Journal of Neuroscience, Vol 15, 3243-3253, Copyright © 1995 by Society for Neuroscience
Interactions between segmental homologs and between isoneuronal branches guide the formation of sensory terminal fields
WB Gan and ER Macagno
Department of Biological Sciences, Columbia University, New York, New York 10027, USA.
Process outgrowth and peripheral field innervation by an identified
mechanosensory neuron were examined in the intact embryonic leech. The
dorsal pressure-sensitive (PD) neurons of the leech CNS are found as
bilateral pairs in every segmental ganglion, and are amenable to study at
early ages in intact embryos. Each PD has one major axonal projection that
putatively pioneers the nerve to the dorsal body wall and branches
extensively in its own segment, and two minor projections that innervate,
via neighboring ganglia, smaller areas in adjacent segments. We found that
adjacent embryonic PD cells form overlapping terminal fields in the body
wall, but that the extent of overlap was governed by inhibitory
interactions among these fields. When one PD neuron was ablated, the
adjacent PD cell changed its peripheral arborization by (1) its major axon
producing more filopodia and extending longer side branches toward the
ablated cell and (2) its minor axon producing a large arbor in the operated
segment. Interestingly, although growth was biased toward the side of the
ablated neuron, reduced outgrowth of the PD cell was found on the side away
from the ablation, while the total extent of arborization of the PD cell
kept relatively constant. Further, we found that axotomy of the major PD
projection resulted in extensive outgrowth of its minor projections. These
results suggest that a single PD neuron has a limited capacity for growth,
each of its branches growing at the expense of the others, and that
inhibitory interactions between neighboring PD neurons influence the extent
and direction of that growth.