Organization of the Drosophila larval visual circuit

Larderet, Ivan; Fritsch, Pauline Mj; Gendre, Nanaë; Neagu-Maier, G. Larisa; Fetter, Richard D.; Schneider-Mizell, Casey M; Truman, James W.; Zlatic, Marta; Cardona, Albert; Sprecher, Simon G.

doi:10.7554/elife.28387

Cited by 68 publications

(72 citation statements)

References 104 publications

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“…This wrapping function, however, is found only in the nerves. In the neuropil, where axons, dendrites, and synapses intermingle, no wrapping of individual axons is detected (Berck et al, 2016;Kremer et al, 2017;Larderet et al, 2017). Given its ability to wrap around axons in the CNS we suggest that ensheathing glia most closely match oligodendrocytes-even though myelin is never formed in the Drosophila CNS.…”

Section: Wrapping and Ensheathing Gliamentioning

confidence: 84%

Drosophila glia: Few cell types and many conserved functions

Yildirim

Petri

Kottmeier

et al. 2018

Glia

141

153

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Glial cells constitute without any dispute an essential element in providing an efficiently operating nervous system. Work in many labs over the last decades has demonstrated that neuronal function, from action potential generation to its propagation, from eliciting synaptic responses to the subsequent postsynaptic integration, is evolutionarily highly conserved. Likewise, the biology of glial cells appears conserved in its core elements and therefore, a deeper understanding of glial cells is expected to benefit from analyzing model organisms such as Drosophila melanogaster. Drosophila is particularly well suited for studying glial biology since in the fly nervous system only a limited number of glial cells exists, which can be individually identified based on position and a set of molecular markers. In combination with the well‐known genetic tool box an unprecedented level of analysis is feasible, that not only can help to identify novel molecules and principles governing glial cell function but also will help to better understand glial functions first identified in the mammalian nervous system. Here we review the current knowledge on Drosophila glia to spark interest in using this system to analyze complex glial traits in the future.

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Section: Wrapping and Ensheathing Gliamentioning

confidence: 84%

Drosophila glia: Few cell types and many conserved functions

Yildirim

Petri

Kottmeier

et al. 2018

Glia

141

153

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“…To identify the photosensory and thermosensory PNs connected to KCs, we identified all neurons downstream of 12 photosensory neurons 65 in the left and right brain hemispheres and all neurons downstream of three previously characterized cold sensing neurons, expressed in 11F02-GAL4 line 66 .…”

Section: Identification Of Pnsmentioning

confidence: 99%

The complete connectome of a learning and memory center in an insect brain

Eichler

Litwin-Kumar

Feng

et al. 2017

Preprint

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Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higherorder circuit supporting associative memory has not been previously available. We reconstructed one such circuit at synaptic resolution, the Drosophila larval mushroom body, and found that most Kenyon cells integrate random combinations of inputs but a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections between output neurons could enhance the selection of learned responses. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory center.Massively parallel, higher-order neuronal circuits such as the cerebellum and insect mushroom body serve to form and retain associations between stimuli and reinforcement in vertebrates and higher invertebrates [1][2][3][4][5][6] . Although these systems provide a biological substrate for adaptive behavior, no complete synapseresolution wiring diagram of their connectivity has been available to guide analysis and inspire understanding. The mushroom body (MB) is a higher-order parallel fiber system in many invertebrate brains, including hemimetabolous as well as holometabolous insects and their larval stages 6 . MB function is essential for associative learning in adult insects 1;3-5 and in Drosophila larvae 1;7;8 , from the earliest larval stages onward 9 . Indeed, the basic organization of the adult and the larval MB and their afferent circuits is very similar; however, larvae have about an order of magnitude fewer neurons 7 . Thus, to systematically investigate the organizational logic of the MB, we used serial section electron microscopy (EM) to map with synaptic resolution the complete MB connectome in a first instar Drosophila larva (L1; Fig. 1a). L1 are foraging animals capable of all behaviors previously described in later larval stages 10 , including adaptive behaviors dependent on associative learning 7;9 (Fig. 1b). Their smaller neurons enable fast EM imaging of the entire nervous system and reconstruction of complete circuits 11;12 . Models of sensory processing in many neural circuits feature neurons that fire in response to combinations of sensory inputs, generating a high-dimensional representation of the sensory environment 13 . The intrinsic MB neurons, the Kenyon cells (KCs), integrate in their dendrites inputs from combinations of projection neurons (PNs) that encode various stimuli, predominantly olfactory in both adult 1;4-6 , and larva 12;14 , but also thermal, gustatory

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“…1a). VPNs further relay signals to higher brain regions that process multiple sensory modalities 15 . Despite the simple anatomy of their visual systems, larvae excel at visually-guided behaviors.…”

Section: Introductionmentioning

confidence: 99%

“…A recent connectome study using serial section transmission electron microscopy (ssTEM) reconstruction mapped synaptic interactions within the LON in the 1 st instar larval brain 15 . This comprehensive wiring diagram of the larval visual circuit revealed two separate visual pathways emerging at the level of the PRs that express either bluetuned Rhodopsin 5 (Rh5-PRs) or green-tuned Rhodopsin 6 (Rh6-PRs).…”

Section: Introductionmentioning

confidence: 99%

“…Behavioral studies suggest that the spectral differentiation in PRs does not code for color discrimination, but rather generates independent processing for spatial and temporal information during larval navigation. Specifically, while Rh5-PRs are essential for navigation based on spatial cues, Rh6-PRs are involved in perceiving temporal changes of light intensity during larval head casts and contribute to effective light avoidance behaviors 15,17,21 . Thus, both behavioral and connectome studies indicate the structural and functional segregation of Rh5-and Rh6-PR pathways.…”

Section: Introductionmentioning

confidence: 99%

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Temporal control of inhibitionviamuscarinic acetylcholine receptor signaling generates ON and OFF selectivity in a simple visual circuit

Qin

Humberg

et al. 2019

Preprint

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ON and OFF selectivity in visual processing is encoded by parallel pathways that respond to either increments or decrements of light. Despite lacking anatomical features to support split channels, Drosophila larvae effectively perform visually-guided behaviors.To understand principles guiding visual computation in this simple circuit, we focus on the physiological properties and behavioral relevance of larval visual interneurons and elucidate their functions in visual processing. We find that the ON vs. OFF discrimination in the larval visual circuit emerges through light-elicited cholinergic signaling that depolarizes the cholinergic interneuron (cha-lOLP) and hyperpolarizes the glutamatergic interneuron (glu-lOLP). Genetic studies further indicate that muscarinic acetylcholine receptor (mAchR)/Gao signaling in glu-lOLP separates the ON and OFF signals through temporal delays, the disruption of which strongly impacts both physiological responses of downstream projection neurons and dark-induced pausing behavior. Together, our studies identify cellular and molecular substrates for OFF detection in the larval visual circuit and suggests temporal control of inhibition functions as an effective strategy in generating ON and OFF selectivity without anatomical segregation.

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Organization of the Drosophila larval visual circuit

Cited by 68 publications

References 104 publications

Drosophila glia: Few cell types and many conserved functions

Drosophila glia: Few cell types and many conserved functions

The complete connectome of a learning and memory center in an insect brain

Temporal control of inhibitionviamuscarinic acetylcholine receptor signaling generates ON and OFF selectivity in a simple visual circuit

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