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The Journal of Neuroscience, March 7, 2007, 27(10):2444-2456; doi:10.1523/JNEUROSCI.4434-06.2007

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Development/Plasticity/Repair
Cell-Autonomous TrkB Signaling in Presynaptic Retinal Ganglion Cells Mediates Axon Arbor Growth and Synapse Maturation during the Establishment of Retinotectal Synaptic Connectivity

Sonya Marshak,¹ Angeliki Maria Nikolakopoulou,¹ Ron Dirks,² Gerard J. Martens,² and Susana Cohen-Cory¹

¹Department of Neurobiology and Behavior, University of California, Irvine, Irvine, California 92697, and ²Department of Molecular Animal Physiology, Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen, 6525 GA Nijmegen, The Netherlands

Correspondence should be addressed to Dr. Susana Cohen-Cory, Department of Neurobiology and Behavior, University of California, Irvine, 2205 McGaugh Hall, Irvine, CA 92697-4550. Email: scohenco{at}uci.edu

BDNF contributes to the activity-dependent establishment and refinement of visual connectivity. In Xenopus, BDNF applications in the optic tectum influence retinal ganglion cell (RGC) axon branching and promote synapse formation and stabilization. The expression patterns of BDNF and TrkB suggest that BDNF specifically regulates the maturation of RGC axons at the target. It is possible, however, that BDNF modulates retinotectal synaptic connectivity by differentially influencing presynaptic RGC axons and postsynaptic tectal cells. Here, we combined single-cell expression of a dominant-negative TrkB–enhanced green fluorescent protein (GFP) fusion protein with confocal microscopy imaging in live Xenopus tadpoles to differentiate between presynaptic and postsynaptic actions of BDNF. Disruption of TrkB signaling in individual RGCs influenced the branching and synaptic maturation of presynaptic axon arbors. Specifically, GFP–TrkB.T1 overexpression increased the proportion of axons with immature, growth cone-like morphology, decreased axon branch stability, and increased axon arbor degeneration. In addition, GFP–TrkB.T1 overexpression reduced the number of red fluorescent protein–synaptobrevin-labeled presynaptic specializations per axon terminal. In contrast, overexpression of GFP–TrkB.T1 in tectal neurons did not alter synaptic number or the morphology or dynamic behavior of their dendritic arbors. Electron microscopy analysis revealed a significant decrease in the number of mature synaptic profiles and in the number of docked synaptic vesicles at retinotectal synapses made by RGC axons expressing GFP–TrkB.T1. Together, our results demonstrate that presynaptic TrkB signaling in RGCs is a key determinant in the establishment of visual connectivity and indicate that changes in tectal neuron synaptic connectivity are secondary to the BDNF-elicited enhanced stability and growth of presynaptic RGCs.

Key words: Xenopus laevis; synapse; axon; tectal neuron; in vivo imaging; transgenic

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Received Oct. 11, 2006; revised Jan. 12, 2007; accepted Jan. 23, 2007.

Correspondence should be addressed to Dr. Susana Cohen-Cory, Department of Neurobiology and Behavior, University of California, Irvine, 2205 McGaugh Hall, Irvine, CA 92697-4550. Email: scohenco{at}uci.edu

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