Wiring visual systems: common and divergent mechanisms and principles

Kolodkin, Alex L.; Hiesinger, P. Robin

doi:10.1016/j.conb.2016.12.006

Cited by 26 publications

(25 citation statements)

References 61 publications

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“…Numerous studies have shown that neurons in ectopic locations readily form synapses with incorrect partners, including themselves 6,7,53 . On the other hand, Mi1, Mi4, C3, C2, Mi8, and Tm1 are all likely to express different cell surface proteins that may bias the likelihood of synaptic contacts 10,16,54 . Our data suggest that R7 terminals can form synapses with these incorrect partners simply by slowing down and stabilizing filopodial interactions.…”

Section: Discussionmentioning

confidence: 99%

“…Fly photoreceptors (R cells) are the primary retinal output neurons that relay visual information with highly stereotypic synaptic connections in dense brain regions, namely the lamina and medulla neuropils of the optic lobe [15][16][17] . Intact fly brains can develop in culture, enabling live imaging at the high spatiotemporal resolution necessary to measure photoreceptor axon filopodial dynamics and synapse formation throughout the entire developmental period of circuit assembly 13,14,18 .…”

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confidence: 99%

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Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

et al. 2020

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Brain wiring is remarkably precise, yet most neurons readily form synapses with incorrect partners when given the opportunity. Dynamic axon-dendritic positioning can restrict synaptogenic encounters, but the spatiotemporal interaction kinetics and their regulation remain essentially unknown inside developing brains. Here we show that the kinetics of axonal filopodia restrict synapse formation and partner choice for neurons that are not otherwise prevented from making incorrect synapses. Using 4D imaging in developing Drosophila brains, we show that filopodial kinetics are regulated by autophagy, a prevalent degradation mechanism whose role in brain development remains poorly understood. With surprising specificity, autophagosomes form in synaptogenic filopodia, followed by filopodial collapse. Altered autophagic degradation of synaptic building material quantitatively regulates synapse formation as shown by computational modeling and genetic experiments. Increased filopodial stability enables incorrect synaptic partnerships. Hence, filopodial autophagy restricts inappropriate partner choice through a process of kinetic exclusion that critically contributes to wiring specificity.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

et al. 2020

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“…Numerous studies have shown that neurons in ectopic locations readily form synapses with incorrect partners, including themselves 6,7,48 . On the other hand, Mi1, Mi4, C3, C2, Mi8 and Tm1 are likely to express cell surface proteins that bias the likelihood of synaptic contacts with R7 and other partners 10,16,49 . Axonal and dendritic interaction dynamics may greatly facilitate, or restrict, what partner neurons get ‘to see each other’ and initiate synapse formation based on molecular interactions 1 .…”

