Development and pathway formation of peripheral neurons during leech embryogenesis

Abstract

By labeling the germinal plates of staged leech embryos with monoclonal antibodies to the immunoglobulin superfamily member Tractin, we have documented the distribution and initial development of peripheral neurons in a hirudinid leech. We find, in addition to sensillar and extrasensillar sensory neurons, that there are 21 identifiable peripheral neurons in each hemisegment. These neurons are found in highly stereotyped positions, and all but two of them are associated with the segmental nerves. We show that eight of the peripheral neurons have the characteristic morphology of stretch receptor neurons and that they form a circumferentially distributed grid aligned in such a way that each of five specialized longitudinal muscle fascicles are monitored by at least two stretch receptor cells covering ventral, lateral, and dorsal regions of the body wall. Furthermore, we show that, in contrast to the dorsal posterior nerve, which is pioneered by central projections, the pathways of the three remaining segmental nerves are likely to be pioneered or guided by peripheral neurons.

Leech filamin and Tractin: Markers for muscle development and nerve formation

“…Figure 7 shows confocal images from three consecutive hemisegments of an Hirudo E9 embryo double labeled with Tractin (red) and ACT (green) antibody. Tractin immunoreactivity has hitherto only been reported for neuronal somata and axons (Huang et al, 1997(Huang et al, , 1998 and this is the first documentation of localization outside the nervous system. The P d axon (in yellow because it is labeled by both Tractin and ACT antibody) clearly navigates along a Tractin antibody-labeled surface in the same confocal plan as the axon.…”

“…Three of these (AA, MA, and PP) are pioneered by peripheral neurons differentiating within the body wall ( Fig. 4) (Jellies et al, 1996;Huang et al, 1998). However, the fourth nerve (DP) follows a completely different trajectory and is aligned with the dorsoventral flattener muscles [ Fig.…”

Ectopic CNS Projections Guide Peripheral Neuron Axons along Novel Pathways in Leech Embryos

“…Scale bar, 85 m. ever, all the known groups of peripheral neurons continue to develop and extend axons. In addition to the sensillar and extrasensillar sensory neurons specifically labeled by Lan3-2, the ACT antibody selectively labels 21 peripheral neurons present in each hemisegment (Huang et al, 1998). In this study we have directly examined the interactions between the axons of the two groups of Lan3-2 and ACT antibody-positive peripheral neurons in the absence of the CNS by antibody double-labeling experiments.…”

“…In this study we have directly examined the interactions between the axons of the two groups of Lan3-2 and ACT antibody-positive peripheral neurons in the absence of the CNS by antibody double-labeling experiments. The most prominent of the ACT-positive peripheral neurons are the nephridial nerve cell (NNC), the eight stretch receptor neurons (HO or "Hoover" cells), and the seven neurons making up the anterior root ganglion (ARG) (Huang et al, 1998). As shown in Figs.…”

“…This kind of strategy is particularly well suited to ensure the formation of common nerve pathways between afferent and efferent projections. We have studied these aspects of nerve development in leech embryos in which the four major segmental nerves per hemisegment contain axons from both peripheral and central neurons and established that three of these nerves (aa, ma, and pp) are pioneered by peripheral neurons, whereas the fourth nerve (dp) is pioneered by central neurons (Jellies et al, 1994(Jellies et al, , 1996Huang et al, 1998).…”