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Developmental emergence of sleep rhythms enables long-term memory in Drosophila

In adulthood, sleep-wake rhythms are one of the most prominent behaviors under circadian control. However, during early life, sleep is spread across the 24-hour day. The mechanism through which sleep rhythms emerge, and consequent advantage conferred to a juvenile animal, is unknown. In the second-i...

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Autores principales: Poe, Amy R., Zhu, Lucy, Szuperak, Milan, McClanahan, Patrick D., Anafi, Ron C., Scholl, Benjamin, Thum, Andreas S., Cavanaugh, Daniel J., Kayser, Matthew S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491288/
https://www.ncbi.nlm.nih.gov/pubmed/37683005
http://dx.doi.org/10.1126/sciadv.adh2301
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author Poe, Amy R.
Zhu, Lucy
Szuperak, Milan
McClanahan, Patrick D.
Anafi, Ron C.
Scholl, Benjamin
Thum, Andreas S.
Cavanaugh, Daniel J.
Kayser, Matthew S.
author_facet Poe, Amy R.
Zhu, Lucy
Szuperak, Milan
McClanahan, Patrick D.
Anafi, Ron C.
Scholl, Benjamin
Thum, Andreas S.
Cavanaugh, Daniel J.
Kayser, Matthew S.
author_sort Poe, Amy R.
collection PubMed
description In adulthood, sleep-wake rhythms are one of the most prominent behaviors under circadian control. However, during early life, sleep is spread across the 24-hour day. The mechanism through which sleep rhythms emerge, and consequent advantage conferred to a juvenile animal, is unknown. In the second-instar Drosophila larvae (L2), like in human infants, sleep is not under circadian control. We identify the precise developmental time point when the clock begins to regulate sleep in Drosophila, leading to emergence of sleep rhythms in early third-instars (L3). At this stage, a cellular connection forms between DN1a clock neurons and arousal-promoting Dh44 neurons, bringing arousal under clock control to drive emergence of circadian sleep. Last, we demonstrate that L3 but not L2 larvae exhibit long-term memory (LTM) of aversive cues and that this LTM depends upon deep sleep generated once sleep rhythms begin. We propose that the developmental emergence of circadian sleep enables more complex cognitive processes, including the onset of enduring memories.
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spelling pubmed-104912882023-09-09 Developmental emergence of sleep rhythms enables long-term memory in Drosophila Poe, Amy R. Zhu, Lucy Szuperak, Milan McClanahan, Patrick D. Anafi, Ron C. Scholl, Benjamin Thum, Andreas S. Cavanaugh, Daniel J. Kayser, Matthew S. Sci Adv Neuroscience In adulthood, sleep-wake rhythms are one of the most prominent behaviors under circadian control. However, during early life, sleep is spread across the 24-hour day. The mechanism through which sleep rhythms emerge, and consequent advantage conferred to a juvenile animal, is unknown. In the second-instar Drosophila larvae (L2), like in human infants, sleep is not under circadian control. We identify the precise developmental time point when the clock begins to regulate sleep in Drosophila, leading to emergence of sleep rhythms in early third-instars (L3). At this stage, a cellular connection forms between DN1a clock neurons and arousal-promoting Dh44 neurons, bringing arousal under clock control to drive emergence of circadian sleep. Last, we demonstrate that L3 but not L2 larvae exhibit long-term memory (LTM) of aversive cues and that this LTM depends upon deep sleep generated once sleep rhythms begin. We propose that the developmental emergence of circadian sleep enables more complex cognitive processes, including the onset of enduring memories. American Association for the Advancement of Science 2023-09-08 /pmc/articles/PMC10491288/ /pubmed/37683005 http://dx.doi.org/10.1126/sciadv.adh2301 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Neuroscience
Poe, Amy R.
Zhu, Lucy
Szuperak, Milan
McClanahan, Patrick D.
Anafi, Ron C.
Scholl, Benjamin
Thum, Andreas S.
Cavanaugh, Daniel J.
Kayser, Matthew S.
Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title_full Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title_fullStr Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title_full_unstemmed Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title_short Developmental emergence of sleep rhythms enables long-term memory in Drosophila
title_sort developmental emergence of sleep rhythms enables long-term memory in drosophila
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491288/
https://www.ncbi.nlm.nih.gov/pubmed/37683005
http://dx.doi.org/10.1126/sciadv.adh2301
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