Sleep-related and diurnal effects on brain diffusivity and cerebrospinal fluid flow

Tuura, Ruth; Volk, Carina; Callaghan, Fraser M.; Jaramillo, Valeria; Huber, Reto

doi:10.1016/j.neuroimage.2021.118420

Cited by 27 publications

(26 citation statements)

References 40 publications

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“…Previous studies revealed slow-wave sleep is the stage at which glymphatic drainage is enhanced 29 . A recent clinical study indicated that increased brain parenchyma mean water diffusivity was positively related to the proportion of total sleep time spent in the REM phase in healthy people 33 . As iRBD patients complained about the disruption of REM sleep due to the RBD symptoms commonly and changes in EEG signature of non-REM sleep have been observed in iRBD 34 , and a potential role of REM sleep oscillations in neurovascular coupling possibly affecting glymphatic activity 35 , 36 , we considered iRBD might result in decreased glymphatic function.…”

Section: Discussionmentioning

confidence: 99%

Neuroimaging evidence of glymphatic system dysfunction in possible REM sleep behavior disorder and Parkinson’s disease

Guo

Wang

et al. 2022

npj Parkinsons Dis.

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Alpha-synucleinopathy is postulated to be central to both idiopathic rapid eye movement sleep behaviour disorder (iRBD) and Parkinson’s disease (PD). Growing evidence suggests an association between the diminished clearance of α-synuclein and glymphatic system dysfunction. However, evidence accumulating primarily based on clinical data to support glymphatic system dysfunction in patients with iRBD and PD is currently insufficient. This study aimed to use diffusion tensor image analysis along the perivascular space (DTI-ALPS) to evaluate glymphatic system activity and its relationship to clinical scores of disease severity in patients with possible iRBD (piRBDs) and those with PD. Further, we validated the correlation between the ALPS index and the prognosis of PD longitudinally. Overall, 168 patients with PD, 119 piRBDs, and 129 healthy controls were enroled. Among them, 50 patients with PD had been longitudinally reexamined. Patients with PD exhibited a lower ALPS index than those with piRBDs (P = 0.036), and both patient groups showed a lower ALPS index than healthy controls (P < 0.001 and P = 0.001). The ALPS index and elevated disease severity were negatively correlated in the piRBD and PD subgroups. Moreover, the ALPS index was correlated with cognitive decline in patients with PD in the longitudinal analyses. In conclusion, DTI-ALPS provided neuroimaging evidence of glymphatic system dysfunction in piRBDs and patients with PD; however, the potential of assessing the pathological progress of α-synucleinopathies as an indicator is worth verifying. Further development of imaging methods for glymphatic system function is also warranted.

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Section: Discussionmentioning

confidence: 99%

Neuroimaging evidence of glymphatic system dysfunction in possible REM sleep behavior disorder and Parkinson’s disease

Guo

Wang

et al. 2022

npj Parkinsons Dis.

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“…It must be noted, however, that this extrapolation does not account for many physiological factors that may vary during the course of 1 h, 24 h or even decades. In fact, recent studies have observed that exercise [ 28 , 29 ], blood flow and blood pressure [ 6 , 30 , 31 ], as well as sleep [ 17 , 32 ] and respiration [ 33 – 38 ] contribute to changes in CSF flow. Moreover, overlap of stroke volume measurements between consecutive cycles was not considered in this extrapolation and should be investigated in further studies.…”

