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Journal of Neuroscience, Vol 12, 1454-1466, Copyright © 1992 by Society for Neuroscience
Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat
J Diamond, M Holmes and M Coughlin
Department of Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada.
We have investigated the co-involvement of endogenous NGF and impulses in
the collateral sprouting of cutaneous sensory nerves in adult rats,
specifically the A delta-axons involved in mechanonociception and the C-
fibers that mediate heat nociception. Their collateral sprouting was
measured by the progressive expansion, respectively, of the behaviorally
defined "pinch" and "heat" fields into surrounding denervated skin (the
light-touch A alpha-fibers do not sprout in adult mammals). The expansions
of such "isolated" fields were totally prevented in animals injected daily
with anti-NGF serum, but developed normally after treatment was
discontinued. Light microscopic and EM examination of the skin confirmed
that the effect of the anti-NGF treatment was attributable to its
prevention of collateral sprouting. Initiation of treatment would also
rapidly halt sprouting already in progress. Finally, intradermal injections
of purified NGF protein would not only increase the rate of nociceptive
fiber sprouting, but also evoke sprouting de novo within normally
innervated skin (again, A alpha- axons were unaffected). We conclude that
the collateral sprouting of intact nociceptive nerves following partial
denervation of skin is entirely dependent on endogenous NGF. The observed
latency of this sprouting was 10-12 d; we estimate, however, that at least
2 d of field expansion is required for its reliable detection. Thus, about
8-10 d are required for NGF levels in the skin to rise to effective levels,
and for the neurons to respond and initiate sprouting. From indirect
findings, the NGF component of this sprouting latency appears to be about 2
d. In accord with earlier findings, the remaining "initiation time" was
reduced by 5-6 d if the neurons were briefly excited, even 2 d prior to the
isolation of their fields. Unexpectedly, this phenomenon of "precocious
sprouting" requires that endogenous NGF be available; the sprouting latency
reverted to normal values when the conditioning impulses were evoked during
a 2 d anti-NGF "umbrella." In contrast to the impulse-sensitive neuronal
mechanisms involved in the initiation of sprouting, those underlying the
sprouting rate were unaffected by nerve activity and were entirely
dependent on the level of endogenous NGF. We suggest that interactions like
that revealed in these studies between a sprouting agent and impulses that
seem to prime the neuron's response to it contribute to plasticity within
the nervous system.
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|
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17(18):
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|
|
|
|
|
|
|
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17(14):
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|
|
|
|
|
|
|
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17(10):
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|
|
|
|
|
|
|
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17(7):
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[Full Text]
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|
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|
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267(5204):
1662 - 1666.
[Abstract]
[PDF]
|
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|
|
|
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1(1):
26 - 34.
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