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Synchronous circadian voltage rhythms with asynchronous calcium rhythms in the suprachiasmatic nucleus

Significance The mammalian master circadian clock, the suprachiasmatic nucleus (SCN), contains a network composed of various neuron types. The SCN network plays critical roles in expressing robust circadian rhythms in physiology and behavior, such as sleep–wake cycles. The molecular clock in individual SCN neurons controls membrane excitability, and sends output signals to various organs. However, how the SCN neurons transmit output signals remains unknown. Using a genetically encoded voltage sensor, we directly measured the circadian rhythms of membrane voltage in the SCN network. Remarkably, the circadian voltage rhythms are synchronous across the entire SCN network, whereas simultaneously recorded Ca2+ rhythms are asynchronous in the dorsal and ventral SCN regions. These results indicate that the SCN network produces coherent output signals. The suprachiasmatic nucleus (SCN), the master circadian clock, contains a network composed of multiple types of neurons which are thought to form a hierarchical and multioscillator system. The molecular clock machinery in SCN neurons drives membrane excitability and sends time cue signals to various brain regions and peripheral organs. However, how and at what time of the day these neurons transmit output signals remain largely unknown. Here, we successfully visualized circadian voltage rhythms optically for many days using a genetically encoded voltage sensor, ArcLightD. Unexpectedly, the voltage rhythms are synchronized across the entire SCN network of cultured slices, whereas simultaneously recorded Ca2+ rhythms are topologically specific to the dorsal and ventral regions. We further found that the temporal order of these two rhythms is cell-type specific: The Ca2+ rhythms phase-lead the voltage rhythms in AVP neurons but Ca2+ and voltage rhythms are nearly in phase in VIP neurons. We confirmed that circadian firing rhythms are also synchronous and are coupled with the voltage rhythms. These results indicate that SCN networks with asynchronous Ca2+ rhythms produce coherent voltage rhythms.