Increased interhemispheric resting-state functional connectivity after sleep deprivation: a resting-state fMRI study

Abstract

Several functional imaging studies have investigated the regional effects of sleep deprivation (SD) on impaired brain function; however, potential changes in the functional interactions between the cerebral hemispheres after SD are not well understood. In this study, we used a recently validated approach, voxel-mirrored homotopic connectivity (VMHC), to directly examine the changes in interhemispheric homotopic resting-state functional connectivity (RSFC) after SD. Resting-state functional MRI (fMRI) was performed in 28 participants both after rest wakefulness (RW) and a total night of SD. An interhemispheric RSFC map was obtained by calculating the Pearson correlation (Fisher Z transformed) between each pair of homotopic voxel time series for each subject in each condition. The between-condition differences in interhemispheric RSFC were then examined at global and voxelwise levels separately. Significantly increased global VMHC was found after sleep deprivation; specifically, a significant increase in VMHC was found in specific brain regions, including the thalamus, paracentral lobule, supplementary motor area, postcentral gyrus and lingual gyrus. No regions showed significantly reduced VMHC after sleep deprivation. Further analysis indicates that these findings did not depend on the various sizes of smoothing kernels that were adopted in the preprocessing steps and that the differences in these regions were still significant with or without global signal regression. Our data suggest that the increased VMHC might reflect the compensatory involvement of bilateral brain areas, especially the bilateral thalamus, to prevent cognitive performance deterioration when sleep pressure is elevated after sleep deprivation. Our findings provide preliminary evidence of interhemispheric correlation changes after SD and contribute to a better understanding of the neural mechanisms of SD.

Increased interhemispheric resting-state functional connectivity in healthy participants with insomnia symptoms

“…[6] In the present study, we revealed increased VMHC in the bilateral thalamus/posterior insula (including anterior insula), fusiform, middle cingulate gyrus, inferior parietal lobe, and postcentral gyrus in healthy participants with sleep disturbance. According to increased VMHC induced by sleep deprivation [21] and reduced frontal–parietal activation after sleep deprivation, [6] our results might reflect compensatory adaptation for dysfunction of the cognitive network after sleep disturbance. Obviously, a more comprehensive task design is needed to test this hypothesis.…”

“…[29] Insomnia mechanisms modulating the arousal network has been suggested from the thalamus. [30–32] Zhu et al [21] reveal a significant increase in VMHC in the thalamus in 28 healthy participants after a total night of sleep deprivation. Li et al [18] find reduced fractional anisotropy in the thalamus, as well as negative correlation between fractional anisotropy in the thalamus and disease duration, in primary insomnia.…”

“…The increased interhemispheric synchrony or homotopy in specific brain regions, such as the thalamus and postcentral gyrus, has been associated with sleep deprivation [21] and studies have shown increased connectivity between insula and emotion-related regions and decreased connectivity between insula and cognitive-related regions in primary insomnia patients. [48] Since VMHC can reflect interhemispheric disturbance of functional coordination for high-level functions, such as cognitive control, interoception, and emotion regulation, [49,50] it may provide more complete evidence for interhemispheric disconnection associated with insomnia.…”

“…[20] Importantly, homotopic functional connectivity may reflect interhemispheric coordination for integrating the brain functions underlying coherent cognition, emotion, and behavior. [21] This method enables clinicians to gain additional insight into the functional organization of the brain in patients with traumatic axonal injury, depression, heroin-dependence, and sleep deprivation. [11,20,22,23] The purpose of the present study was to analyze the integrity of interhemispheric interactions between healthy participants with insomnia symptoms and healthy participants without insomnia symptoms.…”

Dynamics of cerebral responses to sustained attention performance during one night of sleep deprivation

“…The increased activation within DMN regions suggested a decreased efficiency in segregation of the DMN from task. Increased activation was also found in the thalamus in our study, which is consistent with previous TSD imaging studies (Chee and Chuah, ; Zhu et al ., ). These studies suggested a compensatory role of the thalamus for increasing the arousal level to counteract elevated sleep pressure after TSD (Chee and Chuah, ).…”