A temporal mechanism that produces neuronal diversity in the Drosophila visual center

Suzuki, Takumi; Kaido, Masako; Takayama, Rie; Sato, Makoto

doi:10.1016/j.ydbio.2013.05.002

Cited by 112 publications

(154 citation statements)

References 34 publications

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“…1C,D). hth expression is detected in medulla neuroblasts and neurons, in the NE progenitors (Reddy et al, 2010;Hasegawa et al, 2011;Morante et al, 2011;Li et al, 2013;Suzuki et al, 2013) and also within the posterior slope of the LF (Fig. 1D,E,F).…”

Section: Resultsmentioning

confidence: 91%

A conserved transcriptional network regulates lamina development in the Drosophila visual system

2014

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The visual system of insects is a multilayered structure composed externally by the compound eye and internally by the three ganglia of the optic lobe: lamina, medulla and the lobula complex. The differentiation of lamina neurons depends heavily on Hedgehog (Hh) signaling, which is delivered by the incoming photoreceptor axons, and occurs in a wave-like fashion. Despite the primary role of lamina neurons in visual perception, it is still unclear how these neurons are specified from neuroepithelial (NE) progenitors. Here we show that a homothorax (hth)-eyes absent (eya)-sine oculis (so)-dachshund (dac) gene regulatory cassette is involved in this specification. Lamina neurons differentiate from NE progenitors that express hth, eya and so. One of the first events in the differentiation of lamina neurons is the upregulation of dac expression in response to Hh signaling. We show that this dac upregulation, which marks the transition from NE progenitors into lamina precursors, also requires Eya/So, the expression of which is locked in by mutual feedback. dac expression is crucial for lamina differentiation because it ensures repression of hth, a negative regulator of single-minded, and thus dac allows further lamina neuron differentiation. Therefore, the specification of lamina neurons is controlled by coupling the cell-autonomous hth-eya-so-dac regulatory cassette to Hh signaling.

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Section: Resultsmentioning

confidence: 91%

A conserved transcriptional network regulates lamina development in the Drosophila visual system

2014

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“…Highlighting that temporal patterning of NBs constitutes a general principle, while the contributing factors vary, recent studies uncovered that medulla NBs rely on their own distinct cascade of temporal identity transcription factors (Li et al, 2013a;Li et al, 2013b;Suzuki et al, 2013): they sequentially express Homothorax (Hth), Klumpfuss (Klu), Ey, Sloppy paired 1 and 2 (Slp), Dichaete (D), and Tailless (Tll) with increasing age (Figure 4A). Unlike in the embryo new medulla NBs are still added, while the already existing ones transition through the temporal cascade and each express one or two overlapping transcription factors depending on their age.…”

Section: Temporal Patterningmentioning

confidence: 99%

“…slp is essential for repression of Ey, while D inhibits Slp. Over-expression of Hth, Ey, Slp1 and 2, or D is not sufficient to induce the next temporal identity factor, and tll is sufficient but not required to repress D. Thus, additional so far unidentified determinants must act in concert with the temporal identity factors to control the timely transitions (Li et al, 2013b;Suzuki et al, 2013).…”

Section: Temporal Patterningmentioning

confidence: 99%

“…With the exception of Klu, which is solely expressed in NBs (Suzuki et al, 2013), temporal identity factors are inherited by GMCs and by a subset of their progeny born in a specific time window. To further increase the diversity of potential subtypes, a second fundamental strategy comes into play, which relies on Notch-dependent binary fate decisions (Li et al, 2013b).…”

Section: Binary Fate Choices By Asymmetric Notch Signalingmentioning

confidence: 99%

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A Challenge of Numbers and Diversity: Neurogenesis in theDrosophilaOptic Lobe

Apitz¹,

Salecker²

2014

Journal of Neurogenetics

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The brain areas that endow insects with the ability to see consist of remarkably complex neural circuits. Reiterated arrays of many diverse neuron subtypes are assembled into modular yet coherent functional retinotopic maps. Tremendous progress in developing genetic tools and cellular markers over the past years advanced our understanding of the mechanisms that control the stepwise production and differentiation of neurons in the visual system of Drosophila melanogaster. The postembryonic optic lobe utilizes at least two modes of neurogenesis that are distinct from other parts of the fly central nervous system. In the first optic ganglion, the lamina, neuroepithelial cells give rise to precursor cells, whose proliferation and differentiation depend on anterograde signals from photoreceptor axons. In the second optic ganglion, the medulla, the coordinated activity of four signaling pathways orchestrates the gradual conversion of neuroepithelial cells into neuroblasts, while a specific cascade of temporal identity transcription factors controls subtype diversification of their progeny.

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“…However, this has now been addressed systematically in several new studies, leading to a description of how cellular diversity in the fly visual system is generated (Li et al 2013a;Suzuki et al 2013;Bertet et al 2014; for review, see Li et al 2013b). The mechanisms of neuronal specification in the medulla neuropil share surprising similarities with that of the fly embryonic ventral nerve cord, where each neural stem cell (called a neuroblast [NB]) expresses sequentially a series of transcription factors ( Fig.…”

Section: The Organization Of the Drosophila Visual Systemmentioning

confidence: 99%

So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice

2014

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The visual system is a powerful model for probing the development, connectivity, and function of neural circuits. Two genetically tractable species, mice and flies, are together providing a great deal of understanding of these processes. Current efforts focus on integrating knowledge gained from three cross-fostering fields of research: (1) understanding how the fates of different cell types are specified during development, (2) revealing the synaptic connections between identified cell types (''connectomics'') by high-resolution three-dimensional circuit anatomy, and (3) causal testing of how identified circuit elements contribute to visual perception and behavior. Here we discuss representative examples from fly and mouse models to illustrate the ongoing success of this tripartite strategy, focusing on the ways it is enhancing our understanding of visual processing and other sensory systems.For many decades, the visual systems of both vertebrates and invertebrates have been a favorite arena for understanding how neural circuits are built and function. A considerable body of work has focused on the specification of cell types of the retina; for instance, the designation of different classes of photoreceptors with distinct spectral sensitivities in the Drosophila retina (Rister and Desplan 2011) and the establishment of the various cell types that comprise the vertebrate retina: photoreceptors, Muller glia, interneurons (horizontal, amacrine, and bipolar cells), and retinal ganglion cells (RGCs) (Livesey and Cepko 2001;Mu et al. 2004;Poch e and Reese 2006). With that knowledge in hand, focus in recent years has expanded to understanding how the circuits formed by these retinal cells are linked to the staggering number of diverse visual neurons in the brain, which in turn enables sophisticated and diverse computational tasks. The ultimate goal is to understand how cellular identity, function, and connectivity relate to visually guided behaviors. (Fig. 1A).

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A temporal mechanism that produces neuronal diversity in the Drosophila visual center

Cited by 112 publications

References 34 publications

A conserved transcriptional network regulates lamina development in the Drosophila visual system

A conserved transcriptional network regulates lamina development in the Drosophila visual system

A Challenge of Numbers and Diversity: Neurogenesis in theDrosophilaOptic Lobe

So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice

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