Abstract
Circadian rhythms in mammals are orchestrated by a central clock within the suprachiasmatic nuclei (SCN). Our understanding of the electrophysiological basis of SCN activity comes overwhelmingly from a small number of nocturnal rodent species, and the extent to which these are retained in day-active animals remains unclear. Here, we recorded the spontaneous and evoked electrical activity of single SCN neurons in the diurnal rodent Rhabdomys pumilio, and developed cutting-edge data assimilation and mathematical modeling approaches to uncover the underlying ionic mechanisms. As in nocturnal rodents, R. pumilio SCN neurons were more excited during daytime hours. By contrast, the evoked activity of R. pumilio neurons included a prominent suppressive response that is not present in the SCN of nocturnal rodents. Our modeling revealed and subsequent experiments confirmed transient subthreshold A-type potassium channels as the primary determinant of this response, and suggest a key role for this ionic mechanism in optimizing SCN function to accommodate R. pumilio's diurnal niche.
Highlights
The mammalian master circadian clock is localized within the hypothalamic suprachiasmatic nucleus (SCN), where nearly 20,000 neurons synchronize their daily activity with the light-dark cycle to orchestrate circadian rhythms in physiology and behavior (Reppert and Weaver, 2002)
We performed immunofluorescence labeling for nuclear DNA with DAPI, and vasoactive intestinal polypeptide (VIP), arginine vasopressin (AVP), and gastrinreleasing peptide (GRP) (Figure 1), which are the main neuropeptides expressed in the SCN, delineate its anatomical boundary, and are critical for circadian rhythm generation and coordination (Abrahamson and Moore, 2001; Ono et al, 2021)
The gross neuroanatomy of the R. pumilio SCN across the rostro-caudal axis is broadly similar to other rodent species (Smale and Boverhof, 1999; Abrahamson and Moore, 2001; Figure 1A)
Summary
The mammalian master circadian clock is localized within the hypothalamic suprachiasmatic nucleus (SCN), where nearly 20,000 neurons synchronize their daily activity with the light-dark cycle to orchestrate circadian rhythms in physiology and behavior (Reppert and Weaver, 2002). If not all, SCN neurons contain an internal molecular clock that operates on a transcription-translation feedback loop (TTFL) (Ko and Takahashi, 2006). Activity of the TTFL drives circadian rhythms in electrical activity, with SCN neurons notably more active during the day (up-state) than at night (down-state). This excitability landscape within the SCN is reinforced by the appropriate synaptic integration of extrinsic signals, which includes photic information from the retina and behavioral feedback reflecting arousal state (Belle and Diekman, 2018), endowing plasticity to the circadian timekeeping system (Michel and Meijer, 2020).
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