Ageing is associated with a high glucose cost in hub regions of the metabolic network

A organisational principle of the human brain is a trade-off between minimising energy cost and maximising communication efficiency. Although hub regions are energetically costly, they are especially important for information transfer across the brain because of their long-range connection. Here we investigate the cost of metabolic networks using rates of glucose in hubs relative to their role in information transfer across the brain in 40 younger (mean age 27.9 years; range 20-42) and 46 older (mean 75.8; 60-89) adults. Ageing was associated with lower global integration of metabolic hub regions, indicating disrupted information transfer across the metabolic network in older adults. For younger adults, the frontal hubs were more central, efficient and connected in facilitating global communication across the brain. Greater local efficiency of hubs in younger adults also minimised the cost of maintaining network communication via fewer paths to locally connected nodes. Older adults had a smaller energy budget in comparison to younger adults, and older adults used a higher proportion of energy to support mostly posterior hub regions. The lower efficiency and higher cost of the metabolic network in older adults was associated with worse cognitive performance. We conclude that ageing is associated with an altered metabolic network topology and a high glucose cost in hub regions. Our results highlight the fundamental role that metabolism plays in supporting information transfer in the brain and the unique insights that metabolic connectivity provides into the ageing brain.