A Dynamic Deep Sleep Stage in<i>Drosophila</i>

Alphen, Bart van; Yap, Melvyn; Kirszenblat, Leonie; Kottler, Benjamin; Swinderen, Bruno van

doi:10.1523/jneurosci.0061-13.2013

Cited by 213 publications

(310 citation statements)

References 46 publications

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“…We call this state of reduced arousal threshold "sleep," applying the same criteria used in previous studies that found that tethered flies, when asleep, have reduced neuronal activity (6, 7). We also show, again consistent with previous results (6), that sleep as defined in the current study is homeostatically regulated by the duration of previous wake. Thus, we conclude that the state of quiescence as defined in our experimental setup qualifies as sleep and not simply as rest.…”

Section: Discussionsupporting

confidence: 93%

“…The study concluded that neural activity in the sleeping fly brain, or at least in a central region spanning the MBs, resembles that seen in mammals in several brainstem cell groups including noradrenergic neurons, whose firing strongly declines or stops completely during sleep (9). A more recent study in tethered flies able to walk on an airsuspended ball also found that periods of immobility >5 min are associated with increased arousal thresholds and with "flat" LFPs (6). LFPs, however, reflect the activity of thousands of cells (10), and the use of modified stereotrodes to resolve single-unit activity in flies is still in its infancy (11).…”

mentioning

confidence: 89%

“…Thus, in flies both sleep deprivation and a rich learning experience lead to a sleep rebound characterized by overall increased sleep time, increased arousal threshold, and longer sleep episodes (4-6). As in mammals, overall neuronal activity in flies is also high during wake and low during sleep (6)(7)(8). Specifically, a seminal study using local field potential (LFP) recordings from the Drosophila medial protocerebrum found high spike-like potentials that disappeared after the block of synaptic transmission in the mushroom bodies (MBs) (7).…”

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confidence: 99%

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Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Bushey

Tononi

Cirelli

2015

Proc. Natl. Acad. Sci. U.S.A.

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Sleep in Drosophila shares many features with mammalian sleep, but it remains unknown whether spontaneous and evoked activity of individual neurons change with the sleep/wake cycle in flies as they do in mammals. Here we used calcium imaging to assess how the Kenyon cells in the fly mushroom bodies change their activity and reactivity to stimuli during sleep, wake, and after short or long sleep deprivation. As before, sleep was defined as a period of immobility of >5 min associated with a reduced behavioral response to a stimulus. We found that calcium levels in Kenyon cells decline when flies fall asleep and increase when they wake up. Moreover, calcium transients in response to two different stimuli are larger in awake flies than in sleeping flies. The activity of Kenyon cells is also affected by sleep/wake history: in awake flies, more cells are spontaneously active and responding to stimuli if the last several hours (5-8 h) before imaging were spent awake rather than asleep. By contrast, long wake (≥29 h) reduces both baseline and evoked neural activity and decreases the ability of neurons to respond consistently to the same repeated stimulus. The latter finding may underlie some of the negative effects of sleep deprivation on cognitive performance and is consistent with the occurrence of local sleep during wake as described in behaving rats. Thus, calcium imaging uncovers new similarities between fly and mammalian sleep: fly neurons are more active and reactive in wake than in sleep, and their activity tracks sleep/wake history.T he fundamental features that characterize mammalian sleep also define Drosophila melanogaster sleep (1-3). Most crucially, in both flies and mammals, sleep is distinguished from simple rest (quiet wake) by an increased arousal threshold, i.e., a reduced ability to respond to external stimuli. Moreover, in flies and mammals sleep is controlled homeostatically by the duration as well by the intensity of prior wake, suggesting basic similarities in the mechanisms of sleep regulation across species. Thus, in flies both sleep deprivation and a rich learning experience lead to a sleep rebound characterized by overall increased sleep time, increased arousal threshold, and longer sleep episodes (4-6). As in mammals, overall neuronal activity in flies is also high during wake and low during sleep (6-8). Specifically, a seminal study using local field potential (LFP) recordings from the Drosophila medial protocerebrum found high spike-like potentials that disappeared after the block of synaptic transmission in the mushroom bodies (MBs) (7). This high spike activity was present when flies were moving or had been quiescent for only a few seconds, but disappeared with sleep (i.e., after periods of immobility >5 min), when the overall LFP power in all frequencies also decreased by ∼60% (7). The study concluded that neural activity in the sleeping fly brain, or at least in a central region spanning the MBs, resembles that seen in mammals in several brainstem cell groups including noradrenergic ne...

