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Journal of Neuroscience, Vol 4, 1715-1735, Copyright © 1984 by Society for Neuroscience
Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons
CA Mason and E Gregory
We have studied the form and fine structure of developing afferent axons in
postnatal mouse cerebellum, before and during the formation of synaptic
connections. In slices of fresh brain, bundles of axons were injected with
horseradish peroxidase (HRP), and individual axons were examined in the
light and electron microscopes. At birth, before formation of cortical
layers, axons with growing tips are rare in the peduncular tracts but
instead ramify throughout the cerebellar anlage. All axons have similar
structures; they branch infrequently and terminate in bud-like tips and/or
small growth cones. Growth cones contain small and large vesicles in the
flank and small vesicles in filopodia. Typical mossy and climbing fiber
branching patterns and bouton shapes are recognizable after postnatal day
(P) 5, even though fibers are still intermingled in a plexus beneath the
newly formed Purkinje cell layer. Climbing fiber-like axon arbors are
highly branched and covered with small foliate growing tips that contact
Purkinje cells. Mossy fiber-like branches have large irregular expansions
that give rise to long filopodia and resemble growth cones seen in vitro.
The flanks of these growth cones contact granule cell dendrites and form
glomeruli typical of mossy fibers, whereas the filopodia make primitive
contacts or are associated with coated vesicles in adjacent profiles. A
novel finding is the occurrence during the second postnatal week of many
single axons that simultaneously have the morphology and synaptic
connections of both climbing and mossy fibers. These "combination" axons
have some branches that extend into the granule cell layer and others that
enter the Purkinje cell layer, with the shape and synaptic connections of
terminals on each branch type corresponding to the respective layer.
Climbing fiber-like branches, including those on combination fibers, extend
over several adjacent Purkinje cells. Combination fibers are rare in late
postnatal or adult stages. These results suggest that long after arrival in
the cerebellum, afferent axons have similar elementary forms and overlap in
their projections. Mature axonal forms are not exhibited until cellular
layers develop. During a limited period of postnatal maturation, some axons
have dual morphologies and synaptic relations with appropriate and
inappropriate partners. These aspects of cerebellar axonal development,
particularly the transient exuberant branching onto two types of target
cells, offer a valuable opportunity to examine, in developing cerebellum,
the sorting out of afferents and the formation of specific synaptic
connections.
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