Morphological changes in leech Retzius neurons after target contact during embryogenesis

Abstract

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.

Competition among the Axonal Projections of an Identified Neuron Contributes to the Retraction of Some of Those Projections

“…Several leech neurons, other than the AP cell, trim some of their processes as well (Wallace, 1984;Glover and Mason, 1986;Gao and Macagno, 1987a,b;Jellies et al, 1987;Baptista and Macagno, 1988;Elsas et al, 1995). The selective retraction of some branches generally seems to occur at the same time as sibling branches are maintained or are growing extensively.…”

“…In establishing their particular branching patterns, neurons often generate some neurites that are later retracted (Land and Lund, 1979;Innocenti, 1981;O'Leary et al, 1981;McLoon, 1982;Wallace, 1984;Stanfield and O'Leary, 1985;Glover and Mason, 1986;Gao and Macagno, 1987a,b;Jellies et al, 1987;Baptista and Macagno, 1988;Callaway and Katz, 1990;O'Rourke et al, 1994). Synapse elimination at the neuromuscular junction (Redfern, 1970;Balice-Gordon and Lichtman, 1993) and the segregation of LGN projections to the visual cortex in the formation of ocular dominance column (LeVay et al, 1978(LeVay et al, , 1980 are well known examples of this phenomenon.…”

“…Therefore, a particular branch may be influenced to stop growing and to retract not only by inhibitory factors in its local environment, but also by strong competition from its more vigorously growing siblings. Indeed, in many developing systems, the retraction of some axonal branches has often been seen to be accompanied by growth of other branches (Innocenti, 1981;Stanfield and O'Leary, 1985;Gao and Macagno, 1987a,b;Jellies et al, 1987;Baptista and Macagno, 1988;Callaway and Katz, 1990;Lamantia and Rakic, 1990). Whether the outgrowth of some axonal branches does or does not contribute to the retraction of their sibling branches, however, has not been thoroughly tested experimentally thus far.…”

Local influence of substrate molecules in determining distinctive growth patterns of identified neurons in culture.

“…There, extensive branching of the axon and synapse formation occur. The axon can then continue to grow unbranched, through the segmental nerves to the skin, where again branching occurs, and sensory endings are formed (30)(31)(32) …”

Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech

“…Embryonic Hirudo were a generous gift from John Jellies, and reared in a breeding colony at the University of Western Michigan, MI, USA. Rearing, maintenance and dissection of these animals have been described elsewhere (Jellies et al, 1987;Jellies et al, 1993). Adult animals were anaesthetized on ice for 15·min before dissection in normal saline, containing (in mmol·l -1 ): 115.0 NaCl, 4.0 KCl, 1.8 CaCl 2 , 1.5 MgCl 2 , 10.0 dextrose, 10.0 Tris-maleate, pH 7.4 (Nicholls and Baylor, 1968).…”