Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila

Dağ, Uğur; Lei, Zhengchang; Le, Jasmine Quynh; Wong, Allan; Bushey, Daniel; Keleman, Krystyna

doi:10.7554/elife.42786

Cited by 64 publications

(106 citation statements)

References 62 publications

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“…The MB and central complex (CX), both highly structured centers, are known to carry out sophisticated computations. Communication from the MB to the CX is likely to be important for conveying information about learned associations of sensory cues and external rewards or punishment (Aso et al, 2014a(Aso et al, , 2014bOwald et al, 2015), novelty (Hattori et al, 2017) and sleep need (Sitaraman et al, 2015a;Dag et al 2019), which, in turn, are expected to influence navigation, sleep and other activities governed by the CX. We describe here the complete network of strong (based on synapse number) neural pathways connecting the MB to the CX (to be discussed further in a companion manuscript on the connectome of the CX).…”

Section: Neuronal Pathways Connecting the Mb And The CXmentioning

confidence: 99%

“…DANs are divided into two major groups, PPL1 and PAM, that preferentially encode punishment and reward, respectively (reviewed in Modi et al, 2020). But there is growing evidence that DANs provide a wider range of information to the MB about novelty, locomotion, sleep state, reward or punishment omission, and safety (Aso and Rubin, 2016;Cohn et al, 2015;Dag et al, 2019;Felsenberg et al, 2018Felsenberg et al, , 2017Gerber et al, 2014;Handler et al, 2019;Hattori et al, 2017;Jacob and Waddell, 2020;Sitaraman et al, 2015b;Tanimoto et al, 2004).…”

Section: Structure Of Dan Connectivitymentioning

confidence: 99%

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The connectome of the adultDrosophilamushroom body: implications for function

Lindsey

Marin

et al. 2020

Preprint

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Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

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Section: Neuronal Pathways Connecting the Mb And The CXmentioning

confidence: 99%

Section: Structure Of Dan Connectivitymentioning

confidence: 99%

The connectome of the adultDrosophilamushroom body: implications for function

Lindsey

Marin

et al. 2020

Preprint

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“…Further, these place cell sequences can be reactivated by cueing in sleep 103,[106][107][108] . Although replay like phenomena have not been observed in flies, cued reactivation during sleep improved recall in bees 109 , and reactivation during sleep of dopaminergic neurons involved in memory acquisition was shown to facilitate consolidation of courtship memory in flies 110 , suggesting that such replay-like processes might be detected in Drosophila too.…”

Section: Discussionmentioning

confidence: 98%

A conserved role for sleep in supporting spatial learning in Drosophila

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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“…A number of neuronal populations that regulate sleep have been identified ( Artiushin and Sehgal, 2017 ; Tomita et al, 2017 ), and among them are two distinct populations in the central complex: EB R5 neurons and the dorsal FB ( Donlea et al, 2014 ; Donlea et al, 2011 ; Liu et al, 2012 ; Liu et al, 2016 ; Pimentel et al, 2016 ; Ueno et al, 2012 ). In addition, Ueno et al, 2012 showed that activation of dopaminergic PPM3 neurons projecting to the ventral FB leads to sleep suppression, while Dag et al, 2019 showed that ventral FB neurons can be sleep-promoting. Our results show that the PB region in the central complex is also involved in sleep regulation.…”

Section: Discussionmentioning

confidence: 99%

Modulation of sleep-courtship balance by nutritional status in Drosophila

Duhart

Baccini

Zhang

et al. 2020

eLife

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Sleep is essential but incompatible with other behaviors, and thus sleep drive competes with other motivations. We previously showed Drosophila males balance sleep and courtship via octopaminergic neurons that act upstream of courtship-regulating P1 neurons (Machado et al., 2017). Here we show nutrition modulates the sleep-courtship balance and identify sleep-regulatory neurons downstream of P1 neurons. Yeast-deprived males exhibited attenuated female-induced nighttime sleep loss yet normal daytime courtship, which suggests male flies consider nutritional status in deciding whether the potential benefit of pursuing female partners outweighs the cost of losing sleep. Trans-synaptic tracing and calcium imaging identified dopaminergic neurons projecting to the protocerebral bridge (DA-PB) as postsynaptic partners of P1 neurons. Activation of DA-PB neurons led to reduced sleep in normally fed but not yeast-deprived males. Additional PB-projecting neurons regulated male sleep, suggesting several groups of PB-projecting neurons act downstream of P1 neurons to mediate nutritional modulation of the sleep-courtship balance.

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Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila

Cited by 64 publications

References 62 publications

The connectome of the adultDrosophilamushroom body: implications for function

The connectome of the adultDrosophilamushroom body: implications for function

A conserved role for sleep in supporting spatial learning in Drosophila

Modulation of sleep-courtship balance by nutritional status in Drosophila

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