The Journal of Neuroscience, September 1, 1998, 18(17):6840-6852
Trigeminal Ganglion Axons Are Repelled By Their Presumptive
Targets
M. William
Rochlin and
Albert I.
Farbman
Department of Neurobiology and Physiology, Northwestern University,
Evanston, Illinois 60208-3520
Previous work suggested that in mouse, presumptive targets of the
trigeminal ganglion, rather than intermediate structures, attract
pioneer axons from the time their growth cones exit the ganglion
(). In rat we find that some presumptive
targets repel trigeminal axons. The repellant activity is concentrated
in the anterior and ventral epithelium of the mandibular arch at
embryonic day 12 (E12) and was also present in the maxillary arch. The
activity is blocked by anti-neuropilin-1. E13 mandible explants repel
trigeminal axons during the first day of outgrowth in
vitro, but thereafter permit or attract trigeminal ganglion
axon outgrowth. By E14, lingual nerve afferents first enter the tongue
in vivo, and the repellant influence becomes restricted
to the midline. The progressive restriction of the repellant influence
may contribute to the in vivo progression of nerve
development: the earliest afferents turn anteriorly lateral to the
tongue, but subsequently arriving afferents advance into the tongue and
then turn away from the midline. Thus, the repellant may influence the
order of nerve branch development and the timing of innervation of
epithelial and subepithelial targets. Heterochronic studies revealed
that the loss of repellant influence from presumptive lateral tongue
surface results from downregulation of the repellant activity, not of
responsiveness to the repellant. Because presumptive targets repel
trigeminal axons during the initial stages of advance from the
trigeminal ganglion and do not have a net attractive influence until
after afferents have arrived near the target, intermediate structures
must guide these axons initially.
Key words:
chemorepellant; chemoattractant; axon guidance; peripheral nervous system; trigeminal ganglion; mandible; development; neuropilin-1; semaphorin III/D
Copyright © 1998 Society for Neuroscience 0270-6474/98/18176840-13$05.00/0