Journal of Neuroscience, Vol 15, 3254-3262, Copyright © 1995 by Society for Neuroscience
Developing neurons use a putative pioneer's peripheral arbor to establish their terminal fields
WB Gan and ER Macagno
Department of Biological Sciences, Columbia University, New York, New York 10027, USA.
Pioneer neurons are known to guide later developing neurons during the
initial phases of axonal outgrowth. To determine whether they are also
important in the formation of terminal fields by the follower cells, we
studied the role of a putative leech pioneer neuron, the pressure-
sensitive (PD) neuron, in the establishment of other neurons' peripheral
arbors. The PD neuron has a major axon that exits from its segmental
ganglion to grow along the dorsal-posterior (DP) nerve to the dorsal body
wall, where it arborizes extensively mainly in its own segment. It also has
two minor axons that project to the two adjacent segments but branch to a
lesser degree. We found that the peripheral projections of several later
developing neurons, including the AP motor neuron and the TD sensory
neuron, followed, with great precision, the major axon and peripheral arbor
of the consegmental PD neuron, up to its fourth-order branches. When a PD
neuron was ablated before it had grown to the body wall, the AP and TD
axons grew normally toward and reached the target area, but then formed
terminal arbors that were greatly reduced in size and abnormal in
morphology. Further, if the ablation of a PD neuron was accompanied by the
induction, in the same segment, of greater outgrowth of the minor axon of a
PD neuron from the adjacent segment, the arbors of the same AP neurons grew
along these novel PD neuron branches. These results demonstrate that the
peripheral arbor of a PD neuron is a both necessary and sufficient template
for the formation of normal terminal fields by certain later growing
follower neurons.