Learning induces coordinated neuronal plasticity of metabolic demands and functional brain networks

Abstract

The neurobiological basis of learning is reflected in adaptations of brain structure, network organization and energy metabolism. However, it is still unknown how different neuroplastic mechanisms act together and if cognitive advancements relate to general or task-specific changes. Therefore, we tested how hierarchical network interactions contribute to improvements in the performance of a visuo-spatial processing task by employing simultaneous PET/MR neuroimaging before and after a 4-week learning period. We combined functional PET and metabolic connectivity mapping (MCM) to infer directional interactions across brain regions. Learning altered the top-down regulation of the salience network onto the occipital cortex, with increases in MCM at resting-state and decreases during task execution. Accordingly, a higher divergence between resting-state and task-specific effects was associated with better cognitive performance, indicating that these adaptations are complementary and both required for successful visuo-spatial skill learning. Simulations further showed that changes at resting-state were dependent on glucose metabolism, whereas those during task performance were driven by functional connectivity between salience and visual networks. Referring to previous work, we suggest that learning establishes a metabolically expensive skill engram at rest, whose retrieval serves for efficient task execution by minimizing prediction errors between neuronal representations of brain regions on different hierarchical levels.

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

“…Simultaneous fPET/fMRI data were acquired from 50 healthy participants during the performance of the video game Tetris®, a challenging cognitive task requiring rapid visuo-spatial processing and motor coordination (14, 19). From this dataset (DS1) we evaluated the overlap of negative task responses in the cerebral metabolic rate of glucose (CMRGlu) and the BOLD signal specifically in the pmDMN.…”

“…Reasons for drop out were failure of arterial blood sampling (n=1) and technical issues during the scan (n=2). In part these subjects also participated in previous studies (14, 19, 47). All subjects completed an initial screening to ensure general health through a routine medical examination (blood tests, electrocardiography, neurological testing, structural clinical interview for DSM-IV).…”

“…To address these open questions, we employed functional PET/MR imaging with [ 18 F]FDG during rest and performance of a visuo-spatial task requiring a broad range of cognitive functions primarily supported by the dorsal attention network (14, 19). The results were then compared to previously published data from tasks of varying complexity (working memory, eyes opening and finger tapping), primarily involving different brain networks (FPN, visual and motor, respectively).…”

Competitive plasticity to reduce the energetic costs of learning

“…In mammals there is physiological evidence that energy availability gates long lasting forms of plasticity (Potter et al, 2010). Furthermore, in humans there is behavioral evidence for a correlation between metabolism and memory (Smith et al, 2011;Klug et al, 2022).Given this evidence, we hypothesize that biological neural plasticity is designed to be energy efficient and that including energy constraints could lead to computational learning rules more closely resembling biology, and a better understanding of observed synaptic plasticity rules. As precise metabolic 1 .…”

“…In mammals there is physiological evidence that energy availability gates long lasting forms of plasticity (Potter et al, 2010). Furthermore, in humans there is behavioral evidence for a correlation between metabolism and memory (Smith et al, 2011;Klug et al, 2022).…”