Microstructure of frontoparietal connections predicts individual resistance to sleep deprivation

Cui, Jike; Tkachenko, Olga; Gogel, Hannah; Kipman, Maia; Preer, Lily; Weber, Marcel; Divatia, Shreya C.; Demers, Lauren A.; Olson, Elizabeth A.; Buchholz, Jennifer L.; Bark, John S.; Rosso, Isabelle M.; Rauch, Scott L.; Killgore, William D. S.

doi:10.1016/j.neuroimage.2014.11.035

Cited by 48 publications

(32 citation statements)

References 43 publications

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“…To the best of our knowledge, the left IFOF does not play a role in mediating sleep, although a recent study found that frontoparietal connection strength predicts individual resistance to sleep deprivation. 35 Therefore, left IFOF WM atrophy could exacerbate poor sleep quality in patients with CFS.…”

Section: Discussionmentioning

confidence: 99%

Medial prefrontal cortex deficits correlate with unrefreshing sleep in patients with chronic fatigue syndrome

et al. 2017

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Funding information The Judith Jane Mason FoundationUnrefreshing sleep is a hallmark of chronic fatigue syndrome/myalgic encephalomyelitis (CFS).This study examined brain structure variations associated with sleep quality in patients with CFS. 38 patients with CFS (34.8 ± 10.1 years old) and 14 normal controls (NCs) (34.7 ± 8.4 years old) were recruited. All subjects completed the Hospital Anxiety and Depression Scale, Pittsburgh Sleep Quality Index (PSQI), and Chalder Fatigue Scale (CFQ) questionnaires. Brain MRI measures included global and regional grey and white matter volumes, magnetization transfer T 1 weighted (MT-T1w) intensities, and T 1 weighted (T1w) and T 2 weighted spin echo signal intensities. We performed voxel based group comparisons of these regional brain MRI measures and regressions of these measures with the PSQI and CFQ scales adjusted for age, anxiety and depression, and the appropriate global measure. In CFS patients, negative correlations were observed in the medial prefrontal cortex (mPFC) between PSQI and MT-T1w intensities (family-wise error corrected cluster, P FWE < 0.05) and between PSQI and T1w intensities (P FWE < 0.05). In the same mPFC location, both MT and T1w intensities were lower in CFS patients compared with NCs (uncorrected voxel P < 0.001). This study is the first to report that brain structural differences are associated with unrefreshing sleep in CFS. This result refutes the suggestion that unrefreshing sleep is a misperception in CFS patients and further investigation of this symptom is warranted. Sleep plays an important role in human health and well-being, with its recuperative, restorative, and learning consolidation properties. 4,5Unrefreshing sleep is a hallmark of ME/CFS that causes patients to wake up feeling tired even after extended periods of sleep, to experience excessive daytime sleepiness, and to have difficulty falling asleep and staying asleep. Therefore, unrefreshing sleep results at least in worsening fatigue symptoms and adds to the 'illness burden' in CFS patients. 6 Roughly 91% of CFS patients report unrefreshing sleep regardless of adequate sleep duration. 7 The effect of unrefreshing sleep is of importance in CFS aetiology because sleep disturbance can cause fatigue, myalgia, and poor attention. 8 A recent path analysis study, exploring the interrelationship of different symptoms in CFS, found that poor sleep quality directly impacted on

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Section: Discussionmentioning

confidence: 99%

Medial prefrontal cortex deficits correlate with unrefreshing sleep in patients with chronic fatigue syndrome

et al. 2017

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“…Previous studies suggested that specific structural measures taken at rest may reflect the degree of individual cognitive vulnerability to sleep deprivation (Cui et al, 2015; Rocklage et al, 2009). Here, we found that structural changes occurring during extended wake can be used to predict individual vigilance levels, and may partially contribute to predict variation in specific behavioral measures related to performance in an impulse control test.…”

Section: Discussionmentioning

confidence: 99%

Sleep reverts changes in human gray and white matter caused by wake-dependent training

et al. 2016

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Learning leads to rapid microstructural changes in grey (GM) and white (WM) matter. Do these changes continue to accumulate if task training continues, and can they be reverted by sleep? We addressed these questions by combining structural and diffusion weighted MRI and high-density EEG in 16 subjects studied during the physiological sleep/wake cycle, after 12h and 24h of intense practice in two different tasks, and after post-training sleep. Compared to baseline wake, 12h of training led to a decline in cortical mean diffusivity. The decrease became even more significant after 24h of task practice combined with sleep deprivation. Prolonged practice also resulted in decreased ventricular volume and increased GM and WM subcortical volumes. All changes reverted after recovery sleep. Moreover, these structural alterations predicted cognitive performance at the individual level, suggesting that sleep's ability to counteract performance deficits is linked to its effects on the brain microstructure. The cellular mechanisms that account for the structural effects of sleep are unknown, but they may be linked to its role in promoting the production of cerebrospinal fluid and the decrease in synapse size and strength, as well as to its recently discovered ability to enhance the extracellular space and the clearance of brain metabolites.

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“…Another study examined whether differences in white matter microstructure may explain individual differences in vulnerability to sleep deprivation, finding that individuals more susceptible to sleep deprivation had lower FA values than less susceptible subjects in multiple brain regions (Rocklage et al, ). Similarly, higher FA values in the white matter of frontoparietal regions predicted better resistance to sleep deprivation (Cui et al, ). More recently, using a whole‐brain multimodal MRI approach 86 participants were investigated to explore the association between subjective sleep quality (PSQI global score) and functional and structural connectivity.…”

Section: Sleep and Myelinmentioning

confidence: 95%

The role of sleep and wakefulness in myelin plasticity

Vivo

Bellesi

2019

Glia

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Myelin plasticity is gaining increasing recognition as an essential partner to synaptic plasticity, which mediates experience‐dependent brain structure and function. However, how neural activity induces adaptive myelination and which mechanisms are involved remain open questions. More than two decades of transcriptomic studies in rodents have revealed that hundreds of brain transcripts change their expression in relation to the sleep–wake cycle. These studies consistently report upregulation of myelin‐related genes during sleep, suggesting that sleep represents a window of opportunity during which myelination occurs. In this review, we summarize recent molecular and morphological studies detailing the dependence of myelin dynamics after sleep, wake, and chronic sleep loss, a condition that can affect myelin substantially. We present novel data about the effects of sleep loss on the node of Ranvier length and provide a hypothetical mechanism through which myelin changes in response to sleep loss. Finally, we discuss the current findings in humans, which appear to confirm the important role of sleep in promoting white matter integrity.

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Microstructure of frontoparietal connections predicts individual resistance to sleep deprivation

Cited by 48 publications

References 43 publications

Medial prefrontal cortex deficits correlate with unrefreshing sleep in patients with chronic fatigue syndrome

Medial prefrontal cortex deficits correlate with unrefreshing sleep in patients with chronic fatigue syndrome

Sleep reverts changes in human gray and white matter caused by wake-dependent training

The role of sleep and wakefulness in myelin plasticity

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