Dissociations between glucose metabolism and blood oxygenation in the human default mode network revealed by simultaneous PET-fMRI

Abstract

The finding of reduced functional MRI (fMRI) activity in the default mode network (DMN) during externally focused cognitive control has been highly influential to our understanding of human brain function. However, these negative fMRI responses, measured as relative decreases in the blood-oxygenation-level–dependent (BOLD) response between rest and task, have also prompted major questions of interpretation. Using hybrid functional positron emission tomography (PET)-MRI, this study shows that task-positive and -negative BOLD responses do not reflect antagonistic patterns of synaptic metabolism. Task-positive BOLD responses in attention and control networks were accompanied by concomitant increases in glucose metabolism during cognitive control, but metabolism in widespread DMN remained high during rest and task despite negative BOLD responses. Dissociations between glucose metabolism and the BOLD response specific to the DMN reveal functional heterogeneity in this network and demonstrate that negative BOLD responses during cognitive control should not be interpreted to reflect relative increases in metabolic activity during rest. Rather, neurovascular coupling underlying BOLD response patterns during rest and task in DMN appears fundamentally different from BOLD responses in other association networks during cognitive control.

Metabolic demands of the posteromedial default mode network are shaped by dorsal attention and frontoparietal control networks

“…Here a negative BOLD response was accompanied by increased glucose metabolism in the anterior/dorsal part of the PCC (Fig. 1b; (16)).…”

“…Next, we tested the hypothesis that negative responses in the DMN are mirrored by the corresponding positive task changes that are specific to other cortical networks. To provide a comprehensive overview of changes across different tasks we also included results from a working memory task (DS2) (16) as well as eyes opened vs. eyes closed conditions and right finger tapping (DS3) (18). For the Tetris® and working memory tasks, overlapping increases in CMRGlu and BOLD signal changes were computed in the same way as above, i.e.…”

“…These only include group-averaged results with contrasts and statistical maps as published previously. Dataset 2 (DS2) consists of fPET/fMRI data from n=23 healthy subjects (mean age ± sd = 25.2 ± 4.0 years, 13 female) acquired during the performance of a working memory manipulation task, which required active transformation of stimuli in working memory (16). Group-level maps of significant increases and decreases in [ 18 F]FDG glucose metabolism and the BOLD signal during task execution as compared to baseline were used (p<0.05 TFCE corrected).…”

Estrogen, Cognitive Performance, and Functional Imaging Studies: What Are We Missing About Neuroprotection?

“…In either task-based fMRI or rs-fMRI, the precise physiological mechanisms underlying the temporal synchronous signal fluctuation between cortical areas are not yet clearly defined. The coupling or uncoupling of neuronal activity and vascular reactivity is an active field of study (Rossetti et al, 2021 ; Stiernman et al, 2021 ). The RSN is elicited by a wide variety of sensory, motor, and cognitive tasks, representing 20% of the overall energy consumed by a person (Raichle, 2010 ).…”

Secretin modulates appetite via brown adipose tissue - brain axis

“…Brain BOLD activity is tightly linked with regional brain glucose metabolism at both resting state (Tomasi et al, 2013; Aiello et al, 2015) and during tasks, yet with markedly different patterns of association (Stiernman et al, 2021). More specifically, while a largely positive regional association was found in resting states, neurometabolic coupling during cognitive tasks suggests dissociations between the two dimensions of measures.…”