Task-relevant brain networks identified with simultaneous PET/MR imaging of metabolism and connectivity

Abstract

Except for task-specific functional MRI, the vast majority of imaging studies assessed human brain function at resting conditions. However, tracking task-specific neuronal activity yields important insight how the brain responds to stimulation. We specifically investigated changes in glucose metabolism, functional connectivity and white matter microstructure during task performance using several recent methodological advancements. Opening the eyes and right finger tapping had elicited an increased glucose metabolism in primary visual and motor cortices, respectively. Furthermore, a decreased metabolism was observed in the regions of the default mode network, which allowed absolute quantification of commonly described deactivations during cognitive tasks. These brain regions showed widespread task-specific changes in functional connectivity, which stretched beyond their primary resting-state networks and presumably reflected the level of recruitment of certain brain regions for each task. Finally, the corresponding white matter fiber pathways exhibited changes in axial and radial diffusivity during the tasks, which were regionally distinctive for certain tract groups. These results highlight that even simple task performance leads to substantial changes of entire brain networks. Exploiting the complementary nature of the different imaging modalities may reveal novel insights how the brain processes external stimuli and which networks are involved in certain tasks.Electronic supplementary materialThe online version of this article (10.1007/s00429-017-1558-0) contains supplementary material, which is available to authorized users.

Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex

“…Our results complement and extend the small number of existing simultaneous BOLD-fMRI/FDG-PET studies reported to date. Consistent with Riedl et al (17) and Wehrl et al (16), we found that blood oxygenation changes in the tissue were related to changes in glucose metabolism in the visual network (however Hahn et al, 2018 (21) found no relationship between glucose metabolism and functional connectivity in the visual and motor cortices using simultaneous BOLD-fMRI/FDG-fPET). Riedl et al (17) showed that local glucose metabolism was highly correlated with BOLD functional connectivity using a simultaneous BOLD-fMRI/FDG-PET with bolus design comparing eyes open versus closed rest, consistent with results obtained in non-simultaneously acquired data (39,(44)(45)(46).…”

“…(39)) which can be very informative but do not allow quantitative inferences to be made. Most existing BOLD-fMRI/FDG-PET studies use a data integration approach, where data from each modality is analysed separately and compared at the second-level using correlation (e.g., (16,21,45,46,48)) or similarity metrics (e.g., (40)). A data integration approach is useful for examining broad relationships between data types, but does not fully capitalise on the shared information between the modalities.…”

“…In a proof-of-concept study, Villien et al (19) adapted the constant infusion technique (18) and used simultaneous MR/FDG-fPET (but not fMRI) to show dynamic changes in glucose metabolism in response to checkerboard stimulation in the visual cortex with a temporal resolution of approximately one minute. Subsequent studies using simultaneous MR/FDG-fPET (20) and BOLD-fMRI/FDG-fPET (21) have extended these findings to demonstrate simultaneous BOLD and FDG activity in the visual and motor cortices during alternate visual stimulation (eyes open versus closed) and finger tapping tasks. Interestingly, Hahn et al, (21) found that endogenously-driven stimulation (i.e., eyes open rest and non-paced finger tapping without external behavioural cues) produced task-related CMR GLC and BOLD activity that were independent of each other; in other words, the task-specific changes were not correlated across the two imaging modalities.…”

From simultaneous to synergistic MR‐PET brain imaging: A review of hybrid MR‐PET imaging methodologies

“…Even with the slow continuous infusion technique, the difference in temporal resolution between FDG-PET and BOLD-fMRI signals represents a significant challenge for designing brain functional experiments that optimise the use of both modalities. One recent study (Hahn et al, 2017) indicate significant neural activity can be simultaneously identified in both imaging modalities (see Figure 2), with a temporal resolution of around 1 min for fPET and 2 s for fMRI .…”

Analysis of continuous infusion functional PET (fPET) in the human brain

“…The aim of the fPET approach is to maintain a continuous plasma supply of FDG to provide improved sensitivity of brain-state changes, and better temporal dynamics than bolus PET to track dynamic change of glucose uptake over time. Several studies have demonstrated that fPET can isolate task related changes in glucose uptake (Hahn et al 2016;Hahn et al 2018;Rischka et al 2018;Villien et al 2014;Jamadar, Ward, Carey, et al 2019).…”