A Circadian Output Circuit Controls Sleep-Wake Arousal in Drosophila

Guo, Fang; Holla, Meghana; Díaz, Madelen M; Rosbash, Michael

doi:10.1016/j.neuron.2018.09.002

Cited by 163 publications

(193 citation statements)

References 52 publications

Supporting

Mentioning

176

Contrasting

Unclassified

Order By: Relevance

“…This is consistent with thermogenetic activation of the AOTU increasing total amount of sleep in flies 17 . Generating coherent AOTU output could be mediated by sleep-modulating DN1 circadian clock neurons 32 , which form direct connections with the AOTU and are likely to modulate oscillatory activity in R2 neurons 14 .…”

Section: Discussionmentioning

confidence: 99%

“…Helicon cells also receive visual information and are part of a recurrent circuit mediating homeostatic sleep regulation 15,33 . Thus, R2 oscillatory activity is likely regulated via a complex interplay of sensory input 19 , circadian rhythms 14,17 and homeostatic sleep regulation 15 .…”

Section: Discussionmentioning

confidence: 99%

“…To investigate, whether input pathways generated or shaped delta-oscillations, we expressed the red light activatable channelrhodopsin CsChrimson in AOTU (anterior optical tubercle) neurons that provide direct sensory and circadian input to R2 14,17,19 . Compared to previous experiments ( Fig.…”

Section: R2 Network-specific Multi-unit Synchronization Generates Delmentioning

confidence: 99%

“…Here, we discover sleep regulating network-specific delta oscillations within the R2 network of the Drosophila ellipsoid body, which is situated at a crossroad involved in sleep regulation [14][15][16] and multi-sensory relay for higher-order neural processing [17][18][19] . We demonstrate wave oscillations characteristic of 'local sleep' phenomena in vertebrates 2,24 .…”

Section: Introductionmentioning

confidence: 99%

“…This defined network of 10 cells per hemisphere (Fig. 1a) resides within the ellipsoid body and is involved in sleep regulation [14][15][16] and multi-sensory relay [17][18][19] .In vivo recordings of the dendritic processes (bulb) of R2 neurons (Fig. 1a) identified electrical compound activity (Fig.…”

mentioning

confidence: 99%

See 4 more Smart Citations

Network-specific synchronization of electrical slow-wave oscillations regulates sleep in Drosophila

Raccuglia

Huang²,

Ender

et al. 2019

Preprint

View full text Add to dashboard Cite

Slow-wave rhythms characteristic of deep sleep oscillate in the delta band (0.5 -4 Hz) andcan be found across various brain regions in vertebrates. Across systems it is however unclear how oscillations arise and whether they are the causal functional unit steering behavior. Here, for the first time in any invertebrate, we discover sleep-relevant delta oscillations in Drosophila.We find that slow-wave oscillations in the sleep-regulating R2 network increase with sleep need. Optical multi-unit voltage recordings reveal that single R2 neurons get synchronized by sensory and circadian input pathways. We show that this synchronization depends on NMDA receptor (NMDARs) coincidence detector function and on an interplay of cholinergic and glutamatergic inputs setting a resonance frequency. Genetically targeting the coincidence detector function of NMDARs in R2, and thus the uncovered mechanism underlying synchronization, abolished network-specific slow-wave oscillations. It also disrupted sleep and facilitated light-induced wakening, directly establishing a causal role for slow-wave oscillations in regulating sleep and sensory gating. We therefore propose that the synchronization-based increase in oscillatory power likely represents an evolutionarily conserved, potentially 'optimal', strategy for constructing sleep-regulating sensory gates. that these delta oscillations depend on multi-unit synchronization mediated through NMDA receptor (NMDAR) coincidence detection. Disrupting this synchronization and thus the emergence of compound delta oscillations disrupts sleep and alters sensory gating during sleep. We thus identify slow-wave oscillations as an electrophysiological correlate for sleep regulation in invertebrates and place these oscillatory patterns at the basis of behavior. The sleep-regulating oscillations are comparable to sleep-regulating thalamic oscillations 20-22 as well as network-specific oscillations observed during sleep deprivation in vertebrates (local sleep) 2,23,24 . Our work demonstrates that slow-wave oscillations and sleep are fundamentally interconnected across systems, potentially representing an evolutionarily conserved strategy for network mechanisms regulating internal states and sleep. Results Sleep deprivation increases network-driven delta oscillations in the sleep-regulating R2 networkExamples of rhythmic activity patterns have previously been reported in insects 9,10 .However, their source, function and interdependence with internal states (such as sleep drive), remain largely unclear. We targeted expression of the GEVI ArcLight specifically to R2 neurons in the Drosophila brain. This defined network of 10 cells per hemisphere (Fig. 1a) resides within the ellipsoid body and is involved in sleep regulation [14][15][16] and multi-sensory relay [17][18][19] .In vivo recordings of the dendritic processes (bulb) of R2 neurons (Fig. 1a) identified electrical compound activity (Fig. 1b) that oscillated at delta-band frequencies between 0.5-1.5 Hz (Fig. 1b, d) in rested flies. We sleep-deprived f...