Section: Discussionmentioning

confidence: 99%

Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

Kiral

Linneweber

Georgiev

et al. 2019

Preprint

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11Brain wiring is remarkably precise, yet most neurons readily form synapses with 12 incorrect partners when given the opportunity. Dynamic axon-dendritic positioning can 13 restrict synaptogenic encounters, but the spatiotemporal interaction kinetics and their 14 regulation remain essentially unknown inside developing brains. Here we show that the 15 kinetics of axonal filopodia restrict synapse formation and partner choice for neurons that are 16 not otherwise prevented from making incorrect synapses. Using 4D imaging in developing 17 Drosophila brains, we show that filopodial kinetics are regulated by autophagy, a prevalent 18 degradation mechanism whose role in brain development remains poorly understood. With 19 surprising specificity, autophagosomes form in synaptogenic filopodia, followed by filopodial 20 collapse. Altered autophagic degradation of synaptic building material quantitatively 21 regulates synapse formation as shown by computational modeling and genetic experiments. 22Increased filopodial stability enables incorrect synaptic partnerships. Hence, filopodial 23 autophagy restricts inappropriate partner choice through a process of kinetic exclusion that 24 critically contributes to wiring specificity. 25 26 27 30 most, if not all, neurons have the ability to form synapses with incorrect partners, including 31 themselves 6,7 . During neural circuit development, spatiotemporal patterning restricts when 32 and where neurons 'see each other' [8][9][10] . Positional effects can thereby prevent incorrect 33 partnerships, even when neurons are not otherwise prevented from forming synapses 7,11,12 . 34 When and where neurons interact with each other to form synapses is a fundamentally 35 dynamic process. Yet, the roles of neuronal interaction dynamics, e.g. the speed or stability 36 of filopodial interactions, is almost completely unknown for dense brain regions in any 37 organism. Our limited understanding of the dynamics of synaptogenic encounters reflects the 38 2 difficulty to observe, live and in vivo, synapse formation at the level of filopodial dynamics in 39 intact, normally developing brains 13,14 . 40 Fly photoreceptors (R cells) are the primary retinal output neurons that relay visual 41 information with highly stereotypic synaptic connections in dense brain regions, namely the 42 lamina and medulla neuropils of the optic lobe [15][16][17] . Intact fly brains can develop in culture, 43 enabling live imaging at the high spatiotemporal resolution necessary to measure 44 photoreceptor axon filopodial dynamics and synapse formation throughout the entire 45 developmental period of circuit assembly 13,14,18 . Axonal filopodia inside the developing brain 46 stabilize to form synapses through the accumulation of synaptic building material, but how 47 limiting amounts of building material in filopodia are regulated is unknown 14 . 48Macroautophagy (autophagy hereafter) is a ubiquitous endomembrane degradation 49 mechanism implicated in neuronal maintenance and function 19 . Neuronal autoph...

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“…More importantly, he recognized the similarities between the neural circuits that underlie vision in vertebrates and flies (Cajal & Sanchez, 1915). Over the past few decades, structural, developmental and functional studies in these organisms have backed up Cajal's view (Kolodkin & Hiesinger, 2017;Sanes & Zipursky, 2010). This wealth of work suggests that conserved features are probably fundamental, and that knowledge obtained from one organism can provide insight into others.…”

Section: Introductionmentioning

confidence: 99%

“…In summary, in addition to open questions remaining, novel ones prompted by the progress made in the past decade will lead to further understanding of the mechanisms that regulate wiring. Moreover, given the similarities between the fly and the vertebrate visual systems (Kolodkin & Hiesinger, 2017;Sanes & Zipursky, 2010), it is expected that findings in both systems will continue to contribute in a complementary way to the identification of conserved developmental principles regulating the wiring of neural circuits. Layers were initially defined by the branching of neurons at specific location along the Z-axis of the medulla (Fischbach & Dittrich, 1989).…”

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confidence: 99%

Untangling the wiring of theDrosophilavisual system: developmental principles and molecular strategies

Plazaola‐Sasieta¹,

Fernández-Pineda

Zhu³

et al. 2017

Journal of Neurogenetics

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The assembly of neural circuits relies on the accurate establishment of connections between synaptic partners. Precise wiring results from responses that neurons elicit to environmental cues and cell-cell contact events during development. A common design principle in both invertebrate and vertebrate adult nervous systems is the orderly array of columnar and layered synaptic units of certain neuropils. This similarity is particularly striking in the visual system, both at the structural and cell-type levels. Given the powerful genetic approaches and tools available in Drosophila, the fly visual system has been extensively used to probe how specific wiring patterns are achieved during development. In this review, we cover the developmental principles and molecular strategies that govern the assembly of columnar units (lamina cartridges and medulla columns), the formation of layers, afferent specific layer selection, and synaptogenesis in Drosophila. The mechanisms include: sequential developmental steps that ensure coordinated assembly of synaptic partners; anterograde and autocrine signaling; interactions between cell-surface molecules, or secreted molecules and their receptors that take place among neurons; and glia signaling to neurons.

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Wiring visual systems: common and divergent mechanisms and principles

Cited by 26 publications

References 61 publications

Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

Autophagy-dependent filopodial kinetics restrict synaptic partner choice during Drosophila brain wiring

Untangling the wiring of theDrosophilavisual system: developmental principles and molecular strategies

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