Abstract
The assembly of a nervous system requires the extension of axons and dendrites to specific regions where they are matched with appropriate synaptic targets. Although the cues that guide long-range outgrowth have been characterized extensively, additional mechanisms are required to explain short-range guidance in neural development. Using a complementary combination of time-lapse imaging by fluorescence confocal microscopy and serial block-face electron microscopy, we identified a novel type of presynaptic projection that participates in the assembly of the vertebrate nervous system. Synapse formation by each hair cell of the zebrafish's lateral line occurs during a particular interval after the cell's birth. During the same period, projections emerge from the cellular soma, extending toward a specific subpopulation of mature hair cells and interacting with polarity-specific afferent nerve terminals. The terminals then extend along the projections to reach appropriately matched presynaptic sites, after which the projections recede. Our results suggest that presynaptic projections act as transient scaffolds for short-range partner matching, a mechanism that may occur elsewhere in the nervous system.
Highlights
Like many other aquatic vertebrates, zebrafish possess lateral line organs that sense water currents (Metcalfe et al 1985)
By using fluorescence confocal microscopy to observe newly arisen hair cells and afferent fibers during the 20 h following mitosis, we found that hair cells made minimal contacts with axons during rearrangement and completed the process without stably associating with afferent terminals
In order to determine whether hair cells make polarity-specific synapses from the outset, we investigated three-dimensional reconstructions of neuromasts by serial block-face electron microscopy (SBEM) (Supplemental Fig. S1; Supplemental Movie 1; Denk and Horstmann 2004)
Summary
Like many other aquatic vertebrates, zebrafish possess lateral line organs that sense water currents (Metcalfe et al 1985). In order to determine whether hair cells make polarity-specific synapses from the outset, we investigated three-dimensional reconstructions of neuromasts by serial block-face electron microscopy (SBEM) (Supplemental Fig. S1; Supplemental Movie 1; Denk and Horstmann 2004). Time-lapse imaging of nascent hair cells during the period of synaptogenesis revealed striking projections that protruded from the base of each soma (Fig. 2A; Supplemental Movies 2,3).
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