Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination

Ting Wen Cheng, Xiao Bo Liu, Regina L. Faulkner, Alexander H. Stephan, Ben A. Barres, Andrew D. Huberman, Hwai-Jong Cheng

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)16376-16382
Number of pages7
JournalJournal of Neuroscience
Volume30
Issue number48
DOIs
StatePublished - Dec 1 2010

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Retinal Ganglion Cells
Synapses
Axons
Superior Colliculi
Neurons
Immunoelectron Microscopy
Presynaptic Terminals
Neuroglia
Nervous System
Mammals

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Cheng, T. W., Liu, X. B., Faulkner, R. L., Stephan, A. H., Barres, B. A., Huberman, A. D., & Cheng, H-J. (2010). Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination. Journal of Neuroscience, 30(48), 16376-16382. https://doi.org/10.1523/JNEUROSCI.3455-10.2010

Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination. / Cheng, Ting Wen; Liu, Xiao Bo; Faulkner, Regina L.; Stephan, Alexander H.; Barres, Ben A.; Huberman, Andrew D.; Cheng, Hwai-Jong.

In: Journal of Neuroscience, Vol. 30, No. 48, 01.12.2010, p. 16376-16382.

Research output: Contribution to journalArticle

Cheng, TW, Liu, XB, Faulkner, RL, Stephan, AH, Barres, BA, Huberman, AD & Cheng, H-J 2010, 'Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination', Journal of Neuroscience, vol. 30, no. 48, pp. 16376-16382. https://doi.org/10.1523/JNEUROSCI.3455-10.2010
Cheng, Ting Wen ; Liu, Xiao Bo ; Faulkner, Regina L. ; Stephan, Alexander H. ; Barres, Ben A. ; Huberman, Andrew D. ; Cheng, Hwai-Jong. / Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 48. pp. 16376-16382.
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