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Evaluating the gray and white matter energy budgets of human brain function.

ABSTRACT: The insatiable appetite for energy to support human brain function is mainly supplied by glucose oxidation (CMR_glc(ox)). But how much energy is consumed for signaling and nonsignaling processes in gray/white matter is highly debated. We examined this issue by combining metabolic measurements of gray/white matter and a theoretical calculation of bottom-up energy budget using biophysical properties of neuronal/glial cells in conjunction with species-exclusive electrophysiological and morphological data. We calculated a CMR_glc(ox)-derived budget and confirmed it with experimental results measured by PET, autoradiography, ¹³C-MRS, and electrophysiology. Several conserved principles were observed regarding the energy costs for brain's signaling and nonsignaling components in both human and rat. The awake resting cortical signaling processes and mass-dependent nonsignaling processes, respectively, demand ?70% and ?30% of CMR_glc(ox). Inhibitory neurons and glia need 15-20% of CMR_glc(ox), with the rest demanded by excitatory neurons. Nonsignaling demands dominate in white matter, in near opposite contrast to gray matter demands. Comparison between ¹³C-MRS data and calculations suggests ?1.2?Hz glutamatergic signaling rate in the awake human cortex, which is ?4 times lower than signaling in the rat cortex. Top-down validated bottom-up budgets could allow computation of anatomy-based CMR_glc(ox) maps and accurate cellular level interpretation of brain metabolic imaging.

SUBMITTER: Yu Y

PROVIDER: S-EPMC6092772 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Evaluating the gray and white matter energy budgets of human brain function.

Yu Yuguo Y Herman Peter P Rothman Douglas L DL Agarwal Divyansh D Hyder Fahmeed F

Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism 20170607 8

The insatiable appetite for energy to support human brain function is mainly supplied by glucose oxidation (CMR<sub>glc(ox)</sub>). But how much energy is consumed for signaling and nonsignaling processes in gray/white matter is highly debated. We examined this issue by combining metabolic measurements of gray/white matter and a theoretical calculation of bottom-up energy budget using biophysical properties of neuronal/glial cells in conjunction with species-exclusive electrophysiological and mo ...[more]

PMID: 28589753

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Project description:BackgroundCholine is an essential nutrient that is pivotal to proper brain development. Research in animal models suggests that perinatal choline deficiency influences neuron development in the hippocampus and cortex, yet these observations require invasive techniques.ObjectiveThis study aimed to characterize the effects of perinatal choline deficiency on gray and white matter development with the use of noninvasive neuroimaging techniques in young pigs.MethodsDuring the last 64 d of the 114-d gestation period Yorkshire sows were provided with a choline-sufficient (CS) or choline-deficient (CD) diet, analyzed to contain 1214 mg or 483 mg total choline/kg diet, respectively. Upon farrowing, pigs (Sus scrofa domesticus) were allowed colostrum consumption for ≤48 h, were further stratified into postnatal treatment groups, and were provided either CS or CD milk replacers, analyzed to contain 1591 or 518 mg total choline/kg diet, respectively, for 28 d. At 30 d of age, pigs were subjected to MRI procedures to assess brain development. Gray and white matter development was assessed through voxel-based morphometry (VBM) and tract-based spatial statistics (TBSS) to assess the effects of prenatal and postnatal dietary choline status.ResultsVBM analysis indicated that prenatally CS pigs exhibited increased (P < 0.01) gray matter in the left and right cortex compared with prenatally CD pigs. Analysis of white matter indicated that prenatally CS pigs exhibited increased (P < 0.01) white matter in the internal capsule, putamen-globus pallidus, and right cortex compared with prenatally CD pigs. No postnatal effects (P > 0.05) of choline status were noted for VBM analyses of gray and white matter. TBSS also showed no significant effects (P > 0.05) of prenatal or postnatal choline status for diffusion values along white matter tracts.ConclusionsObservations from this study suggest that prenatal choline deficiency results in altered cortical gray matter and reduced white matter in the internal capsule and putamen of young pigs. With the use of noninvasive neuroimaging techniques, results from our study indicate that prenatal choline deficiency greatly alters gray and white matter development in pigs, thereby providing a translational assessment that may be used in clinical populations.

Dataset Information

Evaluating the gray and white matter energy budgets of human brain function.

Publications

Evaluating the gray and white matter energy budgets of human brain function.

Similar Datasets

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