Gray matter-specific changes in brain bioenergetics after acute sleep deprivation: a 31P magnetic resonance spectroscopy study at 4 Tesla.

Abstract

STUDY OBJECTIVES:

A principal function of sleep may be restoration of brain energy metabolism caused by the energetic demands of wakefulness. Because energetic demands in the brain are greater in gray than white matter, this study used linear mixed-effects models to examine tissue-type specific changes in high-energy phosphates derived using 31P magnetic resonance spectroscopy (MRS) after sleep deprivation and recovery sleep.

DESIGN:

Experimental laboratory study.

SETTING:

Outpatient neuroimaging center at a private psychiatric hospital.

PARTICIPANTS:

A total of 32 MRS scans performed in eight healthy individuals (mean age 35 y; range 23-51 y).

INTERVENTIONS:

Phosphocreatine (PCr) and β-nucleoside triphosphate (NTP) were measured using 31P MRS three dimensional-chemical shift imaging at high field (4 Tesla) after a baseline night of sleep, acute sleep deprivation (SD), and 2 nights of recovery sleep. Novel linear mixed-effects models were constructed using spectral and tissue segmentation data to examine changes in bioenergetics in gray and white matter.

MEASUREMENTS AND RESULTS:

PCr increased in gray matter after 2 nights of recovery sleep relative to SD with no significant changes in white matter. Exploratory analyses also demonstrated that increases in PCr were associated with increases in electroencephalographic slow wave activity during recovery sleep. No significant changes in β-NTP were observed.

CONCLUSIONS:

These results demonstrate that sleep deprivation and subsequent recovery-induced changes in high-energy phosphates primarily occur in gray matter, and increases in PCr after recovery sleep may be related to sleep homeostasis.

• Authors: David T Plante, George H Trksak, J Eric Jensen, David M Penetar, Caitlin Ravichandran, Brady A Riedner, Wendy L Tartarini, Cynthia M Dorsey, Perry F Renshaw, Scott E Lukas, David G Harper
• Journal: Sleep (Sleep) Vol. 37 Issue 12 Pg. 1919-27 (Dec 01 2014) ISSN: 1550-9109 [Electronic] United States
• PMID: 25325507 (Publication Type: Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't)
• Copyright: © 2014 Associated Professional Sleep Societies, LLC.

Chemical References

• Nucleotides
• Phosphocreatine

Topics

• Adult
• Electroencephalography
• Energy Metabolism
• Female
• Gray Matter (metabolism, physiopathology)
• Healthy Volunteers
• Homeostasis
• Humans
• Magnetic Resonance Spectroscopy
• Male
• Middle Aged
• Nucleotides (metabolism)
• Phosphocreatine (metabolism)
• Secondary Metabolism
• Sleep (physiology)
• Sleep Deprivation (metabolism, physiopathology)
• White Matter (metabolism)
• Young Adult