The cellular mechanisms underlying axogenesis and dendritogenesis are not completely understood. The axons and dendrites of retinal bipolar cells, which contact their synaptic partners within specific laminae in the inner and outer retina, provide a good system for exploring these issues. Using transgenic mice expressing enhanced green fluorescent protein (GFP) in a subset of bipolar cells, we determined that axonal and dendritic arbors of these interneurons develop directly from apical and basal processes attached to the outer and inner limiting membranes, respectively. Selective stabilization of processes contributed to stratification of axonal and dendritic arbors within the appropriate synaptic layer. This unusual mode of axogenesis and dendritogenesis from neuroepithelial-like processes may act to preserve neighbor-neighbor relationships in synaptic wiring between the outer and inner retina.
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We thank R.F. Margolskee and R.H. Masland for providing the GUS8.4-GFP mice. This work is supported by grants from the US National Institutes of Health (EY10699 to R.O.L.W. and EY11105 to N.V.) and the Bakewell and Alafi Neuroimaging Laboratories.
3D rotation of a confocal stack from a P3 Grm6-GFP retinal cross-section. In this region, a GFP positive bipolar axon terminal can be distinguished from the relatively dimmer IPL processes of neighboring amacrine cells and RGCs upon rotation of the image stack. For example, a GFP-labeled process (arrow 2) that appears close to the bipolar cell axon (arrow 1) in the initial frame, clearly moves apart from the axon in subsequent frames when the stack is rotated. Here, we have also highlighted the bipolar axon and its fine terminals in white using the 3D segmentation program in Amira, to provide a high contrast view of the axon. Inner nuclear layer (INL), inner plexiform layer (IPL), ganglion cell layer (GCL).
Time-lapse showing process motility in some axonal arbors of P6 bipolar cells in the Grm6-GFP mouse retina (confocal image stacks, 7 time frames, 30 min between frames). Note extensions and retractions that are particularly evident in the bright axon.
3D confocal reconstruction of P10 Grm6-GFP retina showing extensions of bipolar cell axons into the ganglion cell layer (GCL), some of which retracted during the recording period. The boundaries of the inner plexiform layer (IPL) and inner nuclear layer (INL) are provided. In the first segment of the movie, the image stack is cropped and rotated in 3D to provide a clearer view of the morphology of the processes within the GCL. In the second segment, the retraction of an axonal terminal (middle of the field of view) in the GCL is apparent in a zoomed up view of this region (7 time points, 20 min between frames).
Movie showing process extension and retraction from the apical process of the cell shown in Fig. 6b (7 frames, 20 min between frames). Outer nuclear layer (ONL), outer plexiform layer (OPL); inner nuclear layer (INL).
About this article
Science China Life Sciences (2010)