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Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 89%

mentioning

confidence: 99%

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Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Bushey

Tononi

Cirelli

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…In Drosophila, although the majority of sleep occurs during the night, flies sleep a substantial amount during the day with males exhibiting more daytime sleep than females. 19,21,[70][71][72] Similarly, forager bees sleep primarily during the night [73][74][75] but also nap during the day. 76 In all other castes, sleep is distributed with approximately equal sleep occurring during the day and the night.…”

Section: Discussionmentioning

confidence: 99%

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Krishnan

Gandour

Ramos

et al. 2016

Sleep

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Study Objectives: Insufficient sleep in individuals appears increasingly common due to the demands of modern work schedules and technology use. Consequently, there is a growing need to understand the interactions between sleep deprivation and memory. The current study determined the effects of acute sleep deprivation on short and long-term associative memory using the marine mollusk Aplysia californica, a relatively simple model system well known for studies of learning and memory. Methods: Aplysia were sleep deprived for 9 hours using context changes and tactile stimulation either prior to or after training for the operant learning paradigm, learning that food is inedible (LFI). The effects of sleep deprivation on short-term (STM) and long-term memory (LTM) were assessed. Results: Acute sleep deprivation prior to LFI training impaired the induction of STM and LTM with persistent effects lasting at least 24 h. Sleep deprivation immediately after training blocked the consolidation of LTM. However, sleep deprivation following the period of molecular consolidation did not affect memory recall. Memory impairments were independent of handling-induced stress, as daytime handled control animals demonstrated no memory deficits. Additional training immediately after sleep deprivation failed to rescue the induction of memory, but additional training alleviated the persistent impairment in memory induction when training occurred 24 h following sleep deprivation. Conclusions: Acute sleep deprivation inhibited the induction and consolidation, but not the recall of memory. These behavioral studies establish Aplysia as an effective model system for studying the interactions between sleep and memory formation.

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“…The MBs contain the neuronal population required to regulate normal sleep activity; overexpression of dFmr1 in the MBs reduced the prolonged sleep episodes of mutant flies (Bushey et al 2009). In another recent study, dFmr1 mutants showed a deeper night-like sleep phenotype during the day, which was regulated by two molecules, dFMRP and cAMP (van Alphen et al 2013). …”

Section: Dfmr1 Mutant Flies Have Abnormal Circadian Rhythmsmentioning

confidence: 92%

Learning and behavioral deficits associated with the absence of the fragile X mental retardation protein: what a fly and mouse model can teach us

2014

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The Fragile X syndrome (FXS) is the most frequent form of inherited mental disability and is considered a monogenic cause of autism spectrum disorder. FXS is caused by a triplet expansion that inhibits the expression of the FMR1 gene. The gene product, the Fragile X Mental Retardation Protein (FMRP), regulates mRNA metabolism in brain and nonneuronal cells. During brain development, FMRP controls the expression of key molecules involved in receptor signaling, cytoskeleton remodeling, protein synthesis and, ultimately, spine morphology. Symptoms associated with FXS include neurodevelopmental delay, cognitive impairment, anxiety, hyperactivity, and autistic-like behavior. Twenty years ago the first Fmr1 KO mouse to study FXS was generated, and several years later other key models including the mutant Drosophila melanogaster, dFmr1, have further helped the understanding of the cellular and molecular causes behind this complex syndrome. Here, we review to which extent these biological models are affected by the absence of FMRP, pointing out the similarities with the observed human dysfunction. Additionally, we discuss several potential treatments under study in animal models that are able to partially revert some of the FXS abnormalities.

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A Dynamic Deep Sleep Stage inDrosophila

Cited by 213 publications

References 46 publications

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Learning and behavioral deficits associated with the absence of the fragile X mental retardation protein: what a fly and mouse model can teach us

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