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Journal of Neuroscience, Vol 12, 619-634, Copyright © 1992 by Society for Neuroscience
Cerebellar target neurons provide a stop signal for afferent neurite extension in vitro
DH Baird, ME Hatten and CA Mason
Department of Pathology, Columbia University, College of Physicians and Surgeons, New York, New York 10032.
The contributions of cell-cell interactions to the establishment of
specific patterns of innervation within target brain regions are not known.
To provide an experimental analysis of the regulation of afferent axonal
growth, we have developed an in vitro assay system, based on the developing
mouse cerebellum, in which afferent axons from a brainstem source of mossy
fiber afferents, the basilar pontine nuclei, were cocultured with astroglia
or granule neurons purified from the cerebellum. In the absence of cells
from the cerebellum, pontine explants produced axons that fasciculated and
extended rapidly on a culture surface treated with poly-lysine or laminin.
When pontine neurites grew onto cerebellar astroglial cells, outgrowth was
more abundant than on substrates alone, suggesting that glial cells provide
a positive signal for axon extension. Time-lapse video microscopy indicated
that the rate of neurite extension increased from less than 50 microns/hr
to more than 100 microns/hr when axonal growth cones moved from the culture
substratum onto an astroglial-cell surface. Acceleration of neurite
extension was also observed as pontine neurites grew onto other pontine
neurites. By contrast, when pontine neurites grew on granule neurons, the
appropriate targets of mossy fibers, the length of pontine neurites was
greatly reduced. As growing axons terminated on granule neurons, the target
cells appeared to provide a "stop-growing signal" for axon extension. The
length of pontine neurites decreased with increasing granule neuron
density. Two lines of evidence suggested that the stop signal was contact
mediated. First, video microscopy showed that pontine growth cones stopped
extending after contacting a granule neuron. Second, the length of afferent
axons was not reduced when pontine neurites grew at a distance from granule
neurons. Competition experiments where both astroglia and granule neurons
were plated together suggested that the growth arrest signal provided by
granule neurons could override the growth-promoting signal provided by
astroglial cells. These results suggest that specific cell- cell
interactions regulate the growth of pontine afferent axons within their
cerebellar target, with axoaxonal and axoglial interactions promoting axon
extension and axon-target cell interactions interrupting axon extension.
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