Developmental emergence of sleep rhythms enables long-term memory in
            <i>Drosophila</i>

Poe, Amy R.; Zhu, Lucy; Szuperak, Milan; McClanahan, Patrick D.; Anafi, Ron C.; Scholl, Benjamin; Thum, Andreas S.; Cavanaugh, Daniel J.; Kayser, Matthew S.

doi:10.1126/sciadv.adh2301

Cited by 7 publications

(33 citation statements)

References 76 publications

(104 reference statements)

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“…We observed no differences in feeding rate across the day in tim mutants indicating that daily changes in feeding rate require a functioning molecular clock at the L3 stage (Figure 1C). These findings underscore the tight relationship between sleep and feeding across development as diurnal differences in sleep emerge concurrently at the L3 stage 21 .…”

Section: Resultsmentioning

confidence: 62%

“…Our data indicate that the emergence of diurnal behavioral differences such as sleep-wake is driven by developmental changes in energetic capacity and suggest that Dh44 neurons may be necessary for sensing of larval nutritional environments. Our data demonstrate that larvae exhibit both sleep-wake and feeding rhythms at the L3 stage, but not earlier 21 . This raises the obvious question of whether sleep and feeding are opposite sides of the same coin.…”

Section: Dh44 Neurons Require Glucose Metabolic Genes To Regulate Sle...mentioning

confidence: 59%

“…We previously determined that release of CCHamide-1 ( CCHa1 ) from DN1as to CCHa1mide-1 receptor ( CCHa1-R ) on Dh44 neurons is necessary for sleep-wake rhythms in L3 21 . Although DN1as and Dh44 are not yet connected in L2, we next asked whether Dh44 neurons in L2 are competent to receive the CCHa1 signal.…”

Section: Resultsmentioning

confidence: 99%

“…All live imaging experiments (P2X2 and CCHa1 bath application) were performed as described previously 21 . Briefly, brains were dissected in artificial hemolymph (AHL) buffer consisting of (in mM): 108 NaCl, 5 KCl, 2 CaCl2, 8.2 MgCl2, 4 NaHCO3, 1 NaH2PO4-H20, 5 Trehalose, 10 Sucrose, 5 HEPES, pH=7.5.…”

Section: P2x2 Activation and Gcamp Imagingmentioning

confidence: 99%

“…DN1a clock neurons anatomically and functionally connect to Dh44 arousal output neurons to drive the consolidation of sleep in L3. Development of this circuit promotes deeper sleep in L3 resulting in the emergence of long-term memory (LTM) capabilities at the L3 stage but not before 21 .…”

Section: Introductionmentioning

confidence: 99%

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Energetic Demands Regulate Sleep-Wake Rhythm Circuit Development

Poe,

Zhu,

Tang

et al. 2023

Preprint

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Sleep and feeding patterns lack a clear daily rhythm during early life. As diurnal animals mature, feeding is consolidated to the day and sleep to the night. Circadian sleep patterns begin with formation of a circuit connecting the central clock to arousal output neurons; emergence of circadian sleep also enables long-term memory (LTM). However, the cues that trigger the development of this clock-arousal circuit are unknown. Here, we identify a role for nutritional status in driving sleep-wake rhythm development in Drosophila larvae. We find that in the 2nd instar (L2) period, sleep and feeding are spread across the day; these behaviors become organized into daily patterns by L3. Forcing mature (L3) animals to adopt immature (L2) feeding strategies disrupts sleep-wake rhythms and the ability to exhibit LTM. In addition, the development of the clock (DN1a)-arousal (Dh44) circuit itself is influenced by the larval nutritional environment. Finally, we demonstrate that larval arousal Dh44 neurons act through glucose metabolic genes to drive onset of daily sleep-wake rhythms. Together, our data suggest that changes to energetic demands in developing organisms triggers the formation of sleep-circadian circuits and behaviors.

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Section: Resultsmentioning

confidence: 62%

Section: Dh44 Neurons Require Glucose Metabolic Genes To Regulate Sle...mentioning

confidence: 59%

Section: Resultsmentioning

confidence: 99%

Section: P2x2 Activation and Gcamp Imagingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Energetic Demands Regulate Sleep-Wake Rhythm Circuit Development

Poe,

Zhu,

Tang

et al. 2023

Preprint

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Developing forebrain synapses are uniquely vulnerable to sleep loss

Gay,

Chartampila,

Lord

et al. 2023

Preprint

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Sleep supports lifelong brain health and cognition. Sleep loss in early life can drive lasting changes in adult behavior, indicating sleep plays a distinct but poorly understood role in brain development. We systematically examined the homeostatic adaptations and synaptic consequences of acute sleep deprivation (SD) in developing and adult mice. Developing mice lack robust homeostatic adaptations to SD, exacerbating cognitive deficits. Synapse proteome and phosphoproteome analysis revealed profound vulnerability to SD in developing mice, including immediate impacts on synaptogenesis and key aspects of brain development. With maturation, a unified biochemical effect of sleep on synapses emerges, together with robust homeostatic adaptations and resilience to SD. Our findings show sleep plays a distinct role in early life supporting synapse development, transitioning to homeostatic functions with maturation.One-Sentence SummaryEffects of sleep loss across life stages indicate sleep plays a distinct role in early life supporting synapse maturation.

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Neuropeptide-dependent spike time precision and plasticity in circadian output neurons

Chong,

Kumar,

Nguyen

et al. 2024

Preprint

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Circadian rhythms influence various physiological and behavioral processes such as sleep-wake cycles, hormone secretion, and metabolism. Circadian output neurons are a group of neurons that receive input from the central circadian clock located in the suprachiasmatic nucleus of the mammalian brain and transmit timing information to different regions of the brain and body, coordinating the circadian rhythms of various physiological processes. In Drosophila, an important set of circadian output neurons are called pars intercerebralis (PI) neurons, which receive input from specific clock neurons called DN1. These neurons can further be subdivided into functionally and anatomically distinctive anterior (DN1a) and posterior (DN1p) clusters. The neuropeptide diuretic hormones 31 (Dh31) and 44 (Dh44) are the insect neuropeptides known to activate PI neurons to control activity rhythms. However, the neurophysiological basis of how Dh31 and Dh44 affect circadian clock neural coding mechanisms underlying sleep in Drosophila is not well understood. Here, we identify Dh31/Dh44-dependent spike time precision and plasticity in PI neurons. We find that the application of synthesized Dh31 and Dh44 affects membrane potential dynamics of PI neurons in the precise timing of the neuronal firing through their synergistic interaction, possibly mediated by calcium-activated potassium channel conductance. Further, we characterize that Dh31/Dh44 enhances postsynaptic potentials in PI neurons. Together, these results suggest multiplexed neuropeptide-dependent spike time precision and plasticity as circadian clock neural coding mechanisms underlying sleep in Drosophila.

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

Cited by 7 publications

References 76 publications

Energetic Demands Regulate Sleep-Wake Rhythm Circuit Development

Energetic Demands Regulate Sleep-Wake Rhythm Circuit Development

Developing forebrain synapses are uniquely vulnerable to sleep loss

Neuropeptide-dependent spike time precision and plasticity in circadian output neurons

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