Identification of octopaminergic neurons that modulate sleep suppression by male sex drive

Machado, Daniel Rodrigues; Afonso, Dinis J.S.; Kenny, Alexandra R; Öztürk-Çolak, Arzu; Moscato, Emilia H.; Mainwaring, Benjamin; Kayser, Matthew S.; Koh, Kyunghee

doi:10.7554/elife.23130

Cited by 67 publications

(100 citation statements)

References 78 publications

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“…A subset of OANs in the SEZ balance sleep and courtship in male flies. Activation of these octopaminergic MS1 neurons suppressed sleep, while silencing the same neurons led to decreased female-induced sleep loss and impaired mating behaviour in male flies [80]. Furthermore, other OANs in the SEZ are important to integrate AKH and DILP signals to modulate activity levels in response to the nutritional situation [9].…”

Section: Which Oans Are Involved In Balancing Activity Levels With Rementioning

confidence: 99%

Endocrine fine-tuning of daily locomotor activity patterns under non-starving conditions in Drosophila

Pauls

Selcho

Raederscheidt

et al. 2020

Preprint

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body ATP-sensitive potassium channels [6]. This triggers AKH release in a calcium-and AMP-activated protein kinase-dependent fashion [13]. Similar to glucagon, AKH acts on energy stores in the fat body by mobilising carbohydrates in form of the haemolymph sugar trehalose (hypertrehalosaemic effect), and by mobilising lipid depots (adipokinetic effect) [8,[14][15][16].OA, an analogue to vertebrate noradrenaline, is considered to act as an insect stress or arousal hormone [17]. OA is produced by octopaminergic neurons (OANs) located mostly along the midline in the brain and ventral nerve cord [18]. Among other functions, OA exerts myotropic effects on skeletal muscles [19] and mediates the adaptation of muscle metabolism to the physiological demands of locomotion [20][21][22].Both AKH and OA are crucial for starvation-induced hyperactivity, as this behaviour is absent in flies with impaired AKH or OA signalling [4,5,[7][8][9]. AKH activates a subset of OANs which are required for starvation-induced hyperactivity [5,9]. These neurons express receptors for AKH and Drosophila insulin-like peptides (DILPs). DILPs act antagonistically to AKH, and suppress starvation-induced hyperactivity via the OANs [9]. Yu and colleagues (2016) showed that the AKH-dependent increase in locomotor activity upon starvation represents a neuromodulatory and behavioural role of AKH and is not an indirect consequence of altered energy metabolism.Remarkably, studies in various insect species suggest that AKH and also OA play a role in the regulation of locomotor activity when the insects have free access to food (reviewed in [23]). For example, the circulating haemolymph titres of AKH correlate positively with daily rhythms in walking activity in the linden bug Pyrrhocoris apterus [24,25]. In Pyrrhocoris [26,27], crickets [28] and the cockroach Periplaneta americana [29,30], injection into the haemolymph or topical application of AKH induces a strong increase in locomotor activity in ad libitum fed animals, independent of the time of day [27,29]. Also in Drosophila, genetic overexpression of AKH enhances locomotor activity when food is freely available [31]. Unlike for starvation-induced hyperactivity, however, it is unclear whether and how AKH:OAN signalling contributes to shape daily activity under ad libitum feeding conditions, or whether increased AKH signalling is a consequence of a locomotor-induced increase in energy demands. Cockroach AKHs are known to increase the spontaneous neuronal activity of octopaminergic dorsal unpaired median neurons in the central nervous system, which express a

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Section: Which Oans Are Involved In Balancing Activity Levels With Rementioning

confidence: 99%

Endocrine fine-tuning of daily locomotor activity patterns under non-starving conditions in Drosophila

Pauls

Selcho

Raederscheidt

et al. 2020

Preprint

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“…Many environmental factors, including food availability, social interactions and temperature, potently impact sleep in diverse phyla (McNamara et al, 2009;Capellini, 2010). For example, sleep is reduced in flies reared in isolation, and exposure of male flies to females suppresses sleep, revealing robust modulation of sleep by social stimuli (Ganguly-Fitzgerald, 2006;Beckwith et al, 2017;Chen et al, 2017;Machado et al, 2017). These important modulators of sleep are likely to be missed in behavioral assays used in most animal systems that measure each animal in an independent arena, and highlight the need for investigating sleep in an ecologically relevant context.…”

