Design Principles of Insect and Vertebrate Visual Systems

Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
Neuron (Impact Factor: 15.05). 04/2010; 66(1):15-36. DOI: 10.1016/j.neuron.2010.01.018
Source: PubMed


A century ago, Cajal noted striking similarities between the neural circuits that underlie vision in vertebrates and flies. Over the past few decades, structural and functional studies have provided strong support for Cajal's view. In parallel, genetic studies have revealed some common molecular mechanisms controlling development of vertebrate and fly visual systems and suggested that they share a common evolutionary origin. Here, we review these shared features, focusing on the first several layers-retina, optic tectum (superior colliculus), and lateral geniculate nucleus in vertebrates; and retina, lamina, and medulla in fly. We argue that vertebrate and fly visual circuits utilize common design principles and that taking advantage of this phylogenetic conservation will speed progress in elucidating both functional strategies and developmental mechanisms, as has already occurred in other areas of neurobiology ranging from electrical signaling and synaptic plasticity to neurogenesis and axon guidance.

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    • "Neurons activated by light decrements (OFF) stratify in the outer two sublaminae (S1-S2), whereas neurons activated by light increments (ON) stratify in the inner three (S3-S5). Cell-type-specific lamination patterns of neurites at precise depths of the IPL restrict potential connectivity and thus contribute to the synaptic specificity of retinal circuits (Sanes and Zipursky, 2010; Masland, 2012). "
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    ABSTRACT: Photoreceptor degenerations are a major cause of blindness and among the most common forms of neurodegeneration in humans. Studies of mouse models revealed that synaptic dysfunction often precedes photoreceptor degeneration, and that abnormal synaptic input from photoreceptors to bipolar cells causes circuits in the inner retina to become hyperactive. Here, we provide a brief overview of frequently used mouse models of photoreceptor degenerations. We then discuss insights into circuit remodeling triggered by early synaptic dysfunction in the outer and hyperactivity in the inner retina. We discuss these insights in the context of other experimental manipulations of synaptic function and activity. Knowledge of the plasticity and early remodeling of retinal circuits will be critical for the design of successful vision rescue strategies.
    Frontiers in Cellular Neuroscience 10/2015; 9. DOI:10.3389/fncel.2015.00395 · 4.29 Impact Factor
    • "The retina is one of the best-understood mammalian circuits, where the neuronal connections in the primary image-forming pathway have been mapped and their functional relevance has been studied extensively (Hoon et al., 2014; Sanes and Zipursky, 2010). Vision in vertebrates is initiated by two types of photoreceptor neurons that respond to stimulation by light: rods and cones. "
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    ABSTRACT: In the retina, rod and cone photoreceptors form distinct connections with different classes of downstream bipolar cells. However, the molecular mechanisms responsible for their selective connectivity are unknown. Here we identify a cell-adhesion protein, ELFN1, to be essential for the formation of synapses between rods and rod ON-bipolar cells in the primary rod pathway. ELFN1 is expressed selectively in rods where it is targeted to the axonal terminals by the synaptic release machinery. At the synapse, ELFN1 binds in trans to mGluR6, the postsynaptic receptor on rod ON-bipolar cells. Elimination of ELFN1 in mice prevents the formation of synaptic contacts involving rods, but not cones, allowing a dissection of the contributions of primary and secondary rod pathways to retinal circuit function and vision. We conclude that ELFN1 is necessary for the selective wiring of rods into the primary rod pathway and is required for high sensitivity of vision.
    Neuron 09/2015; 87(6):1248-1260. DOI:10.1016/j.neuron.2015.09.002 · 15.05 Impact Factor
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    • "referred to as retinotopic map. Neurons of the medulla receive input from the retina and the lamina and are organized into columns and layers and project to the lobula and lobula plate (reviewed in Sanes and Zipursky, 2010). The genetic and cellular mechanisms of neurogenesis in the lobula and lobula plate have only recently been explored in greater detail. "
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    ABSTRACT: Brain development goes through phases of proliferative growth and differentiation to ensure the formation of correct number and variety of neurons. How and when naïve neuroepithelial cells decide to enter a differentiation pathway remains poorly understood. In the Drosophila visual system, four optic ganglia emerge from neuroepithelia of the inner (IPC) and outer (OPC) proliferation centers. Here we demonstrate that the orphan nuclear receptor Tailless (Tll) is a key factor for the development of all optic ganglia. We describe tll expression during larval optic lobe development in unprecedented detail and find a spatiotemporally dynamic pattern. In the larval OPC, symmetrically dividing neuroepithelial cells transform into asymmetrically dividing medulla neuroblast and into lamina precursor cells in a precisely regulated fashion. Using genetic manipulations we found that tll is required for proper neuroepithelium morphology and neuroepithelial cell survival. We show that tll regulates the precise timing of the transition from neuroepithelial cells to medulla neuroblasts. In particular, however, we demonstrate that tll has a crucial role for the specification of lamina precursor cells. We propose that the Tll/Tlx transcription factors have an evolutionary conserved role in regulating neural precursor cell states in the Drosophila optic lobe and in the mammalian retina. Copyright © 2015. Published by Elsevier Inc.
    Developmental Biology 06/2015; DOI:10.1016/j.ydbio.2015.06.011 · 3.55 Impact Factor
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