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Enhanced oxidative capacity of ground squirrel brain mitochondria during hibernation

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AJP Regulatory Integrative and Comparative Physiology

Published online on

Abstract

During hibernation, thirteen-lined ground squirrels (Ictidomys tridecemlineatus) regularly cycle between bouts of torpor and interbout arousal (IBA).  Most of the brain is electrically quiescent during torpor, but regains activity quickly upon arousal to IBA resulting in extreme oscillations in energy demand during hibernation.  We predicted increased functional capacity of brain mitochondria during hibernation compared to spring to accommodate the variable energy demands of hibernation.  To address this hypothesis, we examined mitochondrial bioenergetics in the ground squirrel brain across three time points: spring (SP), torpor (TOR), and IBA.  Respiration rates of isolated brain mitochondria through complex I of the electron transport chain were over twofold higher in TOR and IBA than in SP (P < 0.05).  We also found a 10% increase in membrane potential between hibernation and spring (P < 0.05), and that proton leak was lower in TOR and IBA than in SP. Finally, there was a 30% increase in calcium loading in SP brain mitochondria compared to TOR and IBA (P < 0.01).  To analyze brain mitochondrial abundance between spring and hibernation, we measured the ratio of copy number in a mitochondrial gene (ND1) versus a nuclear gene (B2M) in frozen cerebral cortex samples.  No significant differences were observed in DNA copies between SP and IBA.  These data show that brain mitochondrial bioenergetics are not static across the year, and suggest that brain mitochondria function more effectively during the hibernation season, allowing for rapid production of energy in order to meet demand when extreme physiological changes are occurring.