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: R2 Network-specific Multi-unit Synchronization Generates Delmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Network-specific synchronization of electrical slow-wave oscillations regulates sleep in Drosophila

Raccuglia

Huang²,

Ender

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

Neuroarchitecture of the central complex of the desert locust: Tangential neurons

Hadeln

Hensgen

Bockhorst

et al. 2019

J of Comparative Neurology

111

View full text Add to dashboard Cite

The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons.While pontine and columnar neurons have been analyzed in detail, especially in the fruit fly and desert locust, understanding of the organization of tangential cells is still rudimentary. As a basis for future functional studies, we have studied the morphologies of tangential neurons of the CX of the desert locust Schistocerca gregaria. Intracellular dye injections revealed 43 different types of tangential neuron, 8 of the PB, 5 of the CBL, 24 of the CBU, 2 of the noduli, and 4 innervating multiple substructures. Cell bodies of these neurons were located in 11 different clusters in the cell body rind. Judging from the presence of fine versus beaded terminals, the vast majority of these neurons provide input into the CX, especially from the lateral complex (LX), the superior protocerebrum, the posterior slope, and other surrounding brain areas, but not directly from the mushroom bodies. Connections are largely subunit-and partly layer-specific. No direct connections were found between the CBU and the CBL. Instead, both subdivisions are connected in parallel with the PB and distinct layers of the noduli.

show abstract

Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types

Hensgen

England

Homberg

et al. 2020

J of Comparative Neurology

View full text Add to dashboard Cite

The central complex (CX) in the insect brain is a higher order integration center that controls a number of behaviors, most prominently goal directed locomotion. The CX comprises the protocerebral bridge (PB), the upper division of the central body (CBU), the lower division of the central body (CBL), and the paired noduli (NO). Although spatial orientation has been extensively studied in honeybees at the behavioral level, most electrophysiological and anatomical analyses have been carried out in other insect species, leaving the morphology and physiology of neurons that constitute the CX in the honeybee mostly enigmatic. The goal of this study was to morphologically identify neuronal cell types of the CX in the honeybee Apis mellifera. By performing iontophoretic dye injections into the CX, we traced 16 subtypes of neuron that connect a subdivision of the CX with other regions in the bee's central brain, and eight subtypes that mainly interconnect different subdivisions of the CX. They establish extensive connections between the CX and the lateral complex, the superior protocerebrum and the posterior protocerebrum. Characterized neuron classes and subtypes are morphologically similar to those described in other insects, suggesting considerable conservation in the neural network relevant for orientation.

show abstract

A Circadian Output Circuit Controls Sleep-Wake Arousal in Drosophila

Abstract: Highlights d Some Drosophila circadian neurons including APDNs promote sleep d Sleep-promoting APDNs signal to the homeostatic sleep center EB-R2 via the TuBu sup d Activation of APDNs promotes calcium oscillation in EB-R2 neurons d The APDN-TuBu sup-EB circuit regulates sleep-wake arousal

Cited by 163 publications

References 52 publications

Network-specific synchronization of electrical slow-wave oscillations regulates sleep in Drosophila

Network-specific synchronization of electrical slow-wave oscillations regulates sleep in Drosophila

Neuroarchitecture of the central complex of the desert locust: Tangential neurons

Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types

Contact Info

Product

Resources

About