Segmental variation in identified neurons may provide an opportunity to examine extrinsic influences on neuronal phenotype, since segmentally homologous neurons must contain much the same intrinsic information, having arisen from very similar or identical precursors. Two large serotonergic Retzius (Rz) cells are found in each segmental ganglion of the leech Hirudo medicinalis. While most Rz cells innervate the body wall in their own segment and, by way of axons in the interganglionic connectives, the body wall of adjacent segments, the Rz cells in ganglia 5 and 6 [Rz(5,6)] lack interganglionic axons and innervate only the reproductive tissue (Glover and Mason, 1986). Here we describe and quantify the development of differences between Rz(5,6) and other Rz cells in peripheral innervation, neuropilar arborization, and soma size. We filled individual Rz cells with Lucifer yellow or HRP in adults and in staged embryos. During the first 72 hr of outgrowth of Rz cell processes, the morphology of Rz(5,6) was indistinguishable from that of other Rz cells. Only after the processes of Rz(5,6) reached the reproductive tissue did they begin to differ from their segmental homologs. This temporal correlation suggests that these morphological differences arise because of some interaction between Rz(5,6) and their target tissue.
A pair of large serotonergic neurons, the Retzius (Rz) cells, is found in each segment of the leech nervous system. Most Rz cells innervate the body wall of their own segment as well as adjacent anterior and posterior segments. Rz cells in segments 5 and 6 [Rz (5,6)] instead innervate the reproductive tissue found only in those segments. Rz cells from adjacent segments [Rz (4,7)] provide the serotonergic innervation of the body wall of segments 5 and 6. During embryogenesis, the body wall and the reproductive tissue are apparently available to both Rz (5,6) and Rz (4,7), yet these neurons choose different targets. We asked how Rz (5,6) and Rz (4,7) choose their respective peripheral targets in the reproductive segments by ablating either the reproductive tissue or specific Rz cells. Ablation of the reproductive tissue caused Rz (5,6) to innervate body wall, although not as proficiently as did standard Rz cells, suggesting a preference of Rz (5,6) for reproductive tissue. Ablation of those Rz cells that would normally innervate the body wall of segments 5 and 6 did not cause Rz (5,6) to innervate body wall, ruling out competition for this target. When Rz (5,6) were ablated, Rz (4,7) innervated the body wall of segments 5 and 6 normally and did not innervate reproductive tissue. Thus, competition did not act in the choice of target by Rz (4,7) either. These results suggest that during normal development, Rz (5,6) and Rz (4,7) choose their targets independently of one another rather than competing for the available targets and that these cells have segment-specific target preferences.
Most Retzius (Rz) cells innervate the body wall of their own and adjacent segments, whereas Rz cells in segments 5 and 6 [Rz (5,6)] innervate the reproductive tissue, which is found only in those segments. Results from the preceding paper (Loer and Kristan, 1989a) showed that Rz (5,6) and standard Rz cells do not normally compete for their respective peripheral targets. These experiments did not, however, distinguish between 2 other possible mechanisms of target selection: intrinsic differences in target preference or differences in the timing of target contact. In order to separate these possibilities experimentally, we transplanted reproductive primordia to standard segments. We found that standard Rz cells were capable of densely innervating ectopic reproductive tissue, provided the target was transplanted at an appropriate time and location. Furthermore, after some processes of standard Rz cells contacted ectopic reproductive tissue, the rest of the cell's processes showed their growth in a way reminiscent of Rz (5,6) processes. These results strongly suggest that Rz (5,6) innervate reproductive tissue at least partly because their processes contact this target during a period that is optimal for them to associate with the target, or when the reproductive tissue is most attractive to Rz processes, or both.
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