Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep

Xi-Jian Dai, Jian Jiang, Zhiqiang Zhang, Xiao Nie, Bi-Xia Liu, Li Pei, Honghan Gong, Jianping Hu, Guangming Lu, Yang Zhan, Xi-Jian Dai, Jian Jiang, Zhiqiang Zhang, Xiao Nie, Bi-Xia Liu, Li Pei, Honghan Gong, Jianping Hu, Guangming Lu, Yang Zhan

Abstract

Background: Insufficient sleep is common in daily life and can lead to cognitive impairment. Sleep disturbance also exists in neuropsychiatric diseases. However, whether and how acute and chronic sleep loss affect brain morphology remain largely unknown. Methods: We used voxel-based morphology method to study the brain structural changes during sleep deprivation (SD) at six time points of rested wakefulness, 20, 24, 32, 36 h SD, and after one night sleep in 22 healthy subjects, and in 39 patients with chronic primary insomnia relative to 39 status-matched good sleepers. Attention network and spatial memory tests were performed at each SD time point in the SD Procedure. The longitudinal data were analyzed using one-way repeated measures ANOVA, and post-hoc analysis was used to determine the between-group differences. Results: Acute SD is associated with widespread gray matter volume (GMV) changes in the thalamus, cerebellum, insula and parietal cortex. Insomnia is associated with increased GMV in temporal cortex, insula and cerebellum. Acute SD is associated with brain atrophy and as SD hours prolong more areas show reduced GMV, and after one night sleep the brain atrophy is restored and replaced by increased GMV in brain areas. SD has accumulative negative effects on attention and working memory. Conclusions: Acute SD and insomnia exhibit distinct morphological changes of GMV. SD has accumulative negative effects on brain morphology and advanced cognitive function. The altered GMV may provide neurobiological basis for attention and memory impairments following sleep loss.

Statement of significance: Sleep is less frequently studied using imaging techniques than neurological and psychiatric disorders. Whether and how acute and chronic sleep loss affect brain morphology remain largely unknown. We used voxel-based morphology method to study brain structural changes in healthy subjects over multiple time points during sleep deprivation (SD) status and in patients with chronic insomnia. We found that prolonged acute SD together with one night sleep recovery exhibits accumulative atrophic effect and recovering plasticity on brain morphology, in line with behavioral changes on attentional tasks. Furthermore, acute SD and chronic insomnia exhibit distinct morphological changes of gray matter volume (GMV) but they also share overlapping GMV changes. The altered GMV may provide structural basis for attention and memory impairments following sleep loss.

Keywords: attention network test; gray matter; insomnia; sleep deprivation; spatial working memory; voxel-based morphometry.

Figures

Figure 1
Figure 1
Schematic diagram of sleep deprivation (SD) procedure.
Figure 2
Figure 2
Schematic diagram of spatial working memory. The task was based on visual recognition of a series of 6 × 6 smaller squares with white. The first, second and third small square were filled with black respectively. Then the fourth square will be filled with black immediately once the first black square was recovered to white. At this time, the subjects were asked to make a keypress response to determine whether the location of the fourth black square was the same with the first black square, or subsequent the fifth was in the same location with the second black square, and so on.
Figure 3
Figure 3
Brain-wide gray matter volume (GMV) differences of the 36 h sleep deprivation (SD) study. Main effect brain areas that passed the statistical criterion using the ANOVA test are marked in red color. Red areas denote positive main effect brain areas in GMV.
Figure 4
Figure 4
Sum and mean gray matter volume (GMV) of all main effect brain areas for each subject in the 36 h sleep deprivation (SD) study. In all subjects, from rested wakefulness (RW) to 36 h SD and from 36 h SD to one night sleep recovery, the total (A) and mean (B) GMV in the main effect brain areas showed a tendency of reduction first and then increase.
Figure 5
Figure 5
Brain-wide gray matter volume (GMV) differences of post-hoc test of each sleep deprivation (SD) time point in the 36 h SD study. The post-hoc test of each SD time point against RW was conducted as the product between the GMV differences of each time point and the GMV differences of main effect brain areas. Brain areas that showed GMV differences at each time point during the 36 h SD procedure against RW from the post-hoc tests, including the time point of 20 h SD (A), 24 h SD (B), 32 h SD (C), 36 h SD (D), and after one night sleep recovery (E). Red areas denote increased GMV (A–E) and green areas denote decreased GMV (C–D) in brain areas.
Figure 6
Figure 6
Brain gray matter volume (GMV) differences without applying mask method using post-hoc t test. Brain GMV differences were conducted using post-hoc t-test without applying the product with the mask of the different brain regions of main effect in 36 h sleep deprivation (SD) study. The statistical threshold was set at family-wise error corrected voxel threshold of p < 0.05 of each time in 36h SD study. The right side of the picture indicates the right side of the brain, and the corresponding left side indicates the left side of the brain. Red areas denote increased GMV brain regions (A–C) and green areas denote decreased GMV (B). (A) Brain GMV differences at 24 h SD relative to rested wakefulness (RW). (B) Brain GMV differences at 36 h SD relative to RW. (C) Brain GMV differences after one night sleep recovery relative to RW.
Figure 7
Figure 7
Brain gray matter volume (GMV) differences of patients with insomnia relative to good sleepers. The statistical threshold was set at uncorrected voxel threshold of p < 0.001 with a minimum cluster threshold of 100 voxels. The right side of the picture indicates the right side of the brain, and the corresponding left side indicates the left side of the brain. Green areas denote decreased GMV and red areas denote increased GMV.
Figure 8
Figure 8
Behavioral findings of attention network test (ANT) and spatial working memory test (SWM). Each behavioral measurement was taken at six time points during the sleep deprivation (SD) session. (A) Accuracy rate of the ANT. (B) Reaction time of the ANT. (C) Lapse rate of the ANT. (D) Reaction time for the alertness, spatial orientation and executive control of the ANT. (E) Accuracy rate of the SWM. (F) Coefficient of variation values of three indexes, including reaction time of the ANT, accuracy rate of the ANT, and accuracy rate of the SWM. Data are presented as mean ± standard values.

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