Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations

William D. Todd, Anne Venner, Christelle Anaclet, Rebecca Y. Broadhurst, Roberto Luca, Sathyajit S. Bandaru, Lindsay Issokson, Lauren M. Hablitz, Olga Cravetchi, Elda Arrigoni, John N. Campbell, Charles N. Allen, David P. Olson and Patrick M. Fuller ()
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William D. Todd: University of Wyoming
Anne Venner: Division of Sleep Medicine, Harvard Medical School
Christelle Anaclet: University of Massachusetts Medical School
Rebecca Y. Broadhurst: Division of Sleep Medicine, Harvard Medical School
Roberto Luca: Division of Sleep Medicine, Harvard Medical School
Sathyajit S. Bandaru: Division of Sleep Medicine, Harvard Medical School
Lindsay Issokson: Division of Sleep Medicine, Harvard Medical School
Lauren M. Hablitz: Oregon Health & Science University
Olga Cravetchi: Oregon Health & Science University
Elda Arrigoni: Division of Sleep Medicine, Harvard Medical School
John N. Campbell: University of Virginia
Charles N. Allen: Oregon Health & Science University
David P. Olson: University of Michigan
Patrick M. Fuller: Division of Sleep Medicine, Harvard Medical School

Nature Communications, 2020, vol. 11, issue 1, 1-20

Abstract: Abstract The hypothalamic suprachiasmatic (SCN) clock contains several neurochemically defined cell groups that contribute to the genesis of circadian rhythms. Using cell-specific and genetically targeted approaches we have confirmed an indispensable role for vasoactive intestinal polypeptide-expressing SCN (SCNVIP) neurons, including their molecular clock, in generating the mammalian locomotor activity (LMA) circadian rhythm. Optogenetic-assisted circuit mapping revealed functional, di-synaptic connectivity between SCNVIP neurons and dorsomedial hypothalamic neurons, providing a circuit substrate by which SCNVIP neurons may regulate LMA rhythms. In vivo photometry revealed that while SCNVIP neurons are acutely responsive to light, their activity is otherwise behavioral state invariant. Single-nuclei RNA-sequencing revealed that SCNVIP neurons comprise two transcriptionally distinct subtypes, including putative pacemaker and non-pacemaker populations. Altogether, our work establishes necessity of SCNVIP neurons for the LMA circadian rhythm, elucidates organization of circadian outflow from and modulatory input to SCNVIP cells, and demonstrates a subpopulation-level molecular heterogeneity that suggests distinct functions for specific SCNVIP subtypes.

Date: 2020
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DOI: 10.1038/s41467-020-17197-2

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