Retrograde Plasticity and Differential Competition of Bipolar Cell Dendrites and Axons in the Developing Retina
Most neurons function in the context of pathways that process and propagate information through a series of stages, e.g., from the sensory periphery to cerebral cortex [1]. Because activity at each stage of a neural pathway depends on connectivity at the preceding one, we hypothesized that during de...
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| Published in: | Current biology 2014-10, Vol.24 (19), p.2301-2306 |
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| Main Authors: | , |
| Format: | Article |
| Language: | eng |
| Subjects: | |
| Online Access: | Get full text |
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| Summary: | Most neurons function in the context of pathways that process and propagate information through a series of stages, e.g., from the sensory periphery to cerebral cortex [1]. Because activity at each stage of a neural pathway depends on connectivity at the preceding one, we hypothesized that during development, axonal output of a neuron may regulate synaptic development of its dendrites (i.e., retrograde plasticity). Within pathways, neurons often receive input from multiple partners and provide output to targets shared with other neurons (i.e., convergence) [2]. Converging axons can intermingle or occupy separate territories on target dendrites. Activity-dependent competition has been shown to bias target innervation by overlapping axons in several systems [3–8]. By contrast, whether territorial axons or dendrites compete for targets and inputs, respectively, has not been tested. Here, we generate transgenic mice in which glutamate release from specific sets of retinal bipolar cells (BCs) is suppressed. We find that dendrites of silenced BCs recruit fewer inputs when their neighbors are active and that dendrites of active BCs recruit more inputs when their neighbors are silenced than either active or silenced BCs with equal neighbors. By contrast, axons of silenced BCs form fewer synapses with their targets, irrespective of the activity of their neighbors. These findings reveal that retrograde plasticity guides BC dendritic development in vivo and demonstrate that dendrites, but not territorial axons, in a convergent neural pathway engage in activity-dependent competition. We propose that at a population level, retrograde plasticity serves to maximize functional representation of inputs.
•Neurotransmission regulates synaptogenesis of territorial axons noncompetitively•Activity of BC axons regulates synaptic development of BC dendrites•Retrograde plasticity involves competition between dendrites of neighboring neurons•Retrograde plasticity may maximize functional input representation in neural pathways
Johnson and Kerschensteiner report that dendrites of developing neurons in the retina compete for synaptic inputs and that the outcome of dendritic competitions depends on retrograde signals elicited by axonal transmitter release. Retrograde control of dendritic development may serve to optimize functional representations along neuronal pathways. |
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| ISSN: | 0960-9822 1879-0445 |