Sleep restores place learning to the adenylyl cyclase mutant <i>rutabaga</i>

Dissel, Stephane; Morgan, Ellen; Duong, Vincent; Chan, Dorothy N.S.; Swinderen, Bruno van; Shaw, Paul J.; Zars, Troy

doi:10.1080/01677063.2020.1720674

Cited by 5 publications

(9 citation statements)

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“…Sleep deprivation impaired learning; conversely, enhancing sleep reversed learning impairments associated with rut mutants and aging. These data build on previous results that suggested a surprising restorative depth to the relationship between sleep and plasticity 19,34 , and extend them to a novel spatial learning task. As discussed below, our results are consistent with findings in rodent spatial learning and human episodic memory research, reinforcing the parallels between spatial learning in animal models and human declarative memories 15,16 .…”

Section: Discussionsupporting

confidence: 86%

“…Moreover, enhancing sleep pharmacologically by feeding rut mutant flies Gaboxadol for two days restored spatial learning. These results are consistent with previous work showing that Gaboxadol enhanced sleep restored learning to rut mutants in other learning assays: Aversive Phototaxis Suppression, courtship conditioning, and place learning 19,34 .…”

Section: Enhancing Sleep Restores Spatial Learning To Rut Mutantssupporting

confidence: 93%

“…Consequently, we hypothesized that rut mutants would also be impaired in spatial learning. As previously described, rut 2080 mutants, which are in a Cs background, sleep the same as Cs controls 19,34 (Figure 4A). Despite having similar sleep profiles, rut 2080 mutants displayed severe behavioral impairment ( Figure 4B).…”

Section: Enhancing Sleep Restores Learning To Rutabaga Mutant Fliessupporting

confidence: 73%

“…Enhancing sleep pharmacologically, by administering the GABA-A agonist Gaboxadol, can restore learning in rut 2080 mutants when evaluated using a variety of learning assays including 1) Aversive Phototaxis Suppression assay, 2) courtship conditioning, and 3) place learning 19,34 To determine whether enhanced sleep could also restore space learning to rut 2080 mutants, we increased sleep in rut 2080 mutants for two days by feeding them 0.1µg/mL Gaboxadol 19,36 . As shown previously, Gaboxadol-fed rut 2080 males show a robust increase in total sleep time which is accompanied by a significant increase in the average duration of sleep bouts during the day (a measure of sleep consolidation) ( Figure 4, D and E).…”

Section: Enhancing Sleep Restores Learning To Rutabaga Mutant Fliesmentioning

confidence: 99%

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A conserved role for sleep in supporting spatial learning inDrosophila

Melnattur

Kirszenblat

Morgan

et al. 2020

Preprint

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Sleep loss and aging impair hippocampus-dependent spatial learning in mammalian systems.Here we use the fly Drosophila melanogaster to investigate the relationship between sleep and spatial learning in healthy and impaired flies. The spatial learning assay is modeled after the Morris Water Maze. The assay uses a 'thermal maze' consisting of a 5X5 grid of Peltier plates maintained at 36-37C and a visual panorama. The first trial begins when a single tile that is associated with a specific visual cue is cooled to 25°C. For subsequent trials, the cold tile is heated, the visual panorama is rotated and the flies must find the new cold-tile by remembering its association with the visual cue. Significant learning was observed with two different wild-type strains -Cs and 2U, validating our design. Sleep deprivation prior to training impaired spatial learning. Learning was also impaired in the classic learning mutant rutabaga (rut); enhancing sleep restored learning to rut mutants. Further we found that flies exhibited dramatic age-dependent cognitive decline in spatial learning starting at 20-24 days of age.These impairments could be reversed by enhancing sleep. Finally, we find that spatial learning requires dopaminergic signaling and that enhancing dopaminergic signaling in aged flies restored learning. Our results are consistent with the impairments seen in rodents and humans.These results thus demonstrate a critical conserved role for sleep in supporting spatial learning, and suggest potential avenues for therapeutic intervention during aging. STATEMENT OF SIGNIFICANCEWe have studied the relationship between sleep and plasticity using a Drosophila learning assay modified after the Morris Water Maze. Using this assay, we find that sleep loss impairs spatial learning. As in mammals, flies exhibited age-dependent spatial learning impairments.Importantly, the age-dependent impairments were reversed by enhancing sleep. Interestingly, our results mirror studies on hippocampus dependent memories in rodents and humans. Thus, our data describe an evolutionarily conserved role for sleep in regulating spatial learning. They also support augmenting sleep as a therapeutic strategy to ameliorate learning impairments.

