Altered coupling between resting‐state glucose metabolism and functional activity in epilepsy

Abstract

Objective: Altered functional activities and hypometabolism have been found in medial temporal lobe epilepsy patients with hippocampal sclerosis (mTLE-HS). Hybrid PET/MR scanners provide opportunities to explore the relationship between resting-state energy consumption and functional activities, but whether repeated seizures disturb the bioenergetic coupling and its relationship with seizure outcomes remain unknown. Methods: 18 F-FDG PET and restingstate functional MRI (rs-fMRI) scans were performed with hybrid PET/MR in 26 patients with mTLE-HS and in healthy controls. Energy consumption was quantified by 18 F-FDG standardized uptake value ratio(SUVR) relative to cerebellum. Spontaneous neural activities were estimated using regional homogeneity (ReHo), fractional amplitude of low frequency fluctuations (fALFF) from rs-fMRI. Between-group differences in SUVR and rs-fMRI derived metrics were evaluated by two-sample t test. Voxel-wise spatial correlations were explored between SUVR and ReHo, fALFF across gray matter and compared between groups. Furthermore, the relationships between altered fALFF/SUVR and ReHo/ SUVR coupling and surgical outcomes were evaluated. Results: Both the patients and healthy controls showed significant positive correlations between SUVR and rs-fMRI metrics. Spatial correlations between SUVR and fMRIderived metrics across gray matter were significantly higher in patients with mTLE-HS compared with healthy controls (fALFF/SUVR, P < 0.001; ReHo/ SUVR, P = 0.022). Higher fALFF/SUVR couplings were found in patients who had Engel class IA after surgery than all other (P = 0.025), while altered ReHo/ SUVR couplings (P = 0.097) were not. Conclusion: These findings demonstrated altered bioenergetic coupling across gray matter and its relationship with seizure outcomes, which may provide novel insights into pathogenesis of mTLE-HS and potential biomarkers for epilepsy surgery planning.

How Energy Supports Our Brain to Yield Consciousness: Insights From Neuroimaging Based on the Neuroenergetics Hypothesis

“…Nevertheless, hypermetabolism in focal brain regions/networks is not necessarily associated with an elevated FC and a higher conscious level. For example, although a coupling between the energy consumption and neural activity within a gray matter is reported in epileptic status; however, this metabolic synchronization is spatially heterogeneous throughout the brain, in the regions showing hypermetabolism and an increased FC, generation and propagation of epileptiform activity usually occur; in contrast, in the regions partly located in the areas corresponding to the DMN, showing hypometabolism and an decreased functional activity, information communication is interrupted (Wang et al, 2020 ), suggesting that widespread, asymmetric, and often severe interictal metabolic alterations play a critical role in epileptic loss of consciousness. In other words, a neurometabolic decoupling in neuroglial populations might play a role in a higher coupling, which may be the modulating result linked to the strong hyperexcitability generated by epileptiform activity.…”

Different Features of Metabolic Connectivity Map and Granger Causality Method in Revealing Directed Dopamine Pathways: A Pilot Study Based on Integrated PET/MR

“…Standard uptake value ratio (SUVr) maps were converted by dividing the mean value of reference region. According to previous research [30,31], cerebellum gray matter was chosen as the reference region. With regard to high-resolution PET data acquisition, there was less need to perform partial volume effect correction.…”

A resting‐state fMRI study of temporal lobe epilepsy using multivariate pattern analysis and Granger causality analysis

“…9 Zeng et al used ReHo analysis to confirm abnormal regional synchronization in specific brain regions of patients with mesial TLE. 10 Cheng et al observed increased ReHo values in the hippocampus, thalamus, and parietal lobes but decreased ReHo values in the posterior cerebellum lobe in TLE patients. 11 All these published mass univariate studies investigating ReHo alterations between TLE patients and normal controls (NC) aim to test whether some brain regions have any difference, rather than to test whether these differences can be used to distinguish TLE patients and NC.…”