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Adaptation to photoperiod via dynamic neurotransmitter segregation.

Authors :
Maddaloni G
Chang YJ
Senft RA
Dymecki SM
Source :
Nature [Nature] 2024 Aug; Vol. 632 (8023), pp. 147-156. Date of Electronic Publication: 2024 Jul 17.
Publication Year :
2024

Abstract

Changes in the amount of daylight (photoperiod) alter physiology and behaviour <superscript>1,2</superscript> . Adaptive responses to seasonal photoperiods are vital to all organisms-dysregulation associates with disease, including affective disorders <superscript>3</superscript> and metabolic syndromes <superscript>4</superscript> . The circadian rhythm circuitry is implicated in such responses <superscript>5,6</superscript> , yet little is known about the precise cellular substrates that underlie phase synchronization to photoperiod change. Here we identify a brain circuit and system of axon branch-specific and reversible neurotransmitter deployment that are critical for behavioural and sleep adaptation to photoperiod. A type of neuron called mrEn1-Pet1 <superscript>7</superscript> in the mouse brainstem median raphe nucleus segregates serotonin from VGLUT3 (also known as SLC17A8, a proxy for glutamate) to different axonal branches that innervate specific brain regions involved in circadian rhythm and sleep-wake timing <superscript>8,9</superscript> . This branch-specific neurotransmitter deployment did not distinguish between daylight and dark phase; however, it reorganized with change in photoperiod. Axonal boutons, but not cell soma, changed neurochemical phenotype upon a shift away from equinox light/dark conditions, and these changes were reversed upon return to equinox conditions. When we genetically disabled Vglut3 in mrEn1-Pet1 neurons, sleep-wake periods, voluntary activity and clock gene expression did not synchronize to the new photoperiod or were delayed. Combining intersectional rabies virus tracing and projection-specific neuronal silencing, we delineated a preoptic area-to-mrEn1Pet1 connection that was responsible for decoding the photoperiodic inputs, driving the neurotransmitter reorganization and promoting behavioural synchronization. Our results reveal a brain circuit and periodic, branch-specific neurotransmitter deployment that regulates organismal adaptation to photoperiod change.<br /> (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)

Details

Language :
English
ISSN :
1476-4687
Volume :
632
Issue :
8023
Database :
MEDLINE
Journal :
Nature
Publication Type :
Academic Journal
Accession number :
39020173
Full Text :
https://doi.org/10.1038/s41586-024-07692-7