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Section: Discussionsupporting

confidence: 86%

Section: Enhancing Sleep Restores Spatial Learning To Rut Mutantssupporting

confidence: 93%

Section: Enhancing Sleep Restores Learning To Rutabaga Mutant Fliessupporting

confidence: 73%

Section: Enhancing Sleep Restores Learning To Rutabaga Mutant Fliesmentioning

confidence: 99%

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A conserved role for sleep in supporting spatial learning inDrosophila

Melnattur

Kirszenblat

Morgan

et al. 2020

Preprint

Self Cite

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“…In Drosophila , the definition of sleep is based on behavioral criteria: quiescence, increased arousal threshold, change in posture, and inactivity of at least 5 min ( Hendricks et al, 2000 ; Shaw et al, 2000 ). Previous work has phenomenally reflected on the literature related to sleep in Drosophila , its neural substrates, and novel approaches and research in the field ( Dubowy and Sehgal, 2017 ; Dissel, 2020 ; Dissel et al, 2020 ; Weiss and Donlea, 2021a ; Gilestro, 2021 ; Shafer and Keene, 2021 ) while the present work will aim to describe recent findings on the specific modulation of memory by sleep.…”

Section: Introductionmentioning

confidence: 99%

Sleep benefits different stages of memory in Drosophila

et al. 2023

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Understanding the physiological mechanisms that modulate memory acquisition and consolidation remains among the most ambitious questions in neuroscience. Massive efforts have been dedicated to deciphering how experience affects behavior, and how different physiological and sensory phenomena modulate memory. Our ability to encode, consolidate and retrieve memories depends on internal drives, and sleep stands out among the physiological processes that affect memory: one of the most relatable benefits of sleep is the aiding of memory that occurs in order to both prepare the brain to learn new information, and after a learning task, to consolidate those new memories. Drosophila lends itself to the study of the interactions between memory and sleep. The fruit fly provides incomparable genetic resources, a mapped connectome, and an existing framework of knowledge on the molecular, cellular, and circuit mechanisms of memory and sleep, making the fruit fly a remarkable model to decipher the sophisticated regulation of learning and memory by the quantity and quality of sleep. Research in Drosophila has stablished not only that sleep facilitates learning in wild-type and memory-impaired animals, but that sleep deprivation interferes with the acquisition of new memories. In addition, it is well-accepted that sleep is paramount in memory consolidation processes. Finally, studies in Drosophila have shown that that learning itself can promote sleep drive. Nevertheless, the molecular and network mechanisms underlying this intertwined relationship are still evasive. Recent remarkable work has shed light on the neural substrates that mediate sleep-dependent memory consolidation. In a similar way, the mechanistic insights of the neural switch control between sleep-dependent and sleep-independent consolidation strategies were recently described. This review will discuss the regulation of memory by sleep in Drosophila, focusing on the most recent advances in the field and pointing out questions awaiting to be investigated.

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A place learning assay for tethered walking Drosophila

Flores-Valle

Seelig

2022

Journal of Neuroscience Methods

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Sleep restores place learning to the adenylyl cyclase mutant rutabaga

Cited by 5 publications

References 47 publications

A conserved role for sleep in supporting spatial learning inDrosophila

A conserved role for sleep in supporting spatial learning inDrosophila

Sleep benefits different stages of memory in Drosophila

A place learning assay for tethered walking Drosophila

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