A Paradoxical Kind of Sleep in Drosophila melanogaster

Tainton-Heap, Lucy A.L.; Kirszenblat, Leonie; Notaras, Eleni; Grabowska, Martyna; Jeans, Rhiannon; Feng, Kai; Shaw, Paul J.; Swinderen, Bruno van

doi:10.1016/j.cub.2020.10.081

Cited by 61 publications

(169 citation statements)

References 73 publications

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“…Blue light did not increase rest in WT flies fed ATR or vehicle, but dramatically increased rest in the dFSB and EB driver flies (Figure 6C,D). The drivers differed in both potency and on/off kinetics: the dFSB driver rapidly induces sleep in all ATR fed flies, and flies woke from sleep shortly after the light was turned off, consistent with prior reports (Tainton-Heap et al, 2020). In contrast, the EB driver induced a lower level of sleep that persisted even after the blue light was removed (Figure 6B).…”

Section: Optogenetically-induced Sleep Is Not Sufficient To Enhance Learningsupporting

confidence: 87%

“…However, we do not find that optogenetically-induced rest promotes learning (Figure 6). This failure to promote learning could be due to optogenetically-induced rest not promoting the learning-associated sleep state (Liu et al, 2019;Wiggin et al, 2020), as the brain-state of flies with dFSB-induced sleep is significantly different from the brain-state of spontaneous sleep (Tainton-Heap et al, 2020). It is also possible that the precise timing of rest is important to its learning-associated function and the timing of optogenetically-induced rest is suboptimal.…”

Section: Learning Memory and Rest In Drosophilamentioning

confidence: 99%

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Rest is Required to Learn an Appetitively-Reinforced Operant Task inDrosophila

Wiggin

Hsiao

Liu

et al. 2020

Preprint

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Maladaptive operant conditioning contributes to development of neuropsychiatric disorders. Candidate genes have been identified that contribute to this maladaptive plasticity, but the neural basis of operant conditioning in genetic model organisms remains poorly understood. The fruit fly Drosophila melanogaster is a versatile genetic model organism that readily forms operant associations with punishment stimuli. However, operant conditioning with a food reward has not been demonstrated in flies, limiting the types of neural circuits that can be studied. Here we present the first sucrose-reinforced operant conditioning paradigm for flies. Flies of both sexes walk along a Y-shaped track with reward locations at the terminus of each hallway. When flies turn in the reinforced direction at the center of the track, sucrose is presented at the end of the hallway. Only flies that rest during training show evidence of learning the reward contingency. Flies rewarded independently of their behavior do not form a learned association but have the same amount of rest as trained flies, showing that rest is not driven by learning. Optogenetically-induced rest does not promote learning, indicating that rest is not sufficient for learning the operant task. We validated the sensitivity of this assay to detect the effect of genetic manipulations by testing the classic learning mutant dunce. Dunce flies are learning impaired in the Y-Track task, indicating a likely role for cAMP in the operant coincidence detector. This novel training paradigm will provide valuable insight into the molecular mechanisms of disease and the link between sleep and learning.SIGNIFICANCE STATEMENTOperant conditioning and mental health are deeply intertwined: maladaptive conditioning contributes to many pathologies, while therapeutic operant conditioning is a frequently used tool in talk therapy. Unlike drug interventions which target molecules or mechanisms, it is not known how operant conditioning changes the brain to promote wellness or distress. To gain mechanistic insight into how this form of learning works, we developed a novel operant training task for the fruit fly Drosophila melanogaster. We made three key discoveries. First, flies are able to learn an operant task to find food reward. Second, rest during training is necessary for learning. Third, the dunce gene is necessary for both classical and operant conditioning in flies, indicating that they may share molecular mechanisms.

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Section: Optogenetically-induced Sleep Is Not Sufficient To Enhance Learningsupporting

confidence: 87%

Section: Learning Memory and Rest In Drosophilamentioning

confidence: 99%

Rest is Required to Learn an Appetitively-Reinforced Operant Task inDrosophila

Wiggin

Hsiao

Liu

et al. 2020

Preprint

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“…In addition, we also found a moderate increase in eye movements and ventilation rate during 'Active sleep'. (Tainton-Heap et al, 2021) suggests strong selection pressure across evolution for an alternation between 'Quiet' and 'Active' sleep states. The occurrence of the non-REM/REM alternation in mammals, birds, and in some reptiles, such as in the bearded dragon and in the argentine tegu Salvator merianae (Dumé ril and Bibron, 1839;Libourel et al, 2018;Shein-Idelson et al, 2016), points to a common origin of the wake-sleep cycle in these groups of animals, which share a common ancestor (Libourel et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Cyclic alternation of quiet and active sleep states in the octopus

Medeiros

Paiva

Lopes³

et al. 2021

iScience

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Previous observations suggest the existence of 'Active sleep' in cephalopods. To investigate in detail the behavioral structure of cephalopod sleep, we video-recorded four adult specimens of Octopus insularis and quantified their distinct states and transitions. Changes in skin color and texture and movements of eyes and mantle were assessed using automated image processing tools, and arousal threshold was measured using sensory stimulation. Two distinct states unresponsive to stimulation occurred in tandem. The first was a 'Quiet sleep' state with uniformly pale skin, closed pupils, and long episode durations (median 415.2 s). The second was an 'Active sleep' state with dynamic skin patterns of color and texture, rapid eye movements, and short episode durations (median 40.8 s). 'Active sleep' was periodic (60% of recurrences between 26 and 39 min) and occurred mostly after 'Quiet sleep' (82% of transitions). These results suggest that cephalopods have an ultradian sleep cycle analogous to that of amniotes.

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“…Functional imaging during sleep has so far only been performed in flies that were placed on the ball for short periods of time 21 . Similarly, circadian activity has so far only been investigated in immobilized animals 2, 3 .…”

Section: Discussionmentioning

confidence: 99%

Automated long-term two-photon imaging in head-fixed walkingDrosophila

Valle

Honnef

Seelig

2021

Preprint

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The brain of Drosophila shows dynamics at multiple timescales, from the millisecond range of fast voltage or calcium transients to functional and structural changes occurring over multiple days. To relate such dynamics to behavior requires monitoring neural circuits across these multiple timescales in behaving animals. Here, we develop a technique for automated long-term two-photon imaging in fruit flies, during wakefulness and sleep, navigating in virtual reality over up to seven days. The method is enabled by laser surgery, a microrobotic arm for controlling forceps for dissection assistance, an automated feeding robot, as well as volumetric, simultaneous multiplane imaging. The approach is validated in the fly's head direction system. Imaging in behaving flies over multiple timescales will be useful for understanding circadian activity, learning and long-term memory, or sleep.

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A Paradoxical Kind of Sleep in Drosophila melanogaster

Cited by 61 publications

References 73 publications

Rest is Required to Learn an Appetitively-Reinforced Operant Task inDrosophila

Rest is Required to Learn an Appetitively-Reinforced Operant Task inDrosophila

Cyclic alternation of quiet and active sleep states in the octopus

Automated long-term two-photon imaging in head-fixed walkingDrosophila

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