific to Low Sleep Efficiency in Major Depressive Disorder.

Ying Yang,Jiajia Zhu,Yongqiang Yu,Biao Zhang,Dao-Min Zhu,Chunli Wang,Yu Zhang,Wenming Zhao,Cun Zhang

doi:10.3389/fnins.2020.00050

Abstract

BackgroundSleep disturbance is common in patients with major depressive disorder (MDD), but the exploration of its neural underpinnings is limited by subjective sleep measurement and single-modality neuroimaging analyses.MethodsNinety six patients with MDD underwent polysomnography examinations and multi-modal magnetic resonance imaging (MRI) scans. According to sleep efficiency, patients were subdivided into well-matched normal sleep efficiency (NSE, N = 42; 14 men; aged 43 ± 10 years) and low sleep efficiency (LSE, N = 54; 23 men; aged 45 ± 12 years) groups. Inter-group differences in brain structure and function were examined by applying voxel-based morphometry (VBM), regional homogeneity (ReHo) and functional connectivity strength (FCS), and tract-based spatial statistics (TBSS) approaches to structural, functional, and diffusion MRI data, respectively.ResultsThere was no significant difference in gray matter volume (GMV) between the NSE and LSE groups. Compared with the NSE group, the LSE group showed increased axial diffusivity in the left superior and posterior corona radiata, and left posterior limb and retrolenticular part of internal capsule. In addition, the LSE group exhibited decreased ReHo in the bilateral lingual gyri and right postcentral gyrus yet increased FCS in the left angular gyrus relative to the NSE group. Moreover, validation analyses revealed that these results remained after adjusting for the medication effect.ConclusionOur data indicate that preserved gray matter morphology, impaired white matter integrity, and decreased local synchronization degree yet increased FCS are specific to low SE in MDD patients. These findings of disassociation between structural and functional alterations might provide insights into the neural mechanisms of sleep disturbance in depression.

Highlights

Major depressive disorder (MDD) is a prevalent psychiatric illness affecting more than 300 million people of all ages worldwide, and it is characterized by abnormalities in mood, cognition, neurovegetative function, and psychomotor activity (American Psychiatric Association, 2013; World Health Organization [WHO], 2017; Frankish et al, 2018)
For the demographic and clinical data, the normal sleep efficiency (NSE) and low sleep efficiency (LSE) groups did not differ in age, education (t = −0.240, P = 0.811), body mass index (BMI) (t = −0.885, P = 0.379), total intracranial volume (TIV) (t = −1.621, P = 0.108), frame-wise displacement (FD) (t = 1.189, P = 0.238), onset age (t = −1.341, P = 0.183), duration of illness (t = 0.954, P = 0.343), Hamilton Rating Scale for Depression (HAMD) (t = −0.335, P = 0.739), Hamilton Rating Scale for Anxiety (HAMA) (t = −0.814, P = 0.417), Pittsburgh Sleep Quality Index (PSQI) (t = −0.162, P = 0.872), Epworth Sleepiness Scale (ESS) (t = −0.608, P = 0.545) and sex (Chi-square test, χ2 = 0.855, P = 0.355)
For the PSG data, the two groups did not differ in time in bed (TIB) (t = −1.135, P = 0.259), the LSE group had decreased total sleep time (TST) (t = 5.811, P < 0.001), non-rapid eye movements (NREM) duration (t = 4.121, P < 0.001), rapid eye movements (REM) duration (t = 3.075, P = 0.003), and sleep efficiency (SE) (t = 13.135, P < 0.001) relative to the NSE group

Summary

Introduction

Major depressive disorder (MDD) is a prevalent psychiatric illness affecting more than 300 million people of all ages worldwide, and it is characterized by abnormalities in mood, cognition, neurovegetative function, and psychomotor activity (American Psychiatric Association, 2013; World Health Organization [WHO], 2017; Frankish et al, 2018). McKinnon et al (2018) suggested that sleep disturbance [the total score of Pittsburgh Sleep Quality Index (PSQI) > 5] in older people with a lifetime history of depression was related to increased functional connectivity in the default mode network. These studies measured sleep quality using subjective scales (e.g., PSQI) rather than objective tools [e.g., polysomnography (PSG)] and the neuroimaging analyses only focused on a single MRI modality. Sleep disturbance is common in patients with major depressive disorder (MDD), but the exploration of its neural underpinnings is limited by subjective sleep measurement and single-modality neuroimaging analyses

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