Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination
Open accessAbstract
Throughout the nervous system, neurons restrict their connections to specific depths or “layers” of their targets to constrain the type and number of synapses they make. Despite the importance of lamina-specific synaptic connectivity, the mechanisms that give rise to this feature in mammals remain poorly understood. Here we examined the cellular events underlying the formation of lamina-specific retinal ganglion cell (RGC) axonal projections to the superior colliculus (SC) of the mouse. By combining a genetically encoded marker of a defined RGC subtype (OFF-αRGCs) with serial immunoelectron microscopy, we resolved the ultrastructure of axon terminals fated for laminar stabilization versus those fated for removal. We found that OFF-αRGCs form synapses across the full depth of the retinorecipient SC before undergoing lamina-specific arbor retraction and synapse elimination to arrive at their mature, restricted pattern of connectivity. Interestingly, we did not observe evidence of axon degeneration or glia-induced synapse engulfment during this process. These findings indicate that lamina-specific visual connections are generated through the selective stabilization of correctly targeted axon arbors and suggest that the decision to maintain or eliminate an axonal projection reflects the molecular compatibility of presynaptic and postsynaptic neurons at a given laminar depth.
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In at least one other developing system, local axonal retraction and synapse elimination appear to occur independent of microglia.
“While in at least one other developing system local axonal retraction and synapse elimination appear to occur independent of microglia (Cheng et al., 2010), recent work describes a role for microglia at developing hippocampal synapses (Paolicelli et al., 2011).”
From Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner (2012) · cites this paper as Cheng et al., 2010
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- Authors
- Cheng, T.-W., Liu, X.-B., Faulkner, R. L., Stephan, A. H., Barres, B. A., Huberman, A. D., & Cheng, H.-J.
- Affiliations
- University of California, Davis (US)
- Stanford Medicine (US)
- University of California San Diego (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-12-01
- Volume
- 30
- Issue
- 48
- Pages
- 16376-16382
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3073606
- OpenAlex
- W2064249418
- Cited by
- 22
- References
- 27
- Citations by year
- 2023: 2 · 2022: 2 · 2021: 1 · 2020: 1 · 2019: 3 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 1 · 2014: 1 · 2013: 1 · 2012: 2
- FWCI
- 0.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (R01DA015043, R37DA015043, DA15043)
- National Eye Institute (R01EY011310, R21EY018320, EY11310)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD045757, HD045757)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- retinal ganglion cells, superior colliculus, synaptic pruning, mice
- MeSH terms
- Animals, Animals, Newborn, Axons, Basement Membrane, Neural Pathways, Retinal Ganglion Cells, Synapses, Visual Pathways, Mice, Knockout, Mice
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