Correspondence between cerebral glucose metabolism and BOLD reveals relative power and cost in human brain

Abstract

The correspondence between cerebral glucose metabolism (indexing energy utilization) and synchronous fluctuations in blood oxygenation (indexing neuronal activity) is relevant for neuronal specialization and is affected by brain disorders. Here, we define novel measures of relative power (rPWR, extent of concurrent energy utilization and activity) and relative cost (rCST, extent that energy utilization exceeds activity), derived from FDG-PET and fMRI. We show that resting-state networks have distinct energetic signatures and that brain could be classified into major bilateral segments based on rPWR and rCST. While medial-visual and default-mode networks have the highest rPWR, frontoparietal networks have the highest rCST. rPWR and rCST estimates are generalizable to other indexes of energy supply and neuronal activity, and are sensitive to neurocognitive effects of acute and chronic alcohol exposure. rPWR and rCST are informative metrics for characterizing brain pathology and alternative energy use, and may provide new multimodal biomarkers of neuropsychiatric disorders.

The effect of chronic neuroglycopenia on resting state networks in GLUT1 syndrome across the lifespan

“…In patients with diabetes, induced hypoglycemia determines broad perturbations of resting state FC patterns with increase connectivity in core nodes including the hypothalamus, basal ganglia, insula, default mode network, sensorimotor, cingulate cortices, and cerebellum while opposite behavior was detected in nondiabetic controls (Bolo et al, ). Interestingly, recurrent hypoglycemia as observed in heavy drinker patients is associated with a stronger positive association between the glucose utilization (measured by FDG‐PET) and neuronal‐glia activity (expressed local FC) in specific brain regions like cerebellum and precuneus (Shokri‐Kojori et al, ). Alcohol abuse leads to increase of the brain acetate utilization and the blood–brain‐barrier transport of acetate (Jiang et al, ).…”

“…Emerging evidences indicate that brain regions may differ in metabolic activity and metabolic supply associations based on regional morphometric and functional proprieties. Under physiological conditions, during rest, the relationship between the glucose utilization and neuroglial activity is heterogeneously distributed with brain regions showing concurrent higher energy utilization and activity (like medial visual and default mode network) and others demonstrating a deviation between glucose utilization and neuroglial activity (Shokri‐Kojori et al, ). The use of energy source other than glucose such as keton bodies could contribute to explain such discrepancy.…”

“…In each subject, seeds' location was verified by superimposing each ROI on individual spatially normalized 3D images and it was checked that the seed does not exceed the boundary of the selected ROI. The rationale for choosing basal ganglia, thalamic, motor and cerebellar regions were based on the available literature on their presumed involvement by PET studies and clinical observation of MDs (Akman et al, ; Pascual, Van Heertum, Wang, Engelstad, & De Vivo, , Pascual et al, ; Vaudano et al, ) while the PCU and visual cortex were selected as presumed to be regions of high‐level of glucose consumption (Ishibashi, Sakurai, Shimoji, Tokumaru, & Ishii, ; Shokri‐Kojori et al, ; Tomasi, Wang, & Volkow, ). After the toolbox had calculated the connectivity for each individual subject, second‐level analyses were performed in order to reveal seed‐based connectivity differences.…”

“…neuronal-glia activity (expressed local FC) in specific brain regions like cerebellum and precuneus (Shokri-Kojori et al, 2019). Alcohol abuse leads to increase of the brain acetate utilization and the blood-brainbarrier transport of acetate (Jiang et al, 2013).…”

“…connected in GLUT1DS. The discrepancy between the visual and cerebellum functional behaviors during chronic reduced glucose supply has been documented by FDG-PET and fMRI studies in heavy drinkers(Shokri-Kojori et al, 2019). Different mechanisms of adaptation based on changes in active glucose metabolic pathways (aerobic glycolysis versus oxidative metabolism in the visual cortex) or the use of alternative source of energy (in the cerebellum) might explain this mismatch (Shokri-Kojori,Tomasi, Wiers, Wang, & Volkow, 2017;Volkow et al, 2015).…”