Section: Additional Ecologically Relevant Factors That Modulate Sleepmentioning

confidence: 99%

The origins and evolution of sleep

Keene

Duboué

2018

Journal of Experimental Biology

143

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Sleep is nearly ubiquitous throughout the animal kingdom, yet little is known about how ecological factors or perturbations to the environment shape the duration and timing of sleep. In diverse animal taxa, poor sleep negatively impacts development, cognitive abilities and longevity. In addition to mammals, sleep has been characterized in genetic model organisms, ranging from the nematode worm to zebrafish, and, more recently, in emergent models with simplified nervous systems such as and jellyfish. In addition, evolutionary models ranging from fruit flies to cavefish have leveraged natural genetic variation to investigate the relationship between ecology and sleep. Here, we describe the contributions of classical and emergent genetic model systems to investigate mechanisms underlying sleep regulation. These studies highlight fundamental interactions between sleep and sensory processing, as well as a remarkable plasticity of sleep in response to environmental changes. Understanding how sleep varies throughout the animal kingdom will provide critical insight into fundamental functions and conserved genetic mechanisms underlying sleep regulation. Furthermore, identification of naturally occurring genetic variation regulating sleep may provide novel drug targets and approaches to treat sleep-related diseases.

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“…Our finding that flies do not rebound after starvation-induced sleep loss can be extended to other ethologically-relevant perturbations. For example, male flies deprived of sleep by pairing with a receptive female, presumably resulting in sexual excitation, does not induce a sleep rebound when the female is removed [61,62]. Together, these findings raise the possibility that flies may be resilient to some ethologically relevant forms of sleep deprivation and highlight the importance of studying the genetic and neural processes regulating sleep across diverse environmental contexts.…”

Section: Discussionmentioning

confidence: 99%

Drosophila insulin-like peptide 2mediates dietary regulation of sleep intensity

Brown

Shah

Faville³

et al. 2019

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18Sleep is a nearly universal behavior that is regulated by diverse environmental and physiological 19 stimuli. A defining feature of sleep is a homeostatic rebound following deprivation, where 20 animals compensate for lost sleep by increasing sleep duration and/or sleep depth. Fruit flies 21 exhibit robust recovery sleep following deprivation and represent a powerful model to study 22 neural circuits regulating sleep homeostasis. Numerous neuronal populations have been 23 identified in modulating sleep homeostasis as well as depth, raising the possibility that recovery 24 sleep is differentially regulated by environmental or physiological processes that induce sleep 25 deprivation. Here, we find that unlike most pharmacological and environmental manipulations 26 commonly used to restrict sleep, starvation potently induces sleep loss without a subsequent 27 rebound in sleep duration or depth. We find that both starvation and a sucrose-only diet result in 28 reduced metabolic rate and increased sleep depth, suggesting that dietary yeast protein is 29 essential for normal sleep depth and homeostasis. Finally, we find that Drosophila insulin like 30 peptide 2 (Dilp2) is required for starvation-induced changes in sleep depth without regulating the 31 duration of sleep. Remarkably, Dilp2 mutant flies require rebound sleep following sleep 32 deprivation, suggesting Dilp2 underlies resilience to sleep loss. Together, these findings reveal 33 innate resilience to starvation-induced sleep loss and identify distinct mechanisms that underlie 34 starvation-induced changes in sleep duration and depth.35 3 Author Summary 36 Sleep is nearly universal throughout the animal kingdom and homeostatic regulation represents 37 a defining feature of sleep, where animals compensate for lost sleep by increasing sleep over 38 subsequent time periods. Despite the robustness of this feature, surprisingly little is known 39 about how recovery-sleep is regulated in response to different types of sleep deprivation. Fruit 40 flies provide a powerful model for investigating the genetic regulation of sleep, and like 41 mammals, display robust recovery sleep following deprivation. Here, we find that unlike most 42 stimuli that suppress sleep, sleep deprivation by starvation does not require a homeostatic 43 rebound. These findings appear to be due to flies engaging in deeper sleep during the period of 44 partial deprivation, suggesting a natural resilience to starvation-induced sleep loss. This unique 45 resilience to starvation-induced sleep loss is dependent on Drosophila insulin-like peptide 2, 46 suggesting a critical role for insulin signaling in regulating interactions between diet and sleep 47 homeostasis. 48 4 Introduction 49Sleep is a near universal behavior that is modulated in accordance with internal and external 50 environments [1][2][3]. Numerous environmental factors can alter sleep including daily changes in 51 light and temperature, stress, social interactions, and nutrient availability [4,5]. A central factor 52 defining sleep i...

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Identification of octopaminergic neurons that modulate sleep suppression by male sex drive

Cited by 67 publications

References 78 publications

Endocrine fine-tuning of daily locomotor activity patterns under non-starving conditions in Drosophila

Endocrine fine-tuning of daily locomotor activity patterns under non-starving conditions in Drosophila

The origins and evolution of sleep

Drosophila insulin-like peptide 2mediates dietary regulation of sleep intensity

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