Recurrent Circuitry for Balancing Sleep Need and Sleep

Donlea, Jeffrey M.; Pimentel, Diogo; Talbot, Clifford B.; Kempf, Anissa; Omoto, Jaison J.; Hartenstein, Volker; Miesenböck, Gero

doi:10.1016/j.neuron.2017.12.016

Cited by 186 publications

(337 citation statements)

References 65 publications

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“…The fact that a highly conserved brain region like the central complex appears to be at the heart of path integration is striking, as the basic neural circuits proposed to underlie path integration are also present in non-homing insects. Clearly this brain region is involved in a stunningly rich variety of behaviors beyond path integration [81,89,109,111,122–124], and it will be a major task to pin these to specific components or computations of the neural circuitry of this brain center. Whether these path integration circuits have been modified from an ancestral version to endow homing insects with a capable path integrator, or if all insects have a basic ability to path integrate is a yet to be illuminated.…”

Section: Steeringmentioning

confidence: 99%

Principles of Insect Path Integration

2018

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Continuously monitoring its position in space relative to a goal is one of the most essential tasks for an animal that moves through its environment. Species as diverse as rats, bees, and crabs achieve this by integrating all changes of direction with the distance covered during their foraging trips, a process called path integration. They generate an estimate of their current position relative to a starting point, enabling a straight-line return, following what is known as a home vector. While in theory path integration always leads the animal precisely back home, in the real world noise limits the usefulness of this strategy when operating in isolation. Noise results from stochastic processes in the nervous system and from unreliable sensory information, particularly when obtaining heading estimates. Path integration, during which angular self-motion provides the sole input for encoding heading (idiothetic path integration), results in accumulating errors that render this strategy useless over long distances. In contrast, when using an external compass this limitation is avoided (allothetic path integration). Many navigating insects indeed rely on external compass cues for estimating body orientation, whereas they obtain distance information by integration of steps or optic-flow-based speed signals. In the insect brain, a region called the central complex plays a key role for path integration. Not only does the central complex house a ring-attractor network that encodes head directions, neurons responding to optic flow also converge with this circuit. A neural substrate for integrating direction and distance into a memorized home vector has therefore been proposed in the central complex. We discuss how behavioral data and the theoretical framework of path integration can be aligned with these neural data.

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Section: Steeringmentioning

confidence: 99%

Principles of Insect Path Integration

2018

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“…The insect central complex has been suggested to serve roles in decision making and action selection (Ritzmann et al, 2012;Sun et al, 2017;Wolff & Strausfeld, 2016), control of locomotion (Martin, Guo, Mu, Harley, & Ritzmann, 2015;Strauss, 2002), spatial orientation and navigation (Heinze, 2017;Pfeiffer & Homberg, 2014;Turner-Evans & Jayaraman, 2016;Varga, Kathman, Martin, Guo, & Ritzmann, 2017), and, in Drosophila, promotion of sleep (Donlea et al, 2018;Liu et al, 2016). TL neurons provide sky compass information to the CBL in locusts, crickets, monarch butterflies, beetles, and bees (el Jundi et al, 2015;Heinze & Reppert, 2011;Homberg, Heinze, Pfeiffer, Kinoshita & el Jundi, 2011;Pegel, Pfeiffer, & Homberg, 2018;Sakura et al, 2008;Stone et al, 2017), and R neurons, heading direction relative to a bright target in fruit flies (Seelig & Jayaraman, 2013;Shiozaki & Kazama, 2017).…”

Section: Functional Implicationsmentioning

confidence: 99%

“…Extracellular recordings in cockroaches and Ca‐imaging experiments in flies indicate that certain central‐complex neurons signal heading direction based on visual panorama information and self‐generated proprioceptive input (Seelig & Jayaraman, , ; Varga & Ritzmann, ). Somewhat unrelated to this is an established role in sleep homeostasis in flies (Donlea et al, ; Liu, Liu, Tabucchi, & Wu, ). In all pterygote insects studied so far, four subunits of the central complex have been recognized; the protocerebral bridge (PB), the upper and lower divisions of the central body (CBU, CBL; also termed fan‐shaped body and ellipsoid body, respectively) and a pair of ventral noduli (Pfeiffer & Homberg, ).…”

Section: Introductionmentioning

confidence: 99%

GABA immunostaining in the central complex of dicondylian insects

Homberg

Humberg

Seyfarth

et al. 2018

J of Comparative Neurology

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The central complex is a group of midline-crossing neuropils in the insect brain involved in head direction coding, sky compass navigation, and spatial visual memory. To compare the neuroarchitecture and neurochemistry of the central complex in insects that differ in locomotion, ways of orientation, time of activity (diurnal, nocturnal), and evolutionary history, we studied the distribution of γ-aminobutyric acid (GABA) immunostaining in the central complex of 29 species, ranging from Zygentoma to Diptera. In all species, the lower division of the central body was densely innervated by GABA-immunoreactive tangential neurons. These neurons had additional arborizations in the bulb, a distinct region of synaptic complexes in the lateral complex, and somata in a cell cluster mediodorsally to the antennal lobe. Differences in the appearance of GABA immunostaining in the lower division of the central body corresponded to differences in neuropil architecture, such as transformation of the lower division into a toroid in certain Diptera and Heteroptera. In nearly all species two additional systems of tangential neuron of the upper division of the central body were GABA-immunoreactive. One of these systems diffusely invaded a superior layer, while the second system showed fan-like projections in an inferior layer. Sparse immunostaining in the protocerebral bridge was detected in cockroaches, a cricket, and two hemipteran species. The data show that three systems of GABA-immunoreactive tangential neurons of the central body are highly conserved and suggest that the layered organization of the upper division of the central body is, likewise, largely maintained from basal to advanced species.

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“…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%

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

Raccuglia

Huang²,

Ender

et al. 2019

Preprint

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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...

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Recurrent Circuitry for Balancing Sleep Need and Sleep

Cited by 186 publications

References 65 publications

Principles of Insect Path Integration

Principles of Insect Path Integration

GABA immunostaining in the central complex of dicondylian insects

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

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