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Significance Structural and functional deterioration of neurons underlie the progressive decline in cognitive and behavioral functions associated with aging. In this study, we found that progressive fragmentation of mitochondria is a hallmark of neuronal aging inCaenorhabditis elegans . Progression of mitochondrial fragmentation is influenced by lifespan and is specifically regulated by neural activity. Loss of sensory-evoked activity worsened age-dependent mitochondrial fragmentation, whereas increased sensory-evoked activity improved it. We showed that sensory-evoked activity maintained mitochondrial morphology by inhibiting the mitochondrial fission protein, dynamin-related protein 1 through phosphorylation at a conserved amino acid residue. These findings contribute to mechanistic understanding of neuronal aging and identify sensory-evoked activity as a critical regulator of neuronal mitochondria during aging.

Neural activity and CaMKII protect mitochondria from fragmentation in aging Caenorhabditis elegans neurons