A combinatorial code of transcription factors specifies subtypes of visual motion-sensing neurons in <i>Drosophila</i>

Hörmann, Nikolai; Schilling, Tabea; Ali, Aicha Haji; Serbe, Étienne; Mayer, Christian; Borst, Alexander; Pujol-Martí, Jesús

doi:10.1242/dev.186296

Cited by 20 publications

(24 citation statements)

References 65 publications

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“…Two recent articles showed the transcriptional profiling during several stages of pupal development of all eight subtypes of T4/T5 neurons (named a, b, c and d), showing that a specific combination of transcription factors define the identity of each subtype ( Hormann et al, 2020 ; Kurmangaliyev et al, 2019 ). Kurmangaliyev et al, using a single-cell RNA sequencing, found an enrichment of Robo2 in T4/T5 neurons of the c and d types.…”

Section: Discussionmentioning

confidence: 99%

Slit/Robo Signaling Regulates Multiple Stages of the Development of the Drosophila Motion Detection System

Guzmán-Palma

Contreras

Mora

et al. 2021

Front. Cell Dev. Biol.

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Neurogenesis is achieved through a sequence of steps that include specification and differentiation of progenitors into mature neurons. Frequently, precursors migrate to distinct positions before terminal differentiation. The Slit-Robo pathway, formed by the secreted ligand Slit and its membrane bound receptor Robo, was first discovered as a regulator of axonal growth. However, today, it is accepted that this pathway can regulate different cellular processes even outside the nervous system. Since most of the studies performed in the nervous system have been focused on axonal and dendritic growth, it is less clear how versatile is this signaling pathway in the developing nervous system. Here we describe the participation of the Slit-Robo pathway in the development of motion sensitive neurons of the Drosophila visual system. We show that Slit and Robo receptors are expressed in different stages during the neurogenesis of motion sensitive neurons. Furthermore, we find that Slit and Robo regulate multiple aspects of their development including neuronal precursor migration, cell segregation between neural stem cells and daughter cells and formation of their connectivity pattern. Specifically, loss of function of slit or robo receptors in differentiated motion sensitive neurons impairs dendritic targeting, while knocking down robo receptors in migratory progenitors or neural stem cells leads to structural defects in the adult optic lobe neuropil, caused by migration and cell segregation defects during larval development. Thus, our work reveals the co-option of the Slit-Robo signaling pathway in distinct developmental stages of a neural lineage.

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Section: Discussionmentioning

confidence: 99%

Slit/Robo Signaling Regulates Multiple Stages of the Development of the Drosophila Motion Detection System

Guzmán-Palma

Contreras

Mora

et al. 2021

Front. Cell Dev. Biol.

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“…Which receptors receive this repertoire of different neurotransmitters at the level of T4/T5 dendrites? Recently, several RNA-sequencing studies described the gene expression pattern of nearly all cell-types in the optic lobe of the fruit fly including T4/T5 neurons ( Pankova and Borst, 2016 ; Konstantinides et al, 2018 ; Davis et al, 2020 ; Hörmann et al, 2020 ). T4/T5 neurons were found to express numerous receptor subunits of different transmitter classes and voltage-gated ion channels at various expression strengths.…”

Section: Introductionmentioning

confidence: 99%

Conditional protein tagging methods reveal highly specific subcellular distribution of ion channels in motion-sensing neurons

Fendl

Vieira

Borst

2020

eLife

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Neurotransmitter receptors and ion channels shape the biophysical properties of neurons, from the sign of the response mediated by neurotransmitter receptors to the dynamics shaped by voltage-gated ion channels. Therefore, knowing the localizations and types of receptors and channels present in neurons is fundamental to our understanding of neural computation. Here, we developed two approaches to visualize the subcellular localization of specific proteins in Drosophila: The flippase-dependent expression of GFP-tagged receptor subunits in single neurons and 'FlpTag', a versatile new tool for the conditional labelling of endogenous proteins. Using these methods, we investigated the subcellular distribution of the receptors GluClα, Rdl, and Dα7 and the ion channels para and Ih in motion-sensing T4/T5 neurons of the Drosophila visual system. We discovered a strictly segregated subcellular distribution of these proteins and a sequential spatial arrangement of glutamate, acetylcholine, and GABA receptors along the dendrite that matched the previously reported EM-reconstructed synapse distributions.

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“…Individual directional preference of a T4/T5 neuron correlates with its dendrite orientation, which manifests during development(34–36). Interestingly, developmental dendrite orientation for subtypes A and B reveal two peaks of diagonal rather than orthogonal orientation of dendrites(36), consistent with their distribution of direction selectivity. Our data show that each T4/T5 subtype retinotopically covers overlapping regions in visual space.…”

Section: Discussionmentioning

confidence: 99%

“…A comprehensive analysis of T4/T5 dendrite anatomy across the visual system will be needed to clarify how adult dendrite orientation is distributed across the visual system to represent the six subtypes. Furthermore, single-cell transcriptomics has assigned developing T4/T5 cells to distinct clusters based on their genetic profiles(36–39), but genes involved in dendrite development or the differentiation are expressed in narrow time windows(39). Interestingly, one recent study identified a genetic subpopulation of T4 neurons, restricted to lobula plate layers A and B(37).…”

Section: Discussionmentioning

confidence: 99%

An optimal population code for global motion estimation in local direction-selective cells

Henning

Ramos-Traslosheros

Gür

et al. 2021

Preprint

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Nervous systems allocate computational resources to match stimulus statistics. However, the physical information that needs to be processed depends on the animal's own behavior. For example, visual motion patterns induced by self-motion provide essential information for navigation. How behavioral constraints affect neural processing is not known. Here we show that, at the population level, local direction-selective T4/T5 neurons in Drosophila represent optic flow fields generated by self-motion, reminiscent to a population code in retinal ganglion cells in vertebrates. Whereas in vertebrates four different cell types encode different optic flow fields, the four uniformly tuned T4/T5 subtypes described previously represent a local snapshot. As a population, six T4/T5 subtypes encode different axes of self-motion. This representation might serve to efficiently encode more complex flow fields generated during flight. Thus, a population code for optic flow appears to be a general coding principle of visual systems, but matching the animal's individual ethological constraints.

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A combinatorial code of transcription factors specifies subtypes of visual motion-sensing neurons in Drosophila

Abstract: We identify a combinatorial code of transcription factors that controls the development of subtypespecific morphologies in motion-detecting neurons of the fruit fly visual system.

Cited by 20 publications

References 65 publications

Slit/Robo Signaling Regulates Multiple Stages of the Development of the Drosophila Motion Detection System

Slit/Robo Signaling Regulates Multiple Stages of the Development of the Drosophila Motion Detection System

Conditional protein tagging methods reveal highly specific subcellular distribution of ion channels in motion-sensing neurons

An optimal population code for global motion estimation in local direction-selective cells

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