Section: Discussionmentioning

confidence: 99%

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Muccio

Chu²,

Minkoff³

et al. 2021

Fluids Barriers CNS

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Background Cerebrospinal fluid (CSF) circulation between the brain and spinal canal, as part of the glymphatic system, provides homeostatic support to brain functions and waste clearance. Recently, it has been observed that CSF flow is strongly driven by cardiovascular brain pulsation, and affected by body orientation. The advancement of MRI has allowed for non-invasive examination of the CSF hydrodynamic properties. However, very few studies have addressed their relationship with body position (e.g., upright versus supine). It is important to understand how CSF hydrodynamics are altered by body position change in a single cardiac phase and how cumulative long hours staying in either upright or supine position can affect craniocervical CSF flow. Methods In this study, we investigate the changes in CSF flow at the craniocervical region with flow-sensitive MRI when subjects are moved from upright to supine position. 30 healthy volunteers were imaged in upright and supine positions using an upright MRI. The cranio-caudal and caudo-cranial CSF flow, velocity and stroke volume were measured at the C2 spinal level over one cardiac cycle using phase contrast MRI. Statistical analysis was performed to identify differences in CSF flow properties between the two positions. Results CSF stroke volume per cardiac cycle, representing CSF volume oscillating in and out of the cranium, was ~ 57.6% greater in supine (p < 0.0001), due to a ~ 83.8% increase in caudo-cranial CSF peak velocity during diastole (p < 0.0001) and extended systolic phase duration when moving from upright (0.25 ± 0.05 s) to supine (0.34 ± 0.08 s; p < 0.0001). Extrapolation to a 24 h timeframe showed significantly larger total CSF volume exchanged at C2 with 10 h spent supine versus only 5 h (p < 0.0001). Conclusions In summary, body position has significant effects on CSF flow in and out of the cranium, with more CSF oscillating in supine compared to upright position. Such difference was driven by an increased caudo-cranial diastolic CSF velocity and an increased systolic phase duration when moving from upright to supine position. Extrapolation to a 24 h timeframe suggests that more time spent in supine position increases total amount of CSF exchange, which may play a beneficial role in waste clearance in the brain.

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“…Additionally, anaesthesia increased glymphatic influx and efflux, indicating that the sleep-wake state may be more responsible for determining the interstitial volume and glymphatic solute clearance efficacy compared to the circadian rhythm [ 59 ]. Conversely, Tuura and colleagues found, after using MRI and electroencephalogram analysis in rodents, there was an increase in water diffusivity during sleep which was positively correlated with the REM sleep stage and negatively correlated with the non-REM sleep stage [ 60 ]. Although CSF flow increases overnight were found to be unrelated to sleep and diffusivity measures, these findings may suggest interstitial clearance is optimal during REM sleep.…”

Section: Glymphatic System Dysfunction In Parkinson’s Disease Pathologymentioning

confidence: 99%

Glymphatic System Dysfunction and Sleep Disturbance May Contribute to the Pathogenesis and Progression of Parkinson’s Disease

Scott-Massey

Boag

Magnier

et al. 2022

IJMS

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Parkinson’s disease (PD) is a multisystem alpha-synucleinopathic neurodegenerative disease and the most prevalent neurodegenerative disorder after Alzheimer’s disease with a high incidence rate in the elderly population. PD is highly multifactorial in etiology and has complex and wide-ranging pathogenic mechanisms. Environmental exposures and genetic predisposition are prominent risk factors. However, current evidence suggests that an intimate link may exist between the risk factor of sleep disturbance and PD pathogenesis. PD is characterized by the pathological hallmarks of alpha-synuclein aggregations and dopaminergic neuron degeneration in the substantia nigra. The loss of dopamine-producing neurons results in both motor and non-motor symptoms, most commonly, bradykinesia, tremor, rigidity, psychiatric disorders, sleep disorders and gastrointestinal problems. Factors that may exacerbate alpha-synuclein accumulation and dopamine neuron loss include neuroinflammation and glymphatic system impairment. Extracellular alpha-synuclein can induce an inflammatory response which can lead to neural cell death and inhibition of neurogenesis. The glymphatic system functions most optimally to remove extracellular brain solutes during sleep and therefore sleep disruption may be a crucial progression factor as well as a risk factor. This literature review interprets and analyses data from experimental and epidemiological studies to determine the recent advances in establishing a relationship between glymphatic system dysfunction, sleep disturbance, and PD pathogenesis and progression. This review addresses current limitations surrounding the ability to affirm a causal link between improved glymphatic clearance by increased sleep quality in PD prevention and management. Furthermore, this review proposes potential therapeutic approaches that could utilize the protective mechanism of sleep, to promote glymphatic clearance that therefore may reduce disease progression as well as symptom severity in PD patients.

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Sleep-related and diurnal effects on brain diffusivity and cerebrospinal fluid flow

Cited by 27 publications

References 40 publications

Neuroimaging evidence of glymphatic system dysfunction in possible REM sleep behavior disorder and Parkinson’s disease

Neuroimaging evidence of glymphatic system dysfunction in possible REM sleep behavior disorder and Parkinson’s disease

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Glymphatic System Dysfunction and Sleep Disturbance May Contribute to the Pathogenesis and Progression of Parkinson’s Disease

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