Nocturnal increase in cerebrospinal fluid secretion as a circadian regulator of intracranial pressure
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Nocturnal increase in cerebrospinal fluid secretion as a circadian regulator of intracranial pressure. / Steffensen, Annette Buur; Edelbo, Beatriche Louise; Barbuskaite, Dagne; Andreassen, Søren Norge; Olsen, Markus Harboe; Møller, Kirsten; MacAulay, Nanna.
In: Fluids and Barriers of the CNS, Vol. 20, No. 1, 49, 2023.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Nocturnal increase in cerebrospinal fluid secretion as a circadian regulator of intracranial pressure
AU - Steffensen, Annette Buur
AU - Edelbo, Beatriche Louise
AU - Barbuskaite, Dagne
AU - Andreassen, Søren Norge
AU - Olsen, Markus Harboe
AU - Møller, Kirsten
AU - MacAulay, Nanna
N1 - Publisher Copyright: © 2023, The Author(s).
PY - 2023
Y1 - 2023
N2 - Background: It is crucial to maintain the intracranial pressure (ICP) within the physiological range to ensure proper brain function. The ICP may fluctuate during the light-dark phase cycle, complicating diagnosis and treatment choice in patients with pressure-related disorders. Such ICP fluctuations may originate in circadian or sleep-wake cycle-mediated modulation of cerebrospinal fluid (CSF) flow dynamics, which in addition could support diurnal regulation of brain waste clearance. Methods: ICP was monitored continuously in patients who underwent placement of an external ventricular drain (EVD) and by telemetric monitoring in experimental rats. CSF was collected via the EVD in patients and the rodent CSF secretion rate determined by in vivo experimentation. Rodent choroid plexus transporter transcripts were quantified with RNAseq and transport activity with ex vivo isotope transport assays. Results: We demonstrated that ICP increases by 30% in the dark phase in both species, independently of vascular parameters. This increase aligns with elevated CSF collection in patients (12%) and CSF production rate in rats (20%), the latter obtained with the ventriculo-cisternal perfusion assay. The dark-phase increase in CSF secretion in rats was, in part, assigned to increased transport activity of the choroid plexus Na+,K+,2Cl- cotransporter (NKCC1), which is implicated in CSF secretion by this tissue. Conclusion: CSF secretion, and thus ICP, increases in the dark phase in humans and rats, irrespective of their diurnal/nocturnal activity preference, in part due to altered choroid plexus transport activity in the rat. Our findings suggest that CSF dynamics are modulated by the circadian rhythm, rather than merely sleep itself.
AB - Background: It is crucial to maintain the intracranial pressure (ICP) within the physiological range to ensure proper brain function. The ICP may fluctuate during the light-dark phase cycle, complicating diagnosis and treatment choice in patients with pressure-related disorders. Such ICP fluctuations may originate in circadian or sleep-wake cycle-mediated modulation of cerebrospinal fluid (CSF) flow dynamics, which in addition could support diurnal regulation of brain waste clearance. Methods: ICP was monitored continuously in patients who underwent placement of an external ventricular drain (EVD) and by telemetric monitoring in experimental rats. CSF was collected via the EVD in patients and the rodent CSF secretion rate determined by in vivo experimentation. Rodent choroid plexus transporter transcripts were quantified with RNAseq and transport activity with ex vivo isotope transport assays. Results: We demonstrated that ICP increases by 30% in the dark phase in both species, independently of vascular parameters. This increase aligns with elevated CSF collection in patients (12%) and CSF production rate in rats (20%), the latter obtained with the ventriculo-cisternal perfusion assay. The dark-phase increase in CSF secretion in rats was, in part, assigned to increased transport activity of the choroid plexus Na+,K+,2Cl- cotransporter (NKCC1), which is implicated in CSF secretion by this tissue. Conclusion: CSF secretion, and thus ICP, increases in the dark phase in humans and rats, irrespective of their diurnal/nocturnal activity preference, in part due to altered choroid plexus transport activity in the rat. Our findings suggest that CSF dynamics are modulated by the circadian rhythm, rather than merely sleep itself.
KW - Cerebrospinal fluid
KW - Choroid plexus
KW - Circadian rhythm
KW - Intracranial pressure
KW - Na,K,2Cl cotransporter
KW - Na/K-ATPase
KW - Sleep
U2 - 10.1186/s12987-023-00451-2
DO - 10.1186/s12987-023-00451-2
M3 - Journal article
C2 - 37353833
AN - SCOPUS:85163001747
VL - 20
JO - Fluids and Barriers of the CNS
JF - Fluids and Barriers of the CNS
SN - 2045-8118
IS - 1
M1 - 49
ER -
ID: 358638675