Presynaptic Active Zone Plasticity Encodes Sleep Need in Drosophila

Huang, Sheng; Piao, Chengji; Beuschel, Christine B.; Götz, Torsten; Sigrist, Stephan J.

doi:10.1016/j.cub.2020.01.019

Cited by 46 publications

(119 citation statements)

References 85 publications

(158 reference statements)

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“…For these ring neurons, ring attractor networks offer a compelling structure-function relationship which can provide a rationale for their ring-shaped structure. On the other hand, sleep related ring neurons serve as homeostatic sleep integrator, encoding sleep drive through structural 18,24 and activity changes 18,23 . To elucidate the relationship between these suggested navigation and sleep functionalities of ring neurons, we therefore asked what role the homeostatic integrator could play in the ring attractor framework.…”

Section: Discussionmentioning

confidence: 99%

“…The introduction of plasticity was motivated by the observation of structural, synaptic and functional changes in homeostatic ring neurons 18,23,24 as well as their likely connectivity to the head direction system 14,28 . In past work, plasticity has been introduced in ring attractor models to circumvent the problem of fine tuning [34][35][36] , in contrast to the role of plasticity proposed here, which is to maintain bump activity at a setpoint.…”

Section: Discussionmentioning

confidence: 99%

“…In past work, plasticity has been introduced in ring attractor models to circumvent the problem of fine tuning [34][35][36] , in contrast to the role of plasticity proposed here, which is to maintain bump activity at a setpoint. The proposed models can capture the increase in activity in ring neurons during wake time 18,24 (Figures 2 and 4), although the exact time course of this integrator signal has not been measured. Additionally, in the proposed models, sleep deprivation leads to a qualitative change in the behavior of ring neurons towards oscillatory dynamics which is reminiscent of the 10/29 experimentally observed transition to bursting dynamics 18 or increase in oscillatory dynamics 23 .…”

Section: Discussionmentioning

confidence: 99%

“…The morphological similarity of the involved ring neurons and the spatial proximity of the circuits as well as the connectome 14 , suggest however that they interact. Given the observed structural changes in the sleep-related ring neurons 18,23,24 , this suggests that the head direction system needs to operate in the face of substantial synaptic and functional changes in connected circuits.…”

Section: Introductionmentioning

confidence: 99%

“…Motivated by these experimental observations of plasticity 18,23,24 , we here use theoretical modeling to discuss how sleep homeostasis and navigation can be understood as a combined system (see Figure 1A for a schematic summary). We show that ring neurons can be assigned the role of integrating homeostatic sleep drive (referred to in the following as 'homeostatic integrator', see Figure 1B), while at the same time maintaining an operational head direction system (wedge neurons) in the face of plasticity.…”

Section: Introductionmentioning

confidence: 99%

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Integration of sleep homeostasis and navigation inDrosophila

Valle

Gonçalves

Seelig

2020

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During sleep, the brain undergoes dynamic and structural changes. In Drosophila, such changes have been observed in the central complex, a brain area important for sleep control and navigation. For navigation, the structure and function of the central complex suggest a relationship to ring attractors, networks that model head direction. This raises the question about a similar structure-function relationship for sleep control.Motivated by experimental findings, we develop a ring attractor model that maintains activity at a setpoint in the face of plasticity. In this model, an integrator of sleep drive emerges with a functional role in stabilizing the network. Nevertheless, the network becomes unstable over extended wake time. Therefore, a sleep phase is introduced where autonomous attractor dynamics, related to its activity during wakefulness, reset the network. The proposed integration of sleep and head direction circuits captures features of their neural dynamics observed in flies and mice during wakefulness and sleep.Author SummaryIn Drosophila, the study of sleep and the study of navigation are largely disconnected fields, even though the same brain structures and connected neural circuits are important for the two different functionalities. Motivated by experimental results from both fields, we use theoretical modeling to describe the coupled dynamics of sleep and navigation circuits and propose a rationale for why they interact. The resulting model can incorporate and explain several experimental findings about sleep and navigation in flies and mice. The model is based on a ring attractor network which is combined with plasticity rules that change between sleep and wake phases and shows autonomous dynamics during sleep, reminiscent of observations in the head direction system of mice.

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