Abstract
Neurons receive input from diverse afferents but form stereotypic connections with each axon type to execute their precise functions. Developmental mechanisms that specify the connectivity of individual axons across populations of converging afferents are not well-understood. Here, we untangled the contributions of activity-dependent and independent interactions that regulate the connectivity of afferents providing major and minor input onto a neuron. Individual transmission-deficient retinal bipolar cells (BCs) reduced synapses with retinal ganglion cells (RGCs), but active BCs of the same type sharing the dendrite surprisingly did not compensate for this loss. Genetic ablation of some BC neighbors resulted in increased synaptogenesis by the remaining axons in a transmission-independent manner. Presence, but not transmission, of the major BC input also dissuades wiring with the minor input and with synaptically compatible but functionally mismatched afferents. Cell-autonomous, activity-dependent and nonautonomous, activity-independent mechanisms thus together tailor connectivity of individual axons among converging inner retinal afferents.
Copyright © 2014 Elsevier Inc. All rights reserved.
Publication types
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Research Support, N.I.H., Extramural
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Research Support, Non-U.S. Gov't
MeSH terms
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Animals
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Animals, Newborn
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Axons / physiology*
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Cell Communication / genetics
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Cell Communication / physiology*
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Disks Large Homolog 4 Protein
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Gene Expression Regulation, Developmental / genetics
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Guanylate Kinases / metabolism
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Luminescent Proteins / genetics
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Membrane Proteins / metabolism
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Metalloendopeptidases / genetics
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Metalloendopeptidases / metabolism
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Mice
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Mice, Transgenic
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Nerve Net / physiology*
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Nerve Tissue Proteins / metabolism
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Receptors, Metabotropic Glutamate / deficiency
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Receptors, Metabotropic Glutamate / metabolism
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Retina / cytology
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Retinal Bipolar Cells / cytology
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Retinal Bipolar Cells / physiology*
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Synapses / metabolism*
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Tetanus Toxin / genetics
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Tetanus Toxin / metabolism
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Vesicle-Associated Membrane Protein 2 / metabolism
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Visual Pathways / physiology
Substances
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Disks Large Homolog 4 Protein
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Dlg4 protein, mouse
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Luminescent Proteins
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Membrane Proteins
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Nerve Tissue Proteins
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Receptors, Metabotropic Glutamate
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Tetanus Toxin
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Vesicle-Associated Membrane Protein 2
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metabotropic glutamate receptor 6
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vesicle-associated membrane protein 2, mouse
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Guanylate Kinases
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Metalloendopeptidases
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zinc-endopeptidase, tetanus neurotoxin