Although pioneer neurons are the first to delineate the axon pathways, it is uncertain whether they have unique pathfinding abilities. As a first step in defining the role of pioneer neurons in the Drosophila embryonic CNS, we describe the temporal profile and trajectory of the axons of four pioneer neurons and show that they differ from previously published reports. We show, by targeted ablation of one, two, three or four pioneer neurons at a time, that (1) no single pioneer neuron is essential for axon tract formation, (2) the interaction between two pioneers is necessary for the establishment of each fascicle and (3) pioneer neurons function synergistically to establish the longitudinal axon tracts, to guide the fasciculation of follower neurons along specific fascicles and to prevent axons from crossing the midline.

REFERENCES

Bastiani
M. J.
,
du Lac
S.
,
Goodman
C. S.
(
1986
)
Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of a specific axonal pathways by the pCC neuron.
J. Neurosci
6
,
3518
3531
Bate
C. M.
(
1976
)
Pioneer neurones in an insect embryo.
Nature
260
,
54
55
Bate
C. M.
,
Grunewald
E. B.
(
1981
)
Embryogenesis of an insect nervous system II: A second class of neuron precursor cells and the origin of the intersegmental connectives.
J. Embryol. Exp. Morph
61
,
317
330
Bossing
T.
,
Udolph
G.
,
Doe
C. Q.
,
Technau
G. M.
(
1996
)
The Embryonic central-nervous-system lineages of Drosophila melanogaster. 1. Neuroblast lineages derived from the ventral half of the neuroectoderm.
Dev. Biol
179
,
41
64
Brand
A. H.
,
Perrimon
N.
(
1993
)
Targeted expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Callahan
C. A.
,
Thomas
J. B.
(
1994
)
Tau--galactosidase, an axon targeted fusion protein.
Proc. Natl. Acad. Sci. USA
91
,
5972
5976
Chitnis
A. B.
,
Kuwada
J. Y.
(
1991
)
Elimination of a brain tract increases errors in pathfinding by follower growth cones in the zebrafish embryo.
Neuron
7
,
277
285
du Lac
S.
,
Bastiani
M. J.
,
Goodman
C. S.
(
1986
)
Guidance of neuronal growth cones in the grasshopper embryo. II. Recognition of a specific axonal pathway by the aCC neuron.
J. Neurosci
6
,
3532
3541
Eisen
J. S.
(
1991
)
Motoneuronal development in the embryonic zebrafish.
Development
2
,
141
147
Eisen
J. S.
,
Myers
P. Z.
,
Westerfield
M.
(
1986
)
Pathway selection by growth cones of identified motoneurons in live zebra fish embryos.
Nature
320
,
269
271
Ghosh
A.
,
Antonini
A.
,
McConnell
S. K.
,
Shatz
C. J.
(
1990
)
Requirement for subplate neurons in the formation of thalamocortical connections.
Nature
347
,
179
181
Gong
Q.
,
Shipley
M. T.
(
1995
)
Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb.
Neuron
14
,
91
101
Grenningloh
G.
,
Rehm
E. J.
,
Goodman
C. S.
(
1991
)
Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule.
Cell
67
,
45
57
Hidalgo
A.
,
Urban
J.
,
Brand
A. H.
(
1995
)
Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS.
Development
121
,
3703
3712
Ho
R. K.
,
Goodman
C. S.
(
1982
)
Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos.
Nature
297
,
404
406
Jacobs
J. R.
,
Goodman
C. S.
(
1989
)
Embryonic development of axon pathways in the Drosophila CNS. II. Behavior of pioneer growth cones.
J. Neurosci
9
,
2412
2422
Keshishian
H.
,
Bentley
D.
(
1983
)
Embryogenesis of peripheral nerve pathways in grasshopper legs. III. Development without pioneer neurons.
Dev. Biol
96
,
116
124
Keynes
R.
,
Cook
G. M. W.
(
1995
)
Axon guidance molecules.
Cell
83
,
161
169
Klose
M.
,
Bentley
D.
(
1989
)
Transient pioneer neurons are essential for formation of an embryonic peripheral nerve.
Science
245
,
982
984
Lin
D. M.
,
Auld
V. J.
,
Goodman
C. S.
(
1995
)
Targeted neuronal cell ablation in the Drosophila embryo: pathfinding by follower growth cones in the absence of pioneers.
Neuron
14
,
707
715
Lin
D. M.
,
Fetter
R. D.
,
Kopczynski
C.
,
Grenningloh
G.
,
Goodman
C. S.
(
1994
)
Genetic analysis of fasciclin II in Drosophila: defasciculation, refasciculation and altered fasciculation.
Neuron
13
,
1055
1069
Passani
M. B.
,
Peinado
A.
,
Engelman
H.
,
Baptista
C. A.
,
Macagno
E. R.
(
1991
)
Normally unused positional cues guide ectopic afferents in the leech CNS.
J. Neurosci
11
,
3868
3876
Pike
S. H.
,
Melancon
E. F.
,
Eisen
J. S.
(
1992
)
Pathfinding by zebrafish motoneurons in the absence of normal pioneer axons.
Development
114
,
825
831
Raper
J. A.
,
Bastiani
M. J.
,
Goodman
C. S.
(
1984
)
Pathfinding by neuronal growth cones in grasshopper embryos. IV. The effects of ablating the A and P axons upon the behavior of the G growth cone.
The. J. Neurosci
4
,
2329
2345
Seeger
M.
,
Tear
G.
,
Ferres-Marco
D.
,
Goodman
C. S.
(
1993
)
Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward and away from the midline.
Neuron
10
,
409
426
Tix
S.
,
Bate
M.
,
Technau
G. M.
(
1989
)
Pre-existing neuronal pathways in the leg imaginal disks of Drosophila.
Development
107
,
855
862
This content is only available via PDF.