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Using a ratiometric pH probe insensitive to superoxide, we show that flashes reflect matrix alkalinization transients of \u223c0.4 pH units that persist in cells permeabilized in ion\u2010free solutions and can be evoked by imposed mitochondrial depolarization. Ablation of the pro\u2010fusion protein Optic atrophy 1 specifically abrogated pH flashes and reduced the propagation of matrix photoactivated GFP (paGFP). Ablation or invalidation of the pro\u2010fission Dynamin\u2010related protein 1 greatly enhanced flash propagation between contiguous mitochondria but marginally increased paGFP matrix diffusion, indicating that flashes propagate without matrix content exchange. The pH flashes were associated with synchronous depolarization and hyperpolarization events that promoted the membrane potential equilibration of juxtaposed mitochondria. 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