Color Discrimination with Broadband Photoreceptors

Schnaitmann, Christopher; Garbers, Christian; Wachtler, Thomas; Tanimoto, Hiromu

doi:10.1016/j.cub.2013.10.037

Cited by 130 publications

(167 citation statements)

References 38 publications

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“…The two types pattern the eye randomly (Bell et al, 2007) and presumably extend the spectral range of the retina (Morante and Desplan, 2008). Both R7 and R8 are required functionally to enable spectral preference and color vision (Gao et al, 2008;Schnaitmann et al, 2010Schnaitmann et al, , 2013Yamaguchi et al, 2010;Melnattur et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Mapping chromatic pathways in the Drosophila visual system

Lin

Luo

Shinomiya

et al. 2015

J of Comparative Neurology

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In Drosophila, color vision and wavelength-selective behaviors are mediated by the compound eye's narrow-spectrum photoreceptors, R7 and R8, and their downstream neurons, Tm5a/b/c and Tm20, in the second optic neuropil, or medulla. These chromatic Tm neurons project axons to a deeper optic neuropil, the lobula, which in insects has been implicated in processing and relaying color information to the central brain. The synaptic targets of the chromatic Tm neurons in the lobula are not known, however. Using a modified GRASP (GFP reconstitution across synaptic partners) method to probe connections between the chromatic Tm neurons and 28 known and novel types of lobula neurons, we identified anatomically the visual projection neurons LT11 and LC14, and the lobula intrinsic neurons Li3 and Li4, as synaptic targets of the chromatic Tm neurons. Single-cell GRASP analyses revealed that Li4 receives synaptic contacts from over 90% of all four types of chromatic Tm neurons while LT11 is postsynaptic to the chromatic Tm neurons with only modest selectivity and at a lower frequency and density. To visualize synaptic contacts at the ultrastructural level, we developed and applied a "two-tag" double labeling method to label LT11's dendrites and the mitochondria in Tm5c's presynaptic terminals. Serial electron microscopic reconstruction confirmed that LT11 receives direct contacts from Tm5c. This method would be generally applicable to map the connections of large complex neurons in Drosophila and other animals. Graphical Abstract CONFLICT OF INTERESTThe authors declare no conflicts of interest. ROLE OF AUTHORSAll authors had access to all data presented in this study. The authors accept responsibility for the integrity and accuracy of the data and data analysis. Study concept and design: TYL, CHL, IAM. Preparation and acquisition of data: TYL, JL, KS, CYT, ZL. Analysis and interpretation of data: TYL, CHL. Drafting of the manuscript: TYL, IAM, CHL. Using trans-synaptic tracing and ultrastructural "two-tag" double-labeling approaches for EM, the authors identify synaptic targets of first-order chromatic interneurons in the deep visual processing center, the lobula. Lobula intrinsic neuron Li4 and projection neuron LT11 receive parallel chromatic inputs but with differential synaptic densities. HHS Public Access

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Section: Introductionmentioning

confidence: 99%

Mapping chromatic pathways in the Drosophila visual system

Lin

Luo

Shinomiya

et al. 2015

J of Comparative Neurology

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“…Based on their rhodopsin expression, ''pale'' and ''yellow'' R7 and R8 transmit information of different chromatic content to the optic lobes, where comparison between R7 and R8 activity from the same ommatidium as well as comparison between neighboring ommatidia lead to color discrimination (Gao et al 2008;Morante and Desplan 2008;Yamaguchi et al 2010;Schnaitmann et al 2013;Melnattur et al 2014). Do postsynaptic elements receive input from all ommatidia regardless of their ''pale'' and ''yellow'' fates, extracting information through a population code?…”

Section: The Organization Of the Drosophila Visual Systemmentioning

confidence: 99%

“…This was supported by behavior experiments using inactivated R1-6 or R7 and R8 photoreceptors (Heisenberg and Buchner 1977;Yamaguchi et al 2010). However, recent results have revealed rather unexpected retinal contributions to different visual behaviors: Color photoreceptor R8 has been implicated in the detection of motion (Wardill et al 2012), while achromatic R1-6 appear to play a role in the detection of color (Schnaitmann et al 2013) and linearly polarized reflections (Wernet et al 2012). Hence, the complex interactions between those photoreceptor cells projecting to the lamina part of the optic lobes (R1-6) and those projecting to the medulla (R7 and R8) indicate that functional separation between these subtypes is far less absolute than previously assumed and that information about different visual qualities like color and motion begins to be integrated at a very early stage.…”

Section: Genetic Dissection Of the Behavioral Contributions By Cell Tmentioning

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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“…The outer photoreceptors, R1-R6, express the broad spectrum-detecting Rhodopsin 1 (Rh1; also known as NinaE) and function in motion detection (Heisenberg and Buchner, 1977;Yamaguchi et al, 2008;Wardill et al, 2012). The inner photoreceptors, R7 and R8, are specialized for color vision, with some contribution from R1-R6 (Schnaitmann et al, 2013). Though morphologically uniform, the fly eye is composed of two main types of ommatidia defined by expression of color-sensing Rhodopsins (Rhs) in the inner photoreceptors .…”

Section: Introductionmentioning

confidence: 99%

The BEAF-32 insulator protein is required for Hippo pathway activity in the terminal differentiation of neuronal subtypes

et al. 2016

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The Hippo pathway is crucial for not only normal growth and apoptosis but also cell fate specification during development. What controls Hippo pathway activity during cell fate specification is incompletely understood. In this article, we identify the insulator protein BEAF-32 as a regulator of Hippo pathway activity in Drosophila photoreceptor differentiation. Though morphologically uniform, the fly eye is composed of two subtypes of R8 photoreceptor neurons defined by expression of light-detecting Rhodopsin proteins. In one R8 subtype, active Hippo signaling induces Rhodopsin 6 (Rh6) and represses Rhodopsin 5 (Rh5), whereas in the other subtype, inactive Hippo signaling induces Rh5 and represses Rh6. The activity state of the Hippo pathway in R8 cells is determined by the expression of warts, a core pathway kinase, which interacts with the growth regulator melted in a doublenegative feedback loop. We show that BEAF-32 is required for expression of warts and repression of melted. Furthermore, BEAF-32 plays a second role downstream of Warts to induce Rh6 and prevent Rh5 fate. BEAF-32 is dispensable for Warts feedback, indicating that BEAF-32 differentially regulates warts and Rhodopsins. Loss of BEAF-32 does not noticeably impair the functions of the Hippo pathway in eye growth regulation. Our study identifies a context-specific regulator of Hippo pathway activity in post-mitotic neuronal fate, and reveals a developmentally specific role for a broadly expressed insulator protein.

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Color Discrimination with Broadband Photoreceptors

Abstract: Our findings show that receptors with a complex and broad spectral sensitivity can contribute to color vision and reveal that chromatic and achromatic circuits in the fly share common photoreceptors.

Cited by 130 publications

References 38 publications

Mapping chromatic pathways in the Drosophila visual system

Mapping chromatic pathways in the Drosophila visual system

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

The BEAF-32 insulator protein is required for Hippo pathway activity in the terminal differentiation of neuronal subtypes

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