Segment-specific morphogenesis of leech Retzius neurons requires particular peripheral targets

Abstract

In most segments of the leech, a pair of Retzius (Rz) cells innervate the body wall musculature and skin; however, in the segments specialized for reproduction (midbody segments 5 and 6), these neurons innervate the reproductive tissue instead. Whereas all Rz cells have the same morphology early in embryogenesis, those in the reproductive segments [Rz(5,6)] become considerably different from their segmental homologs. Unlike standard Rz cells, Rz(5,6) do not have axons in the interganglionic connectives or in the body wall (Glover and Mason, 1986). Rz(5,6) also have significantly smaller somata and fewer branches in the ganglionic neuropil than do standard Rz cells (Jellies et al., 1987). Since these differences between Rz cells do not become apparent until after Rz(5,6) processes appear to contact the reproductive tissue primordia, interactions between Rz(5,6) processes and the reproductive tissue may determine the segmental specializations of these neurons. We have tested this possibility by ablating the reproductive tissue primordia early in embryogenesis and subsequently examining Rz(5,6) morphology. In the absence of reproductive tissue, Rz(5,6) became more like standard Rz cells: they retained axons in the interganglionic connectives, they projected into the body wall, and the density of their arborization within the neuropil increased. These results indicate that the development of some segmental specializations of Rz(5,6) involves an interaction with their unique target tissue.

Segmental differentiation in the leech nervous system: specific phenotypic changes associated with ectopic targets.

“…The lack of lateral N cells in ganglia associated with sex organs could be an example ofthis type ofmechanism. Another hypothesis supported by our observations, as well as those of Kristan and co-workers (26,27) on the development of the Retzius cells, is that segmental heterogeneity in targets leads to segmental differences in the properties of homologous neurons. The lack of expression by cell 158 of the antigens recognized by Laz1-1 and the modified branching of the Retzius cells in ganglia that innervate ectopic sex organs offer indications of the validity of this suggestion.…”

“…2 and 3), and exit through the lateral root nerves to innervate peripheral targets in body segments five and six, such as the body wall. The local Retzius cells in the sex ganglia appear to restrict their peripheral innervation largely to the sex organs (26,27).…”

“…Preliminary observations in animals in which sex organs have been ablated (C. Loer, private communication) indicate that such changes do not take place, for the most part, under these circumstances. Furthermore, transplantation of the sex organs to ectopic locations elicits innervation by the local Retzius cells, though whether their projection patterns are changed has yet to be assessed (27). It is thus reasonable to suggest that the target organs do play a role in the differentiation of specific aspects of the ganglionic phenotype.…”

Morphological plasticity of motor axons in Drosophila mutants with altered excitability

“…In recent years, however, studies of long-term physiological and anatomical changes in Aplysia during behav-ioral conditioning (Kandel et al, 1986;Bailey and Chen, 1988a,b), as well as studies of regeneration (Murphey and Lemere, 1984;Shepherd and Murphey, 1986;Loer et al, 1987;Loer and Kristan, 1989) have changed this view. Instead, it has become apparent that, even though the behavioral repertoire of invertebrates is less complex than that of vertebrates, developmental and physiological plasticity is a common feature (reviewed in Lnenicka and Murphey, 1989; see also Technau, 1984;Meinertzhagen, 1989).…”

Segmentation in Annelids: Cellular and Molecular Basis for Metameric Body Plan

“…For instance, in the leech Hirudo medicinalis, distinct patterns of cell morphology and synaptic contacts of the serotonergic Ratzius neurons in the genital segments devolve from interactions of the immature Retzius cell with the genital primordia (Loer et al, 1987;Loer and Kristan, 1989a, b). Similarly, segment-specific survival of distal tubule cells (which form the distal end of the nephridial tubule) in an ectodermal lineage in Helobdella is achieved via interactions with surrounding tissues, probably nephridial primordia (Martindale and Shankland, 1988).…”